Aboitiz, F & Al -Language Origins - Catalogo- 3-5906 (0117) IMPRESION PENDIENTE

7/28/2019 Aboitiz, F & Al -Language Origins - Catalogo- 3-5906 (0117) IMPRESION PENDIENTE

http://slidepdf.com/reader/full/aboitiz-f-al-language-origins-catalogo-3-5906-0117-impresion-pendiente 1/17

Brain and Language 98 (2006) 40–56

www.elsevier.com/locate/b&l

0093-934X/$ - see front matter © 2006 Elsevier Inc. All rights reserved.

doi:10.1016/j.bandl.2006.01.006

Cortical memory mechanisms and language origins

Francisco Aboitiz ¤, Ricardo R. García, Conrado Bosman, Enzo Brunetti

Depto. Psiquiatría, Facultad de Medicina, Ponti Wcia Universidad Católica de Chile, Marcoleta no. 387 2o piso, Casilla 114-D Santiago 1, Chile

Accepted 12 January 2006

Available online 14 February 2006

Abstract

We have previously proposed that cortical auditory-vocal networks of the monkey brain can be partly homologized with language

networks that participate in the phonological loop. In this paper, we suggest that other linguistic phenomena like semantic and syntactic

processing also rely on the activation of transient memory networks, which can be compared to active memory networks in the primate.

Consequently, short-term cortical memory ensembles that participate in language processing can be phylogenetically tracked to more

simple networks present in the primate brain, which became increasingly complex in hominid evolution. This perspective is discussed in

the context of two current interpretations of language origins, the “mirror-system hypothesis” and generativist grammar.

© 2006 Elsevier Inc. All rights reserved.

Keywords: Broca’s area; Mirror neurons; Syntax; Wernicke’s area; Working memory

1. Introduction

In the last decade, there has been a growing interest in

short-term memory phenomena that maintain the neuronal

activation related to perceptual or long-term mnemonic

items, in order to execute a near-future response (Fuster,

1995a; Fuster & Alexander, 1971; Levy & Goldman-Rakic,

2000). In humans, this kind of memory has been termed

working memory (Baddeley, 1992; Baddeley & Hitch,

1974), and has been proposed to participate in several cog-

nitive mechanisms, including language acquisition and pro-

cessing (Baddeley, 1992, 2000, 2003; Baddeley, Papagno, &

Vallar, 1988; Caplan, Alpert, & Waters, 1998; Caplan,

Alpert, Waters, & Olivieri, 2000; Fiebach, Schelewsky, &Friederici, 2002; Fiebach, Schlesewsky, Lohmann, von Cra-

mon, & Friederici, 2005; Gathercole & Baddeley, 1990;

Gibson, 1998; Just & Carpenter, 1992; King & Kutas, 1995;

Müller & Basho, 2004). Furthermore, cognitive and neuro-

biological evidence suggests that the distinct aspects of lan-

guage processing, including phonological, lexical, semantic,

and syntactic domains, all rely importantly on short-term

memory mechanisms (Bookheimer, 2002; Caplan &

Waters, 1999; Hickock & Poeppel, 2000; Lieberman, 2002).

Working memory has been classically subdivided into a

general, all-purpose executive system that manipulates the

mnemonic items, and “slave” systems involved in sensori-

motor rehearsal. The latter have been further subdivided

into a visuospatial sketchpad, which maintains online visu-

ospatial information, and a phonological loop, that allows

internal rehearsal of phonological utterances (Baddeley &

Hitch, 1974). SpeciWcally, in humans, the phonological loop

has been anatomically identiWed (see below) and shown to

be important for language learning. For example, patients

with phonological working memory deWcits show impair-ments in long-term phonological learning, and a link has

been observed between performance in the phonological

loop and vocabulary level in children (Baddeley et al., 1988;

Gathercole & Baddeley, 1990). Furthermore, speciWc lan-

guage impairment, a developmental condition character-

ized by deWcits in language learning, appears to have as a

central characteristic a phonological working memory dys-

function (Webster & Shevell, 2004). According to Baddeley

(2000), this evidence suggests that the loop might have

evolved to enhance language acquisition.

* Corresponding author. Fax: +56 2 665 1951.

E-mail address: [email protected] (F. Aboitiz).

URL: http://www.neuro.cl (F. Aboitiz).

mailto:%[email protected]

http://www.neuro.cl/

http://www.neuro.cl/





F. Aboitiz et al. / Brain and Language 98 (2006) 40–56 41

However, cortical short-term memory mechanisms are

more diverse and involve other modalities or sensorimotor

domains than the phonological loop and the visuospatial

sketchpad (Fuster, 1995a). Furthermore, certain higher-

level cognitive phenomena such as attention also imply

short-term memory mechanisms that do not exactly Wt the

concept of “slave” sensorimotor systems (de Fockert, Rees,Frith, & Lavie, 2001). Although the concept of a central

executive that distributes resources in diV erent processing

domains might adequately grasp some of these phenomena,

the anatomical localization of this system in the dorsolat-

eral prefrontal cortex has been questioned by some authors

(Goldman-Rakic, 1996, 2000). Partly for this reason, we

consider that the more general, neurophysiological concept

of active memory (Fuster, 1995a; Fuster & Alexander,

1971) may be more appropriate in this context. This term

implies “a broad network of associative memory” which is

maintained “as a perceptual memory fragment in order to

execute a motor act in the near future” (Fuster, 1995b,

p. 64). In other words, active memory is a property of neu-

ronal ensembles that consists of the capacity to maintain an

activated state during the execution of a cognitive task, thus

holding information online for a brief time interval (Fuster,

1995a, 1995b). Nevertheless, more than being speciWc mem-

ory circuits, the above networks are elements that link sen-

sory and motor domains in the context of near-future

behavior. Furthermore, the fact that active memory ensem-

bles are associative as Fuster proposes implies that they are

changeable, plastic, and that these overlap and interact with

other active networks during the preparation and execution

of complex behaviors, thus generating larger ensembles

manipulating more than one memory item (for a more for-mal analysis, see Glassman, 2003). The mechanisms by

which these networks maintain their activated state are not

yet clear, but an intriguing possibility is that they do so

through the establishment of reciprocally connected ensem-

bles which oscillate synchronously (Engel, Fries, & Singer,

2001; Singer, 1999; Durstewitz, Seamans, & Sejnowski,

2000; Yuste, MacLean, Smith, & Lansner, 2005). There is

accumulating evidence indicating that neural synchrony

with a precision in the millisecond range participates in sev-

eral cognitive phenomena including working memory, in a

manner consistent with Hebb’s postulate of maintained

reciprocal activation. These studies show that short-term

storage mechanisms involve an increase in neural syn-

chrony between prefrontal cortex and posterior cortex,

together with enhancing the activation of long-term mem-

ory representations (Engel & Singer, 2001; Fingelkurts

et al., 2003; Palva, Palva, & Kaila, 2005; Ruchkin, Graf-

man, Cameron, & Berndt, 2003; Tallon-Baudry, Bertrand,

& Fischer, 2001; Tallon-Baudry, Mandon, Freiwald, &

Kreiter, 2004).

In this article, we propose (1) that the neural circuits that

participate in the phonological loop can be anatomically

described in incipient form in the non-human primate

brain, and that therefore these are homologous to the

human circuits (Aboitiz, 1995; Aboitiz & García, 1997);

and (2) that in part, language has evolved by virtue of an

expanding short-term memory capacity, which has allowed

the processing and manipulation of increasingly complex

sequences of sounds, conveying elaborate meanings and

eventually participating in syntactic processes. Thus, the

language-speciWc areas of the human brain may have ini-

tially evolved as a circuit for phonological rehearsalinvolved in learning relatively long phonological utter-

ances, which became conventionalized and acquired simple

meanings by associative interactions with other sensorimo-

tor domains. As the memory systems involved in this pro-

cess expanded, it became possible to activate more complex

memories representing several items that could be combi-

natorially manipulated (Glassman, 2003). This allowed

utterances and their meanings to become also increasingly

complex and speciWc. Eventually, primitive syntactic rules

appeared within the context of a highly intricate short-term

memory network that allowed to maintain previously per-

ceived lexical items on line while others were still being pro-

cessed. Although intuitively appealing, this proposal faces

other recent hypotheses. One of them is the “mirror-sys-

tem” hypothesis, which emphasizes the role of hand-grasp-

ing mirror neurons in language origins (Arbib & Bota,

2003; Rizzolatti & Arbib, 1998). Shortly, the hypothesis

suggests that the manual mirror-neuron system provided

the necessary plasticity for symbolic communication to

arise in a gestural domain, which was eventually overcome

by vocal communication. Although we feel that the concept

of mirror neurons is in general complementary to our

views, there are some points of disagreement which we will

discuss. Another proposal relates to Chomsky’s generativist

approach which claims that syntax, and speciWcally theoperation termed syntactic recursion (i.e., the ability to

recursively embed sentences within larger sentences; see

below), is the only faculty that is exclusive of human lan-

guage and unlikely to result from evolution by natural

selection (see Hauser, Chomsky, & Fitch, 2002). We claim

that linguistic recursion demands signiWcant working mem-

ory resources, and that at least partly, neural networks that

participate in recursion were gradually elaborated from

simpler networks involved in active memory in the primate

brain.

In the rest of the article, we will discuss evidence in favor

of our hypothesis. We will brieXy update evidence on the

location and connectivity of the human language areas and

of the phonological loop, and their presumed homologues

in the monkey. Then, we will face this evidence with the

mirror-system hypothesis. Finally, we will analyze the role

of short-term memory in syntactical processing, especially

in the case of recursive structures, and will propose a neuro-

biological substrate for it and its evolution.

2. Neuroanatomy of phonological working memory and

homologies between monkey and human

More than a century of analyses of focalized brain

lesions in humans has evidenced that cortical language



42 F. Aboitiz et al. / Brain and Language 98 (2006) 40–56

networks minimally consist of a posterior component sur-

rounding the temporoparietal junction of the left hemi-

sphere (Wernicke’s area), that mediates speech perception

and aspects of phonological production; an anterior com-

ponent that includes Brodmann’s areas 44 and 45 or

Broca’s area, which processes motor output and aspects

of syntax, and a connection between these two compo-nents, which includes the arcuate fasciculus (although

importantly, surrounding regions also participate; Dron-

kers, Shapiro, Redfern, & Knight, 1992; Dronkers, Wil-

kins, Van Valin, Redfern, & Jaeger, 2004). This scheme

has been conWrmed and expanded by analyses of stimula-

tion brain mapping which have established that regions

essential for language processing are usually restricted to

one hemisphere and tend to locate in temporal, inferior

parietal and inferior frontal areas (although there is sub-

stantial variance in individual patterns of localization;

Ojemann, 1991, 2003), and by several imaging studies to

be reviewed below. In earlier articles (Aboitiz, 1995; Abo-

itiz & García, 1997), we tentatively proposed a framework

for homology between the classical human language areas

and their primate counterparts, based on the available evi-

dence at that time (for example, Barbas & Pandya, 1989;

Preuss & Goldman-Rakic, 1991a, 1991b, 1991c), which

has been recently updated according to new evidence

(Aboitiz, García, Brunetti, & Bosman, in press) (see

Fig. 1).

The auditory cortex, both in the human and the

macaque, is organized in a series of concentric rings (core,

belt, and parabelt; Hackett, Stepniewska, & Kaas, 1998)

from which two main streams emerge: a ventral one, run-

ning through the anterior superior temporal gyrus, con-

veying information about the intrinsic features of auditory

stimuli (the “what” pathway); and a dorsal one, projecting

to the inferior parietal lobe and involved with spatial and

dynamic processing (the “where,” or movement pathway;

Kaas & Hackett, 1999; Tian, Reser, Durham, Kustov, &Rauschecker, 2001; Zatorre & Belin, 2001). These two

pathways project to diV erent regions of the prefrontal cor-

tex: in the macaque, the “where” pathway ends mainly in

dorsolateral prefrontal areas (areas 8 and 46) which in part

relate to eye movement control; and the “what” pathway

ends in more ventrolateral areas (mainly 12 and 45, the lat-

ter related to Broca’s area in humans; Hackett, Step-

niewska, & Kaas, 1999; Rauschecker & Tian, 2000;

Romanski, Tian, Mishkin, Goldman-Rakic, & Raushec-

ker, 1999; Romanski, Bates, & Goldman-Rakic, 1999).

There is evidence indicating that these temporo-frontal

circuits subserve performance in auditory working mem-

ory tasks (Gottlieb, Vaadia, & Abeles, 1989; Pasternak &

Greenlee, 2005). Interestingly, an auditory domain has

been identiWed in the macaque areas 12 and 45, in which

most neurons prefer vocalizations than other acoustic

stimuli, while some neurons were also responsive to visual

stimuli (Romanski & Goldman-Rakic, 2002; Romanski,

Averbeck, & Diltz, 2005). This domain receives projections

from the anterior lateral belt auditory area, which has

more selectivity to calls than the more caudal area (Raus-

checker & Tian, 2000; Tian et al., 2001). In this region, a

specialization of “what” and “where” streams in responses

to complex sounds and localizations has not been yet con-

Wrmed (Romanski et al., 2005), and it remains to be deter-mined whether the dorsal stream contributes a diV erent

auditory domain in more dorsal frontal regions. Another

line of evidence has been provided by Petrides and Pandya

(1984, 1988, 1999, 2001; see also Petrides, in press) , who

proposed a similar scheme to the above, in which area 45 is

subdivided into areas 45A and 45B, and describe a dys-

granular area 44, adjacent to area 45B. Nevertheless, these

authors describe some projections from caudal auditory

regions (for example, area Tpt) to ventrolateral prefrontal

areas, indicating a degree of overlap between the “where”

and “what” streams (Petrides & Pandya, 1988).

In parallel to the auditory “what” and “where” path-

ways, the visual system shows a separation between a ven-

tral stream along the inferior temporal lobe, related to

object processing; and a dorsal stream directed to the parie-

tal lobe, that is related to spatial behavior. These pathways

tend to segregate in the inferior and superior aspects of the

frontal lobe, respectively (Bullier, Schall, & Morel, 1996;

Felleman & Van Essen, 1991). Nevertheless, projections

from the inferior parietal regions reach the inferior frontal

cortex of the monkey, where they converge with projections

from inferior temporal areas subserving object information

(Fig. 1). More speciWcally, the intraparietal (area 7ip) and

inferior parietal (area 7b) regions project to the anterior

and the posterior banks of the inferior arcuate sulcus,

Fig. 1. Some connections that have been described from temporoparietal

regions to the lateral and inferior frontal cortex of the monkey. In the

superior temporal lobe, areas AI, R, and RT of the auditory cortex make

up the auditory core, while areas RTM, RM, and CM correspond to the

medial belt and areas RTL, AL, ML, and CL represent the lateral belt.

The lateral parabelt consists of areas RP and CP, while area Tpt may be

adjacent to these. The caudal parabelt projects to dorsolateral prefrontal

areas, while the rostral parabelt projects to ventrolateral prefrontal

regions. Area TE, in the anterior temporal lobe, is related to visual recog-

nition and projects to ventral lateral cortex. In the intraparietal and infe-

rior parietal lobe, areas 7ip and 7b, respectively, project to ventrolateral

regions of the frontal cortex, among other regions. Numbers in the frontal

cortex indicate the respective Brodmann’s areas. For further explanation,

see text.




respectively (Cavada & Goldman-Rakic, 1989; Petrides &

Pandya, 1984; Preuss & Goldman-Rakic, 1991a, 1991b,

1991c). Similarly, Petrides and Pandya (1984, 1999, 2001;

see also Petrides, in press) emphasize connections between

area 45 with the posterior inferior parietal lobe (area PG)

and area 44 with the intraparietal and anterior inferior

parietal lobe (areas AIP and PFG, respectively). Note thatperhaps more than spatial processing in the context of

behavioral orientation, inferior parietal regions participate

in tasks involving grasping and object manipulation (Riz-

zolatti & Arbib, 1998; see below). Their projections to the

inferior frontal lobe overlap with the object-processing

pathway from the inferior temporal lobe, contributing to

the integration of information between hand and object

(Nelissen, Luppino, VanduV el, Rizzolatti, & Orban, 2005).

As will be seen below, although the auditory dorsal path-

way (as said, roughly parallel to the visual parietal path-

way) is less likely to be involved in manipulative tasks, it

participates in processing the temporal dynamics of com-

plex sounds, which make it somewhat analogous to the

motion-sensitive regions of the parietal lobe.

In humans, a dorsal and a ventral stream for processing

sounds have also been identiWed (Belin & Zatorre, 2000;

Zatorre & Belin, 2001; see also Scott & Johnsrude, 2003). In

speech perception, the ventral stream participates in identi-

fying the speaker, while the dorsal stream is considered to

be primarily involved in perceiving the time-course of com-

plex sounds, a mechanism based on accurate time analysis

of spectral motion. This process might seem to be more

related to the “what” function of categorizing sounds, but

these authors claim that it is analogous to the function of

the motion-sensitive visual parietal area MT, in that thetime-course of the signal is an essential variable (Belin &

Zatorre, 2000; Zatorre & Belin, 2001). More than identify-

ing the speaker, this type of processing is especially well

suited to process complex vocalization sequences which

reXect motion of the vocal apparatus, and particularly

speech, where the time-course of the formant frequencies

contains most of the phonemic information. Romanski

et al. (2000) concur with these authors in that this general

form of ‘motion processing’ mechanism may be one of the

functions of the dorsal pathway, but can be used in service

of both auditory space perception and the perception of

complex vocalizations. Additional evidence indicates that

the temporal pathway for speech perception is subdivided

into a component directed along the supratemporal cortical

plane and linked to speech production rather than percep-

tion; and a component located in the posterior left superior

temporal sulcus, related to verbal recall (Wise et al., 2001).

The latter is considered to participate in verbal generation

and rehearsal (the phonological loop), and has been pro-

posed to participate in the acquisition of long-term memo-

ries of novel words. Finally, a recent study using diV usion

MRI tractography in humans detected both a ventral path-

way (via the uncinate fasciculus) and a dorsal pathway (via

the arcuate fasciculus and including connections with area

40 in the supramarginal gyrus), connecting the auditory

areas with the inferior frontal lobe (Parker et al., 2005).

Interestingly, these tracts were highly asymmetric, being

more robust on the left side.

Summarizing, the ventrolateral prefrontal region of the

monkey, including areas 44/45 (comparable to Broca’s

area), is a complex multimodal region receiving projections

from the auditory “what” stream (but also some projec-tions from the “where” stream), from the inferior temporal

region and from intraparietal/inferior parietal areas

(Fig. 1). In humans, anatomically similar regions have been

described to participate in the phonological loop, which

subserves phonological working memory. This loop has

been described to include a storage component located in

the left supramarginal gyrus of the inferior parietal lobe

(Brodmann’s area 40), and a rehearsal component involv-

ing Broca’s area (areas 44 and 45; Awh, Smith, & Jonides,

1995; Frackowiak, 1994; Habib, Demonet, & Frackowiak,

1996; Hickok, Buchsbaum, Humphries, & Muftuler, 2003;

Paulesu, Frith, & Frackowiak, 1993; Salmon et al., 1996;

see also reviews by Aboitiz & García, 1997; Baddeley, 2003;

Smith & Jonides, 1998). This is consistent with a recent

analysis of human cortical connectivity, indicating impor-

tant connections between Wernicke’s area and area 40

(Parker et al., 2005). More extensive evidence from lesion

studies has conWrmed that parietal lesions in humans lead

to sentence comprehension deWcits, by virtue of a rehearsal

disorder related to the interruption of the parieto-frontal

phonological loop, as occurs in conduction aphasia (Dron-

kers et al., 2004; see also Aboitiz & García, 1997; Smith &

Jonides, 1998). Furthermore, electrical stimulation brain

mapping techniques during awake neurosurgery have

determined that sites essential for recent verbal memory of names tend to be located in temporo-parietal sites (related

with storage) and in inferior frontal sites (related with

retrieval) (Ojemann, 1978, 1991, 2003; Ojemann & Mateer,

1979).

Based on this kind of evidence, we proposed that the supe-

rior temporal–inferior parietal–ventrolateral prefrontal path-

way that participates in the phonological loop could be

incipiently present in the non-human primate. In hominid

evolution, this pathway may have further diV erentiated into

a complex phonological device, involved in learning complex

vocal utterances by imitation and setting a Wrst stage in the

diV erentiation of language-speciWc areas in the left hemi-

sphere of the human brain (Aboitiz, 1995; Aboitiz & García,

1997; see also Fitch, 2000). The ventral auditory stream pos-

sibly represents a more ancient component of the vocaliza-

tion sensorimotor system, whose main function could be to

identify and assess the condition of the caller. As mentioned,

recent evidence suggests that in macaques this pathway is

more related to vocalizations than the dorsal stream, which

participates in spatial orienting for action (Romanski et al.,

2005). However, in primitive hominids in which vocalizations

became more plastic and conveyed longer and more elabo-

rate messages, the dorsal stream became progressively

involved in processing complex sequences of vocalizations,

recruiting inferior parietal areas (Aboitiz & García, 1997).




The occipito-temporoparietal junction is an evolutionarily

expanding cortical region, and its growth may have facili-

tated the development of the dorsal auditory pathway and

the phonological loop. SpeciWcally, areas 40 and 39 of the

human inferior parietal lobe are probably new in phylogeny,

as they were not identiWed in the monkey (Brodmann, 1909).

(Nevertheless, it is not entirely clear that they are absent inthe chimpanzee; Gannon, Kheck, Braun, & Holloway, 2005.)

Furthermore, these areas were described to have “no sharp

boundaries” with the temporal region (with areas 22 and 37,

respectively; Brodmann, 1909). This suggests anatomical and

functional continuity between posterior temporal areas and

inferior parietal regions in humans, which is conWrmed by the

recently observed connections between Wernicke’s region

and area 40 (Parker et al., 2005). Thus, we claim that

although the human phonological loop may include new cor-

tical areas and connections, it derives from a preexisting

auditory-inferior frontal circuit that is present in the non-

human primate.

3. The phonological loop and mirror neurons

The working memory hypothesis has not been the only

neurobiological proposal to explain early language evolu-

tion. Based on the discovery of mirror neurons for grasping

(which become active both when performing the action and

when observing it) in a circuit involving the anterior intra-

parietal area and area F5c of the monkey ventrolateral pre-

frontal region, Rizzolatti and Arbib (1998), and later Arbib

and Bota (2003) and Arbib (2005) developed another

hypothesis for language origins. Considering the overlap of

these networks with the homologues of language-speciWcregions, the potential role of these neurons in imitative pro-

cesses (see also Miklósi, 1999; Rizzolatti & Arbib, 1999),

and the fact that in monkeys, vocalizations have little vol-

untary control, they claimed that the grasping mirror sys-

tem provided the scaV olding for imitative behavior and

voluntary control over communication. They proposed a

sequence of events for language origins starting from an

imitation system for grasping, followed by the elaboration

of complex gestural communication in which pantomime

permits to assign a primitive, conventionalized reference

system to speciWc gestures. This mode of communication

develops into a conventionalized manual-based communi-cation system (protosign) that disambiguates the contents

of pantomime. Subsequently, the manual communication

system evolves into “protospeech,” which gives the vocal

apparatus suYcient Xexibility, and eventually language

originates. In other words, the hand-based parieto-prefron-

tal imitation system provided the behavioral plasticity nec-

essary to generate a diversity of vocalizations which could

evolve into language. A related hypothesis has been put for-

ward by Corballis (2003), who claims that there was an ini-

tial stage in which communication was mainly vocal, then

became gestural and acquired symbolic characteristics, and

Wnally became vocal again. These hypotheses have been

partly supported by the observation of a mirror system in

relation to sounds caused by actions (Kohler et al., 2002;

see also Pizzamiglio et al., 2005), and in cells representing

lip and mouth movements (Ferrari, Gallese, Rizzolatti, &

Fogassi, 2003). The latter are especially important in the

context of a recent report indicating that the macaque area

44 is involved in orofacial motor responses, with only a few

neurons responding to combined manual and orofacialresponses (there was only one penetration site for combined

responses out of eight sites with orofacial speciWcity; Pet-

rides, Cadoret, & Mackey, 2005). Interestingly, chimpan-

zees are able to match vocalizations to gesturing faces, thus

visually recognizing other vocalizing individuals and assess-

ing their social situation (Izumi & Kojima, 2004). Although

this form of cross-modal capacity is considered to involve

widespread frontal, inferior parietal, and posterior tempo-

ral regions (Calvert et al., 1999), it may also be related to

associations between orofacial mirror neurons and vocali-

zation-sensitive neurons in the inferior frontal region.

Furthermore, a mirror system has been proposed to be

involved in the generation of primitive concepts that serve

as cognitive requisites for a lexicon of action-related utter-

ances (Gallese, 2003), and evidence indicates that hand-ges-

turing is related to conceptual learning (Goldin-Meadow &

Wagner, 2005). There is also evidence of overlap between

Broca’s area and the frontal representation of actions.

Areas 44 and 45 have been observed to be active during

action observation in humans (Rizzolatti & Craighero,

2004), and a recent report in the monkey indicates that area

45 is a region in which the integration of object and action

information occurs, which may have served as a prelinguis-

tic link between verb and object (Nelissen et al., 2005). A

related interpretation is that in humans, area 44 is moreinvolved in linguistic and non-linguistic communication

processes that are expressed in the control of various

aspects of the body, especially orofacial movements; while

area 45 relates more closely to syntactic and semantic pro-

cesses that are not directly expressed in motor control (Pet-

rides, in press; Petrides et al., 2005; nevertheless, other

evidence points to a role of human area 44 in syntactical

and phonological working memory; Fiebach et al., 2005).

Other lines of evidence also support a close relation

between hand control and communication ability. In pri-

mates, there is a clear relation between handedness and lan-

guage lateralization. Most apes tend to be right-handed,

even for hand-signing (Hopkins & Leavens, 1998; Hopkins

et al., 2005), and the perception of vocalizations is lateral-

ized to the left hemisphere at least in monkeys (Hamilton &

Vermeire, 1988). Aphasic patients and stutterers seem to

beneWt from pointing and from hand gestures (Hanlon,

Brown, & Gerstmen, 1990; Mayberry, Jacques, & DeDe,

1998), although it is not yet clear whether they do so simply

because a manual system is the only one they have avail-

able. Finally, pointing is a behavior that may originally

derive from a grasping action, has a clear communicative

intention, and appears in children before speech (Feyere-

sien & Havard, 1999), which underlines the interdepen-

dence between gestural and vocal communication.




The concepts of a mirror system and of the role of imita-

tion in language origins are quite complementary to our

proposals (see also Arbib, 2005). We consider that gestural

and vocal communication coevolved to a large extent, and

have already put emphasis on the development of imitative

abilities in early language evolution (see Aboitiz & García,

1997; Aboitiz, García, Brunetti, & Bosman, 2005; Bosman,García, & Aboitiz, 2004; Bosman, López, & Aboitiz, 2005).

Nevertheless, we are somewhat cautious about the necessity

to postulate a speciWc stage in which gestural, signing lan-

guage was the main modality of symbolic communication,

that preceded the origin of speech. In the next section, we

will discuss this issue in some detail.

4. Vocalizations and gestures in non-human primates

A Wrst question in relation to the hand-signing hypothesis

is concerned with how relevant is signing versus vocaliza-

tions in primates. Some authors claim that in wild non-

human primates including chimpanzees, spontaneous

hand-signing is more limited than vocal communication

(Acardi, 2003; Seyfarth & Cheney, 2003), which is compati-

ble with a continuity in vocal communication in human

evolution. Other studies have indicated that chimpanzees

and other apes engage in both gestural and vocal communi-

cation, with vocal communication being more common in

arboreal species (who have less visual contact) and in

instances in which there is no eye contact, and gestural

communication is more common in terrestrial species and

in instances of social proximity (Pika, Liebal, Call, & Tom-

asello, in press; Vogel, 1999; Hostetter, Cantero, & Hop-

kins, 2001 for studies in captive chimpanzees).Furthermore, ape vocalizations tend to be highly ritualized

and related to evolutionarily urgent behaviors, such as

defense, food Wnding, and group traveling, while gestures

are performed in less stringent situations such as playing,

and used quite Xexibly (Acardi, 2000; Liebal, Call, & Toma-

sello, 2004; Pika et al., in press). There is evidence of

regional variability in the types of vocalizations emitted by

wild chimpanzees, but this has been considered to depend

on ecological factors and diV erences in body size rather

than on social learning (Mitani, Hunley, & Murdoch, 1999).

However, in populations of captive chimpanzees, group

diV

erences in vocalizations have been attributed to sociallearning since individuals within each group have diV erent

origins but nevertheless have little within-group variability

and high intergroup variability (Marshall, Wrangham, &

Acardi, 1999). Direct reference to objects or situations has

been hard to evidence, both in gestural or vocal communi-

cation, but there is some evidence of referential gestures in

relation to food (Pika et al., in press), and of the use of gaze

alternation between the referred object (usually food) and a

human experimenter (Leavens & Hopkins, 1998; Leavens,

Hopkins, & Thomas, 2004). Although in vocal communica-

tion there is even less evidence for referential communica-

tion, it has been observed that bonobos (a variety of

chimpanzee) are able to produce acoustically distinct

screams during agonistic interactions, depending on the

role they play in conXict (victim versus aggressor). The

authors suggest that these scream variants are promising

candidates for functioning as referential signals (Slocombe

& Zuberbuhler, 2005). Summarizing, although there is both

vocal and gestural communication in non-human primates,

in neither case they use symbols of the human kind (Pikaet al., in press). Thus, both modalities of communication are

equally distant from human language. Although gestural

communication is more plastic, vocal communication has

in its favor that it uses the same sensorimotor circuit as spo-

ken language (which is a strong argument for its evolution-

ary continuity), and as will be discussed below, making this

system more plastic would not be a diYcult evolutionary

step.

The fact that apes can be taught on sign language and

not on vocal communication has been claimed to support

the notion that non-human primates lack the required vol-

untary control over vocalizations. Therefore, speech may

have not evolved without the aid of the hand-grasping sys-

tem (Corballis, 2003). It seems that in this reasoning, a lim-

ited capacity for ontogenetic learning is being used as an

argument precluding the possibility of phylogenetic change

towards increasing plasticity and voluntary control. In our

view this makes little evolutionary sense. There is no a pri-

ori reason why a selective trend could not have originated

towards increasing plasticity and control of the vocal tract,

leading to the same or even more behavioral Xexibility

(including combinatorial abilities) than that observed in

hand coordination. Vocal imitation and plasticity has been

observed in species such as elephants, seals, and dolphins

(Janik, 2000; Poole, Tyack, Stoeger-Horwath, & Watwood,2005; Shapiro, Slater, & Janik, 2004), suggesting that a

hand-grasping system is not a prerequisite for the acquisi-

tion of voluntary control of the vocal system and imitative

capacity (elephants have a grasping trunk, but what about

seals and dolphins?). More generally, in animals, mirror

neurons and the ability to recognize and imitate actions

may not be restricted to the hand-grasping system (Bosman

et al., 2004; Miklósi, 1999). Thus, we concur with Rizzolatti

and Arbib (1999) in that “the F5 ‘mirror’ mechanism repre-

sents a particular variant of an ancient mechanism that

underlies a variety of behaviors” (p.152).

5. The neural substrates

Let us examine more closely the neuroanatomical and

neurophysiological control of the vocal apparatus. Arbib

and Bota (2003) assert that in non-human primates, the

cortical control of vocalizations is strongly dependent on

the anterior cingulate, while the homologue of human

Broca’s area is proposed to be related to hand control, with

its extensive connections with the inferior parietal lobe.

First, we would like to point that cingulate control for

vocalizations is found in monkeys and humans, and in both

cases its function has to do with motivation rather than

processing (Aboitiz et al., 2005; Paus, 2001). A second issue




relates to the proposed role of the inferior parietal lobe in

both hand control and human linguistic processes (Rizzol-

atti & Arbib, 1998). We already mentioned that the inferior

parietal regions (including area 40) of the human are prob-

ably more complex than the monkey inferior parietal and

intraparietal areas (Castiello, 2005). Furthermore, in

humans, the functions of hand control and linguistic pro-cessing could be segregated in the inferior parietal lobe.

Patients with circumscribed lesions of areas 39 and 40 show

severe deWcits for imitation of meaningless gestures (Gold-

enberg, 1997; Goldenberg & Hagmann, 1997). An imaging

study indicated area 40 and parietal area MT/V5 in imita-

tion of hand postures (Goldenberg, 2001), although

another report found activation only in area MT/V5 (Peig-

neux et al., 2000). A more recent analysis of visually guided

grasping detected activity in the anterior intraparietal sul-

cus, involving mostly the dorsal aspect of area 40 (Frey,

Vinton, Norlund, & Grafton, 2005; see also Castiello, 2005).

On the other hand, the phonological storage function

involves mainly the more ventral supramarginal gyrus

(Smith & Jonides, 1998).

The third issue in this context relates to the role of the

inferior frontal areas in hand grasping and language pro-

cessing. As mentioned, there is human evidence suggesting

that the representation of these functions overlaps in this

region (Rizzolatti & Craighero, 2004). In the monkey, area

45 has been shown to participate in the recognition of hand

grasping (Nelissen et al., 2005), but the study by Petrides

et al. (2005) indicates that area 44 is almost devoid of hand-

grasping neurons but rather contains orofacial motor neu-

rons. More importantly, exponents of the hand-signing

hypothesis have underlined the presumed absence of volun-tary, prefrontal control over vocalizations in monkeys,

which would suggest that these areas are mainly related to

hand control (Arbib & Bota, 2003; Corballis, 2003). How-

ever, as we mentioned above, the ventrolateral prefrontal

cortex of monkeys contains a vocalization-sensitive domain

(Romanski & Goldman-Rakic, 2002; Romanski et al.,

2005) and a motor representation of the larynx (Jürgens,

2003). Electrical stimulation of the latter can elicit vocal

fold movements (Hast, Fischer, Wetzel, & Thompson,

1974), and cortical lesions in the supplementary motor area

can signiWcantly reduce the total number of vocalizations

emitted by monkeys (Gemba, Miki, & Sasaki, 1997; Kirzin-

ger & Jürgens, 1982), indicating a degree of prefrontal con-

trol over the vocal apparatus. Previously, we suggested that

the prefrontal, vocalization-sensitive neurons described

above represent the phylogenetic precursors of a vocaliza-

tion mirror system (Bosman et al., 2004). All that is needed

is that these neurons participate in articulatory processes,

which would not be a diYcult evolutionary step. An elabo-

ration of this auditory-vocalization circuit may have been

suYcient to develop imitative vocal behavior, leading to an

incipient phonological loop. In humans, a fronto-parietal-

temporal network that responds both to perception and

oral production of sounds including speech and tonal pro-

duction has been identiWed (Hickok et al., 2003), and a

recent fMRI study has demonstrated that listening to

speech activates a superior portion of the ventral premotor

cortex that largely overlaps with a speech production

motor area (Wilson, Saygin, Sereno, & Iacoboni, 2004).

This evidence is consistent with the existence of a human

vocalization mirror system, partly derived from the vocali-

zation-sensitive regions above described in the monkeyfrontal cortex. In this context, another organ that is essen-

tial for human speech is the tongue. Interestingly, there is a

phylogenetic trend towards the strengthening of cortico-

hypoglossal projections (involved in tongue control) from

non-primate mammals via non-human primates to humans

(Jürgens & Alipour, 2002), which is consistent with the

independent development of cortical control over the

vocalization apparatus in the human lineage. The tongue is

used in other functions such as swallowing, but these main-

tain their reXex nature and are presumably conserved

among primates. Speech is perhaps the function that most

beneWts from a movable and voluntarily controlled tongue.

6. Why developing a plastic vocalization system?

The exquisitely Wne-tuned movements that characterize

speech production require a delicate control of the vocal

apparatus and of the lips, tongue, jaw, and larynx (Dron-

kers & Ogar, 2004). In humans, motor control over this sys-

tem is partly located in the precentral gyrus of the insula

(Dronkers, 1996) and in the inferior frontal gyrus (Hillis

et al., 2004). If as mentioned, primate vocalizations are used

in evolutionarily “urgent” functions (Pika et al., in press), it

is reasonable to consider that in hominid evolution they

suV ered a higher selective pressure than gestures. In somecircumstances, increasing vocal plasticity and cortical con-

trol over the phonatory apparatus may have been selective

beneWt, as they allowed to convey more detailed informa-

tion about evolutionarily urgent issues. One possibility is

that prosodic and gestural markings permitted a stronger

mother-and-child relation, and other kinds of social bond-

ing that enhanced group cohesiveness and cooperation

(Kuhl, 2003; Falk, 2004). More speciWcally, early hominin

mothers engaged in reciprocal vocal (and gestural) interac-

tions with their progeny (infants or children). In this way,

both became “locked” in a mutual dynamics where the

child gradually generated a template of his/her mother’sgestures and vocalizations that permitted the maintenance

of mutual communicative interactions, largely conveying

emotional information (Aboitiz & Schröter, 2004). In these

circumstances, there was a selective prize for those individ-

uals with an increased vocal motor control, and eventually,

with an increased memory span to remember complex

sequences of utterances in order to facilitate recognition

and maintain the reciprocity in social interactions (this does

not exclude the parallel development of gestural communi-

cation). In this line, the evolution and development of bird-

song provides a useful model for early phonological

acquisition. Birds able to learn and transmit more complex

songs have a selective beneWt over those who develop less




elaborate sequences (Gil-da-Costa et al., 2004; Doupe &

Kuhl, 1999; Okanoya, 2004; Jarvis, 2004; see also Kuhl,

2003 for the social signiWcance of early language).

The plasticity of the vocalization apparatus posed it as a

good candidate to communicate referential associations

that became conventionalized in the community. Thus,

complex vocalizations may have been related Wrst to highlyemotional situations, and were accompanied by gestures

including facial movements and ritualized pantomine.

These complex, multimodal communication signals became

associated to speciWc events, generating the most basic

forms of conventionalized reference. Eventually, and with

the further evolution of the phonological capacity, these

multimodal signals became dominated by vocalizations,

but never (not even in present-day human communication)

entirely lost their multimodal, gestural-vocal nature.

A Wnal issue relates to imitative abilities. In macaques,

there is evidence for cognitive imitation (Subiaul, Cantlon,

Holloway, & Terrace, 2004), and natural imitation is

strongly facilitated by joint attention (Kumashiro et al.,

2003). In another study, it was found that neonatal chim-

panzees were able to recognize and imitate human facial

gestures, but this ability is lost after 2 months of age; on

the other hand, in humans imitation gestures appear at

approximately 8–12 months (Myowa-Yamakoshi, Tomo-

naga, Tanaka, & Matsuzawa, 2004). This evidence sug-

gests that the capacity to imitate is either ancient or has

appeared more than once in primate evolution, and is not

a uniquely human characteristic. However, all these stud-

ies have been performed in controlled laboratory condi-

tions. Another issue is whether chimpanzees and other

primates imitate in natural conditions. There has beenmuch controversy as to whether apes are able to transmit

behavioral patterns by imitation or by processes like ritu-

alization, in which stereotyped behaviors are used to

anticipate to initiate play or mating with another individ-

ual (for review see Vogel, 1999). Some evidence suggests

that in apes, ritualization is a major element in socially

transmitted behavior (Pika et al., in press), and several

gestural behaviors including pointing and some forms of

pantomime may be conceived as originating in this man-

ner. Nevertheless, other evidence indicates that chimpan-

zees and other apes are also able to learn by social

imitation. Recently, Whiten, Horner, and de Waal (2005)

trained some captive chimpanzees in one of two tech-

niques to obtain food from a box. Subsequently, these

individuals transmitted this behavior to the other mem-

bers of the community. Furthermore, animals that had

learn one technique but the majority in their group had

learned the other, eventually changed to the majority

behavior. The emerging picture is that apes are able of

imitation, but within a repertoire of several social learning

mechanisms, and in a much more limited form than

humans (Whiten, 2005). Thus, we agree with Arbib (2005)

in that these forms of imitation are diV erent from the com-

plex imitation capacity involved in pantomime and other,

human forms of imitation, but consider that these provide

a starting point for the development of more complex imi-

tative capacities, leading to more elaborate forms of com-

munication.

After all this discussion, we consider that parsimony

indicates that the most likely situation is that both, gestural

and vocal communication coevolved intimately, as they still

do now, but we see no grounds or evidence supporting thepresumed ancestral, symbolic signing stage (Aboitiz et al.,

in press; Bosman et al., 2004; and in press). In this sense,

our position is somewhat close to Arbib’s (2005), who sug-

gests an “expanding spiral” in which gestural communica-

tion including complex pantomime coevolved with vocal

communication, each potentiating the development of the

other. It diV ers, however, from Corballis’ (2003) position,

proposing a speciWc stage in which symbolic communica-

tion was predominantly hand-gestural, which was eventu-

ally “taken over” by vocal communication. SpeciWcally, we

consider unlikely that such a stage became an evolution-

arily stable condition, able to diversify and propagate.

Hands are used for other behaviors such as tool use and

carrying objects, and do not appear as optimal communica-

tion devices as long as they require that individuals stay in

front of each other doing nothing else with their hands. So,

this modality might work in idle situations but not so much

in circumstances of behavioral coordination. Furthermore,

there is no evidence that gestural communication was ever

more developed than it is now in spoken languages, lacking

several of the crucially deWning characteristics of language

(note that human sign languages are usually derived from,

or arise within the context of a vocal-communicating com-

munity). Thus, even if voluntary control was initially more

developed for hand control than for vocal communication,the most likely interpretation is that gestural communica-

tion never reached a symbolic stage without the aid of an

elaborate vocal communication system.

7. Syntax: Memory and recursion

Phonology is not the only linguistic function that makes

use of short-term memory. Lexical processing, in which the

phonological representation of a word becomes associated

with a meaning, also implies the transient coactivation of the

respective mnemonic representations. Abundant evidence

suggests that lexical memories consist of activated associativenetworks involving say, object- or motor-speciWc regions (in

the cases of names for objects and action words, respec-

tively), with language-speciWc regions (Damasio & Tranel,

1993; Damasio, Grabowski, Tranel, Hichwa, & Damasio,

1996; Pulvermüller, 1999, 2005; Pulvermüller, Lutzenberger,

& Preissl, 1999; see also Fuster, 1995a, 1995b, 2003). Never-

theless, and in accordance with the concept of associative

memory, naming networks are not likely to be rigid modules

or hardwired centers; they should rather be conceived as

highly modiWable by experience (Damasio et al., 1996; Fus-

ter, 1995a, 2003). This evidence conWrms Geschwind’s (1965)

early proposal that the human brain was unique in its ability

to perform cross-modal cortical associations, ant that this




enabled it to the development of a naming system. This

capacity is related with the development of posterior tempo-

ral lobe and inferior parietal areas, which show great individ-

ual variability in their morphology and have been also

related to the generation of the phonological loop (Ide, Rod-

ríguez, Zaidel, & Aboitiz, 1996; Ide et al., 1999).

Furthermore, the processing of more complex linguisticitems, such as syntactical structures, is also strongly depen-

dent on short-term memory. As Fuster (1995a) puts it,

“ƒlanguage, especially when it is new, complex, and

extended in time, makes constant use of those functions of

memory and set. As I speak, I need to keep track of what I

just said a few moments ago and, at the same time, prepare

for saying what is in accord with that. The predicate is

dependent on the subject, the verb on the subject and the

predicate, the dependent clause on the larger sentence, and

so on. All these are, in essence, cross-temporal contingen-

cies, and in speech there is a running reconciliation of these

contingencies that constantly change, interleaved and

embedded within another. It is the dorsolateral prefrontal

cortex that normally eV ects that reconciling, with its grasp

of the short-term past and the short-term future” (pp. 280–

281; see also Fig. 2). This comment, although strongly

appealing, is perhaps too coarse-grained for the purposes of

this paper. In the following sections, we will intend to dis-

sect some of the complex linkages that exist in diV erent

memory domains during language processing.

According to Pinker and JackendoV (2005), syntax con-

sists of the principles by which words and morphemes are

concatenated into sentences, helping to determine how the

meanings of words are combined into the meanings of

phrases and sentences. Syntax consists of several elements,one of which is word order, in which the distinct elements

are conventionally arranged in a speciWc order in each lan-

guage; another component is agreement, marking inXec-

tions in verbs or adjectives for number, person, gender, and

other features of related nouns; and yet another is case-

marking (nominative, accusative, and others). A fourth

component of syntax consists of the hierarchical construc-

tion of phrases, in which each phrase corresponds to a spe-

ciWc constituent of meaning. Furthermore, one

fundamental property of this hierarchical arrangement is

its recursivity. Generally speaking, recursion consists of the

application of some function onto itself (phrases may be

composed of nested phrases), which permits to iterate this

function endlessly, thus generating diV erent hierarchical

levels according to the iteration sequence, and permitting

the manipulation (movement) of the elements in this hierar-chy (Chomsky, 1991; Hauser et al., 2002; see also Fitch &

Hauser, 2004). An important element in the generation of

recursive structures is the so-called long-distance dependen-

cies between words, which bracket phrases embedded

within larger phrases (Chomsky, 1991). Thus, embedded

phrases can be moved to diV erent positions within a sen-

tence, changing the canonical order of the original phrase

to transform it into say, a passive sentence or a wh-ques-

tion. Moved phrases can be tracked to their original posi-

tions by a “trace” that connects the new position with the

extraction site. Some authors in the chomskyan tradition

claim that recursivity is the most fundamental property of

human language, is modularly separate from other cogni-

tive functions, and is highly unlikely to result from the

process of natural selection. This ability is claimed to be

non-existent in primates, as tamarin monkeys were shown

not to be able to learn a quite simple recursive language,

consisting of n instances of a symbol A followed by n

instances of symbol B (Fitch & Hauser, 2004). Nevertheless,

Pinker and JackendoV (2005) reply that it is not clear that

this symbol sequence represents a truly linguistic structure,

as no known language shows this kind of recursivity. As

will be discussed below, we consider that the capacity for

linguistic recursion originated in the context of an expand-

ing working memory capacity that permitted to manipulatethe diV erent items composing a complex sequence of words

(or phrases). In primates, this capacity is highly limited due

to the relatively poor development of cortico-cortical asso-

ciations compared to humans, but with increasing brain

size and subsequent cultural evolution, these networks

became robust enough to manipulate more complex items.

Our proposal is that recursivity and movement of phrase

components can only exist if backed by a strong short-term

memory mechanism that allows one to keep track of the

Fig. 2. Highly schematic concept of cortical interactions between networks of posterior and frontal cortices in the construction of a simple phrase. This

implies the coactivation of several short-term memory networks, each representing a phonological representation (squares) and a lexical representation

(circles), which although are activated in sequence, they need to be maintained in memory and associated as the phrase is being processed. Once the mean-

ing of the phrase has been extracted, it is bound or integrated as a semantic “chunk” that can be mentally manipulated in the context of a larger sentence

(Gibson, 1998; Hagoort, 2005). In this context, it is of interest to mention Glassman’s (2003) conception of two phenomenal levels during working memory

operation, binding together of many attribute representations within each respective memory “chunk,” and then the combinatorial play among three or

four distinct chunk representations. Anatomical details are not intended to be speciWc. The Wgure is a modiWcation and composite of Fuster’s (2003)

Fig. 7.9 and Pulvermüller’s (2005) Fig. 1.




long-distance dependencies present in both embedded

phrases and syntactic movement (see also Pinker, 1995).

Short sentence processing imposes a rather small load on

working memory capacity, and does not require a special-

ized or too elaborate short-term memory network. Process-

ing simple but relatively long, canonical sentences, in which

head-dependent relations have to be maintained for sometime until the phrase ends being processed, impose an addi-

tional load on memory and require relatively more robust

networks. Finally, transformational movement imposes even

higher memory loads, thus requiring the activation of more

complex networks. In human evolution, those individuals

able to develop more robust short-term neuronal networks

were able to mentally manipulate the components of a sen-

tence, thus communicating more complex messages, and

selecting what to communicate in diV erent circumstances.

This permitted them to cooperate better and to establish

stronger social bonds. An “expanding spiral” developed

between increased working memory capacity and more

complex communication, resulting in the evolution of rela-

tively intricate recursive abilities. Nevertheless, it is necessary

to note that perhaps not all syntactically ordered languages

have the properties of recursion claimed by Hauser et al.

(2002). The amazonian language Piraha has been claimed to

lack any evidence of recursion (Everett, 2004; see also Pinker

& JackendoV , 2005) but has a clear phonology, morphology,

syntax, and sentence organization. It is not clear if this lan-

guage never had recursion or lost it, but in the case that this

Wnding is conWrmed, it would indicate that syntactic lan-

guages may exist in which there are no recursion rules. Thus,

it is conceivable that modes of communication with primi-

tive syntactic rules, not including recursion (in the sense of phrase movement properties), but being speciWc on other

attributes such as word order and agreement, preexisted to

more complex languages. With the involvement of increas-

ing working memory resources, these languages tended to

evolve toward more complex, recursive grammars.

8. Models and experimental studies on working memory and

syntactical movement

In the past, short-term memory was seen by some scholars

to be a mere constraint that puts limits to syntactic process-

ing (Miller & Chomsky, 1963), while more recent authorsconsider that it has a much more active role in parsing (Gib-

son, 1998; Just & Carpenter, 1992; King & Just, 1991; King &

Kutas, 1995; see also Müller & Basho, 2004). In fact, it has

been proposed that short-term memory mechanisms make it

possible to maintain distinct linguistic elements on line while

a larger structure is being processed (Gibson, 1998, 2000; Just

& Carpenter, 1992). In these views, syntactical parsing

involves two kinds of processes: integration and short-term

memory. Integration refers to the cost of integrating distant

head-dependent relations in a phrase, which may neuro-

physiologically relate to a “binding” mechanism that glues

perceptual (lexical) elements into a coherent frame (Hagoort,

2003, 2005; Schoenemann, 1999; see Fig. 2). Interestingly,

beside language, Broca’s area has been also involved in musi-

cal processing, and the integrative mechanisms involved have

been proposed to be similar to those for syntactic parsing

(Patel, 2003; Patel, Gibson, Ratner, Besson, & Holcomb,

1998; although some argue that they are perhaps not so simi-

lar to the linkage of phonology to the lexicon or the way in

which syntax supports a compositional semantics). Gibson(1998) also claims that there are memory costs associated

with the resources required to store the incomplete current

input string as it is being processed, in order to appropriately

assign thematic roles onto syntactic constituents. Gibson

hypothesizes that each element that does not yet have a the-

matic role (such as “agent,” “patient,” etc.) while the sen-

tence is being processed imposes a burden on working

memory. As we have discussed above, the neural networks

involved in these processes include language-related areas

(especially Broca’s area and its vicinities), but are also highly

widespread by virtue of the associative nature of these mem-

ories. In this line, intracranial recording studies have revealed

that neurons that participate (but are not necessarily essen-

tial) in verbal short-term memory are widely spread in both

hemispheres (Ojemann, SchoenWeld-McNeill, & Corina,

2002). Furthermore, individual neurons usually relate to only

one mnemonic function and are surrounded by nearby neu-

rons having diV erent relationships, which suggests the exis-

tence of interlacing networks, especially well suited for

associative interactions (Ojemann, 2003).

Interestingly, Broca’s aphasics seem to have a speciWc

impairment in tracking the traces that connect components

with their extraction sites during syntactical movement

(Grodzinsky, 2000). Some authors claim that the inability

of Broca’s aphasics to track traces may reXect a workingmemory deWcit (for example, Hickok, 2000; Müller, 2000;

Stowe, 2000; Szelag & Pöppel, 2000). Furthermore, recent

imaging analyses have shown that diV erent forms of syntac-

tic movement speciWcally activate the same cortical regions:

the left inferior frontal gyrus and bilaterally, the posterior

superior temporal cortex (Ben-Shachar, Hendler, Kahn,

Ben-Bashat, & Grodzinsky, 2003; Ben-Shachar, Palti, &

Grodzinsky, 2004), which is anatomically consistent with

the activation of an auditory short-term memory circuit

(Gottlieb et al., 1989; Pasternak & Greenlee, 2005; Roman-

ski, Bates, et al., 1999; Romanski, Tian, et al., 1999). Other

functions, regulating intra-sentential dependencies that are

diV erent from syntactic movement, seem to be related to

activation of other regions such as the anterior insula, ven-

tral precentral sulcus, and the superior frontal gyrus (Grod-

zinsky, in press). Much recent evidence indicates that

Broca’s area is speciWcally activated with syntactic move-

ment and during processing of long-distance dependencies,

which are considered to imply working memory costs

(Caplan & Waters, 1999; Caplan et al., 1998, 2000; Cooke

et al., 2002; Fiebach et al., 2002; Friederici, 2004; Kaan &

Swaab, 2002; King & Kutas, 1995; Stromswold, Caplan,

Alpert, & Rauch, 1996). For example, in an fMRI study,

Cooke et al. (2002) report that the left inferior frontal cor-

tex is recruited to support the cognitive resources required




to maintain long-distance syntactic dependencies during

the comprehension of complex grammatical sentences. Fie-

bach et al. (2002) were able to dissociate memory and inte-

gration costs by using subject-initial and object-initial, long

and short wh-questions. Object-initial sentences were

highly dependent upon the subject that would be encoun-

tered later, while subject-initial sentences do not depend of the later appearance of an object argument. Thus, long,

object-initial sentences required a higher memory load but

the same integration costs as long, subject initial sentences.

In these conditions, the authors reported a sustained nega-

tivity over the left frontal scalp that was maximal for long

object wh-questions. In a subsequent study, the same

authors found that Broca’s area (particularly area 44) was

especially activated when processing complexly embedded

sentences, in comparison with similar grammatical struc-

tures which put less load on working memory (Fiebach

et al., 2005). These authors conclude that this evidence

strongly supports the role of Broca’s area in syntactical

working memory processes.

Summarizing, evidence suggests that short-term memory

mechanisms do more than putting limits to syntactical pro-

cessing; they rather play an important role in this phenome-

non. Furthermore, we concur with Fuster (1995a, 1995b)

and others in that the kind of memory involved in syntacti-

cal processing is based on the transient activation of associa-

tive networks in the cerebral cortex, and is in principle not

diV erent than other forms of cortical memory, whose precur-

sors can be found in the monkey brain. Admittedly, we are

not claiming that language and syntax can be fully explained

by memory mechanisms. There are many elements of pho-

nological, lexical, and syntactical processing such as the met-rical structure of words, inXectional rules, recognition of

syntactic components and other phenomena that may well

be language-speciWc, and are not easily explained by mem-

ory mechanisms or by current cognitive theories (Pinker &

JackendoV , 2005). Language is clearly a complex adaptation

involving specializations in perception, production, and pro-

cessing at several levels. Other cognitive phenomena, such as

the ability to recognize actions, categorizing, or problem-

solving, are strongly implicated as well and may have served

as prerequisites for linguistic evolution (Fadiga & Craighero,

2004; Gallese, 2003; Langacker, 1987, 2000; Mandler, 2004;

Nelissen et al., 2005). Nevertheless, we mentioned above that

active memory is deWned in the context of near-future

behavior, i.e., implies manipulation of cognitive items to

attain a Wnal goal. In a similar way, it permits to manipulate

the distinct components of a sentence in diV erent ways in

order to extract meaning. Thus, processes such as categoriza-

tion and problem-solving, although not identical to working

memory mechanisms, are also highly dependent on the on-

line maintenance of information.

9. Modularity or associative networks for working memory?

In the context of this discussion, there have been recent

controversies about the modular nature of the memory

mechanisms involved in syntactical processing. Some

authors contend that the system for syntactical processing

is separate from the phonological, lexical or semantic

domains (Caplan, 1987; Caplan & Waters, 1999; Ferreira &

Clifton, 1986; Martin & SaV ran, 1997; Martin, 1987), while

others consider that grammar is intrinsically linked to them

(Langacker, 2000; Lieberman, 2002). In our view, the verbalworking memory system is not a single indissociable ele-

ment, but on the other hand each component (phonologi-

cal, lexical, and syntactic) is not independent but highly

interacting with the others. This is to be expected if active

memories are essentially associative (Fuster, 1995a). Thus,

there are diV erent but partially overlapping network sys-

tems related to each domain involved in language process-

ing, which is consistent with neurobiological evidence

(Fuster, 1995a, 2003; King & Kutas, 1995; Levy & Gold-

man-Rakic, 2000; Pasternak & Greenlee, 2005; Romanski,

Tian, et al., 1999). This view agrees with fMRI results iden-

tifying three relatively separate regions of functional spe-

cialization in the inferior frontal gyrus: phonology, syntax,

and semantics (for review, see Bookheimer, 2002). There-

fore, lexical networks are diV erent but overlap in important

aspects with other kinds of networks involved in phonolog-

ical and in syntactical processing, which explains why in

some instances increasing syntactic load interferes with

phonological working memory and vice versa (Just & Car-

penter, 1992). In fact, we consider that it is precisely the

overlap between these networks that allows to process sen-

tences as integrated phonological, lexical, and syntactic uni-

ties from which a single meaning can be extracted. Putting

it another way, syntactical working memory needs to be

‘anchored’ in lexical working memory networks in order toidentify the words, their meaning, and their grammatical

properties, while lexical working memory needs to be

‘anchored’ in phonological representations that contain the

acoustic and motor dimensions of the diV erent words. In

the words of Lieberman (2002), “verbal working memory

appears to be an integral component, perhaps the key com-

ponent, of the human functional language system, coupling

speech perception, production, semantics, and syntax” (p.

70). Again, the integration of these diV erent processing lev-

els may be conceived as a “binding problem” in which the

activities associated to each mechanism become coordi-

nated and interdependent (Hagoort, 2005; Singer, 2001).

This view is thus in an intermediate position between those

who consider a separate neural subsystem for each process-

ing domain (Caplan, 1987) and cognitive approaches that

consider grammar and meaning as inseparable components

of language (Langacker, 2000).

10. Discussion

In this article, we have updated some of our previous

proposals (Aboitiz, 1995; Aboitiz & García, 1997) in which

we proposed that the language regions arose as a specializa-

tion of auditory-vocal working memory networks which in

a Wrst instance elaborated into a primitive phonological




loop. Eventually, this apparatus recruited additional mem-

ory networks representing meaning, contributing to the

development of increasingly complex forms of social com-

munication. The expansion of this system allowed the man-

agement of complex utterances in speciWc orderings such as

to convey more detailed meanings and to avoid ambiguity

in communication. The brain regions supporting languageare known to be more extense than the relatively narrow

circuits that we have pointed in this article (Dronkers &

Ogar, 2004; Dronkers et al., 1992; Kaan & Swaab, 2002),

and a more complete discussion of primate–human homo-

logues would, ideally, include these areas too. However, at

this point this would be a too ambitious project and we

have preferred to restrict our analysis to the regions that

have been classically involved with language processing.

The networks involved in syntactical processing are con-

ceived to be more extended than the phonological loop (as

they need to maintain online items more complex than just

phonological representations), but the evidence discussed

suggests that they are still partly restricted to the language-

speciWc regions (especially in the frontal lobe). Our hypoth-

esis is that in the non-human primate, there are much

simpler but comparable networks, which have not acquired

the robustness necessary to maintain and manipulate the

complex information items required for syntactical- and

even less for recursive sentence processing. In other words,

we claim that the issue of the appearance of some syntacti-

cal rules, including the recursive properties in language pro-

cessing, were behavioral innovations that became possible

due to the elaboration on preexisting neural networks,

whose function was (and is) to maintain items online dur-

ing the execution of a speciWc behavior. In order to developthese more stable and robust networks, a conversational

ability must have existed in which individuals were able to

engage in reciprocal phonological (and meaningful) inter-

actions for suYcient time, to permit the maintenance of a

“state of mind” that captured attentional and memory

resources. Cultural evolution may have provided a means

for increasing the complexity of these networks. The mod-

ern human brain had already acquired its actual size about

195,000 years ago (MacDougall, Brown, & Fleagle, 2005),

long before there were any signs of cultural activity indicat-

ing complex symbolic thinking, which date from about

75,000 years ago (Henshilwood, d’Errico, Vanhaeren, van

Niekerk, & Jacobs, 2004). This suggests that increasing

brain size was not suYcient for a fully developed language,

and that further cultural evolution was essential for lan-

guage acquisition. The developing cerebral cortex is capa-

ble of incredible plastic rearrangements in response to

environmental (and social) stimuli (Krubitzer & Kahn,

2003). Thus, cultural selection of behaviors including

increasingly more sophisticated social interactions, tool

manipulation, and other elaborate conducts may have

provided the means to develop increasingly elaborate

short-term memory network systems, linking phonology,

meaning, and syntax (Aboitiz, 1988). On this point, we may

agree with Arbib (2005), who makes the explicit claim that

human brain size evolution was not driven by the need for

syntax, but only by the demands of protolanguage, with

syntax being the fruit of cultural evolution. Nevertheless,

this does not exclude the possibility of continuing genetic

selection for the development of highly tuned sensorimotor

circuits, which permitted better cortical control and more

eYcient memory networks within the context of a Wxedbrain size (Aboitiz, 1988, 1995). Finally, there is recent evi-

dence in humans of rapid adaptive evolution of at least two

genes controlling brain size, which suggests that genetic

evolution of the human brain is still an undergoing process

(Evans et al., 2005; Mekel-Bobrov et al., 2005).

The present perspective has been discussed in the context

of two current hypotheses on language evolution. The Wrst

comes from students of mirror neurons for grasping, who

claim that a mirror system was essential for the evolution of

a brain that could support language. As mentioned, we

agree that a mirror system may have been especially impor-

tant for recognizing actions and for the development of imi-

tative capacities, which in turn were essential for the

development of a phonological loop and other cognitive and

linguistic capacities. We are more wary on the assumption

that there was an initial, symbolic hand-signing stage prior

to the origin of speech. We consider that this presumed stage

is not yet backed by suYcient evidence and there are simpler

alternatives, such as the acquisition of a vocalization mirror

system in early hominids within the context of a multimodal

vocal–gestural communication system. In this sense, the

recent Wnding by Petrides et al. (2005) of orofacial neurons

in the macaque’s area 44 may point to a brain location in

which associations between speciWc vocalizations and facial

gestures are performed. Furthermore, even in the case thathand-signing served as an initial scaV olding for the develop-

ment of vocal linguistic abilities, the subsequent evolution of

the language areas was in our view, highly dependent of the

development of auditory-vocal short-term memory net-

works that are present in non-human primates. The second

perspective relates to the generativist approach whose expo-

nents, in their latest writings, have proposed that the capac-

ity for recursion is unique to human language (which might

be correct), and is unlikely to have originated by natural

selection since it is a single characteristic, not arising as the

result of sequential steps (Hauser et al., 2002; this perspec-

tive has been contested by Pinker & JackendoV , 2005; and

see reply by Fitch, Hauser, & Chomsky, 2005). In our view,

whether the behavioral phenomenon of recursion is indeed

unique to human language, and whether there are simpler

and more complex (derived) forms of recursion in diV erent

languages remain as empirical questions. However, we also

consider that the acquisition of recursion has been only pos-

sible through the increasing complexity of the short-term

memory networks involved in meaningful communication,

which most likely has been a gradual process (via either cul-

tural or genetic evolution).

There have been other neurobiological theories of early

speech evolution, and we will mention only a few of them.

The motor theory of speech perception claims that the




listener processes speech by comparing the input with a

motor template for speech production (Liberman & Mat-

tingly, 1985). Another proposal is the concept of categori-

cal perception, where speech sounds are not directly

translated into their acoustical parameters but rather are

labeled within distinct phonological categories (Kuhl,

1992). These two theories are entirely consistent with theexistence and evolution of a phonological loop (see Lie-

berman, 2002). Finally, there is the concept of selection

for precise motor timing which permitted the complex

articulation of speech movements (Dronkers & Ogar,

2004), which were related with the acquisition of other

Wne motor tasks such as object manipulation and stone

throwing (Calvin, 1983). Again, this idea is complemen-

tary to our proposals, although as said we are not sure

that control of hand coordination was a strict requisite

for the evolution of vocal communication. Rather, the

two evolved together, in an intimate relationship.

Finally, although relying on relatively few genetic

changes (Culotta, 2005), language and human communi-

cation involve modiWcations at several functional levels,

including gross morphology, motor control, perceptual

mechanisms, and the elaboration of speciWc neural net-

works participating in higher aspects of phonological, lex-

ical, and semantic processing. Our emphasis in this article

has been to point to neural structures and networks that

participate in certain aspects of language processing, and

tracking these to more simple networks in the primate

brain, which have a similar topographic organization as

in the human and participate in similar processes. We

consider that this evidence makes a case for evolutionary

continuity (homology) between the respective neural sys-tems.

Acknowledgment

This work was supported by the Millennium Nucleus for

Integrative Neuroscience.

References

Aboitiz, F. (1988). Epigenesis and the evolution of the human brain. Medi-

cal Hypotheses, 25, 55–59.

Aboitiz, F. (1995). Working memory networks and the origin of language

areas in the human brain. Medical Hypotheses, 44, 504–506.Aboitiz, F., & García, R. (1997). The evolutionary origin of the language

areas in the human brain. A neuroanatomical perspective. Brain

Research Reviews, 25, 381–396.

Aboitiz, F., García, R., Brunetti, E., & Bosman, C. (in press). The origin of

Broca’s area and its connections from an ancestral working/active

memory network. In K. Amunts & Y. Grodzinsky (Eds.), Broca’s area.

Oxford: Oxford University Press.

Aboitiz, F., García, R., Brunetti, E., & Bosman, C. (2005). Imitation and

memory in language origins. Neural Networks, 18, 1357.

Aboitiz, F., & Schröter, C. (2004). Prelinguistic evolution and motherese:

A hypothesis on the neural substrates. Behavioral and Brain Sciences,

27 , 503–504.

Acardi, A. C. (2000). Vocal responsiveness in male wild chimpanzees:

Implications for the evolution of language. Journal of Human Evolu-

tion, 39, 205–223.

Acardi, A. C. (2003). Is gestural communication more sophisticated than

vocal communication in wild chimpanzees? Behavioral and Brain Sci-

ences, 26 , 210–211.

Arbib, M. (2005). From monkey-like action recognition to human lan-

guage. An evolutionary framework for neurolinguistics. Behavioral and

Brain Sciences, 28, 105–167.

Arbib, M., & Bota, M. (2003). Language evolution: Neural homologies

and neuroinformatics. Neural Networks, 16 , 1237–1260.

Awh, E., Smith, E. E., & Jonides, J. (1995). Human rehearsal processes and

the frontal lobes: PET evidence. Annals of the New York Academy of

Sciences, 769, 97–118.

Baddeley, A. (1992). Working memory. Science, 255, 556–559.

Baddeley, A. (2000). The episodic buV er: A new component of working

memory? Trends in Cognitive Sciences, 4, 417–423.

Baddeley, A. (2003). Working memory: Looking back and lookin forward.

Nature Reviews Neuroscience, 4, 829–839.

Baddeley, A. D., & Hitch, G. J. (1974). Working memory. In G. A. Bower

(Ed.), The psychology of learning and motivation . New York: Academic

Press.

Baddeley, A. D., Papagno, C., & Vallar, G. (1988). When long-term learn-

ing depends on short-term memory. Journal of Memory and Language,

27 , 586–595.

Barbas, H., & Pandya, D. N. (1989). Architecture and intrinsic connectionsof the prefrontal cortex in the rhesus monkey. Journal of Comparative

Neurology, 286 , 353–375.

Belin, P., & Zatorre, R. J. (2000). ‘What,’ ‘where’ and ‘how’ in auditory

cortex. Nature Neuroscience, 3, 965–966.

Ben-Shachar, M., Hendler, T., Kahn, I., Ben-Bashat, D., & Grodzinsky, Y.

(2003). The neural reality of syntactic transformations—Evidence from

fMRI. Psychological Science, 14, 433–440.

Ben-Shachar, M., Palti, D., & Grodzinsky, Y. (2004). Neural correlates of

syntactic movement: Converging evidence from two fMRI experi-

ments. Neuroimage, 21, 1320–1336.

Bookheimer, S. (2002). Functional fMRI of language: New approaches to

understanding the cortical organization of semantic processing. Annual

Review of Neuroscience, 25, 151–188.

Bosman, C., García, R., & Aboitiz, F. (2004). FOXP2 and the language

working memory system. Trends in Cognitive Sciences, 6 , 251–252.Bosman, C., López, V., & Aboitiz, F. (2005). Sharpening Occam’s razor: Is

there necessity of a hand-signing stage prior to vocal communication?

Behavioral and Brain Sciences, 28, 128–129.

Brodmann, K. (1909). Vergleichende Lokalisationslehre der Gro hirnrinde.

Leipzig: Barth.

Bullier, J., Schall, J. D., & Morel, A. (1996). Functional streams in occipito-

frontal connections in the monkey. Behavioral Brain Research, 76 ,

89–97.

Calvert, G. A., Brammer, M. J., Bullmore, E. T., Campbell, R., Iversen, S.

D., & David, A. S. (1999). Response ampliWcation in sensory-speciWc

cortices during crossmodal binding. Neuroreport, 10, 2619–2623.

Calvin, W. H. (1983). A stone’s throw and its launch window: Timing pre-

cision and its implications for language and hominid brains. Journal of

Theoretical Biology, 104, 121–135.

Caplan, D. (1987). Neurolinguistics and linguistic aphasiology: An introduc-tion. Cambridge: Cambridge University Press.

Caplan, D., Alpert, N., & Waters, G. (1998). EV ects of syntactic structure

and propositional number on patterns of regional cerebral blood Xow.

Journal of Cognitive Neuroscience, 10, 541–552.

Caplan, D., Alpert, N., Waters, G., & Olivieri, A. (2000). Activation of

Broca’s area by syntactic processing under conditions of concurrent

articulation. Human Brain Mapping, 9, 65–71.

Caplan, D., & Waters, G. S. (1999). Verbal working memory and sentence

comprehension. Behavioral and Brain Sciences, 22, 77–126.

Castiello, U. (2005). The neuroscience of grasping. Nature Reviews Neuro-

science, 6 , 726–736.

Cavada, C., & Goldman-Rakic, P. (1989). Posterior parietal cortex in rhe-

sus monkey: II. Evidence for segregated cortico-cortical networks link-

ing sensory and limbic areas with the frontal lobe. Journal of

Comparative Neurology, 287 , 422–445.




Chomsky, N. (1991). Linguistics and cognitive science: Problems and mys-

teries. In A. Kasher (Ed.), The chomskyan turn. Cambridge, MA: Black-

well.

Cooke, A., Zurif, E. B., DeVita, C., Alsop, D., Koenig, P., Detre, J., et al.

(2002). Neural basis for sentence comprehension: Grammatical and

short-term memory components. Human Brain Mapping, 15, 80–94.

Culotta, E. (2005). What genetic changes made us human? Science, 309, 91.

Corballis, M. C. (2003). From mouth to hand: Gesture, speech, and

the evolution of right-handedness. Behavioral and Brain Sciences, 26 ,

199–208.

Damasio, A. R., & Tranel, D. (1993). Nouns and verbs are retrieved with

diV erently distributed neural systems. Proceedings of the National

Academy of Sciences of the United States of America, 90, 4957–4960.

Damasio, H., Grabowski, T. J., Tranel, D., Hichwa, R. D., & Damasio, A.

R. (1996). A neural basis for lexical retrieval. Nature, 380, 409–505.

de Fockert, J. W., Rees, G., Frith, C. D., & Lavie, N. (2001). The role of

working memory in visual selective attention. Science, 291, 1803–1806.

Doupe, A. J., & Kuhl, P. K. (1999). Birdsong and human speech: Common

themes and mechanisms. Annual Review of Neuroscience, 22, 567–631.

Dronkers, N. F. (1996). A new brain region for coordinating speech articu-

lation. Nature, 384, 159–161.

Dronkers, N., & Ogar, J. (2004). Brain areas involved in speech produc-

tion.Brain, 127

, 1461–1462.Dronkers, N. F., Shapiro, J. K., Redfern, B., & Knight, R. T. (1992). The

role of Broca’s area in Broca’s aphasia. Journal of Clinical and Experi-

mental Neuropsychology, 14, 52–53.

Dronkers, N. F., Wilkins, D. P., Van Valin, R. D., Jr., Redfern, B. B., & Jae-

ger, J. J. (2004). Lesion analysis of the brain areas involved in language

comprehension. Cognition, 92, 145–177.

Durstewitz, D., Seamans, J. K., & Sejnowski, T. J. (2000). Neurocomputa-

tional models of working memory. Nature Neuroscience, 3(Suppl.),

1184–1191.

Engel, A. K., Fries, P., & Singer, W. (2001). Dynamic predictions: Oscilla-

tions and synchrony in top-down processing. Nature Reviews Neurosci-

ence, 2, 704–717.

Engel, A. K., & Singer, W. (2001). Temporal binding and the neural corre-

lates of sensory awareness. Trends in Cognitive Sciences, 5, 16–25.

Evans, P. D., Gilbert, S. L., Mekel-Bobrov, N., Vallender, E. J., Anderson,J. R., Vaez-Azizi, L. M., et al. (2005). Microcephalin, a gene regulating

brain size, continues to evolve adaptively in humans. Science, 309,

1717–1720.

Everett, D. (2004). Cultural constraints on grammar and cognition in

Piraha: Another look at the design features of human language . Unpub-

lished manuscript, Manchester: University of Manchester. <http://

lings.ln.man.ac.uk/info/staV /DE/cultgram.pdf />.

Fadiga, L., & Craighero, L. (2004). Electrophysiology of action representa-

tion. Journal of Clinical Neurophysiology, 21, 157–169.

Falk, D. (2004). Prelinguistic evolution in early hominins: Whence mother-

ese? Behavioral and Brain Sciences, 27 , 491–503.

Felleman, D. J., & Van Essen, D. C. (1991). Distributed hierarchical pro-

cessing in the primate cerebral cortex. Cerebral Cortex, 1, 1–47.

Ferrari, P. F., Gallese, V., Rizzolatti, G., & Fogassi, L. (2003). Mirror neu-

rons responding to the observation of ingestive and communicativemouth actions in the monkey ventral premotor cortex. European Jour-

nal of Neuroscience, 17 , 1703–1714.

Ferreira, F., & Clifton, C. (1986). The independence of syntactic process-

ing. Journal of Memory and Language, 25, 1–18.

Feyeresien, P., & Havard, I. (1999). Mental imagery and production of

hand gestures by younger and older adults. Journal of Nonverbal

Behavior, 23, 153–171.

Fiebach, C. J., Schelewsky, M., & Friederici, A. D. (2002). Separating syn-

tactic memory costs and syntactic integration costs during parsing: The

processing of german Wh-questions. Journal of Memory and Language,

47 , 250–272.

Fiebach, C. J., Schlesewsky, M., Lohmann, G., von Cramon, D. Y., &

Friederici, A. D. (2005). Revisiting the role of Broca’s area in sentence

processing: Syntactic integration versus syntactic working memory.

Human Brain Mapping, 24, 79–91.

Fingelkurts, A., Fingelkurts, A., Krause, C., Kaplan, A., Borisov, S., &

Sams, M. (2003). Structural (operational) synchrony of EEG alpha

activity during an auditory memory task. Neuroimage, 20, 529–542.

Fitch, W. T. (2000). The evolution of speech: A comparative review. Trends

in Cognitive Sciences, 4, 258–267.

Fitch, W. T., & Hauser, M. D. (2004). Computational constraints on syn-

tactic processing in a nonhuman primate. Science, 303, 377–380.

Fitch, W. T., Hauser, M. D., & Chomsky, N. (2005). The evolution of

the language faculty: ClariWcations and implications. Cognition, 97 ,

179–210.

Frackowiak, R. S. (1994). Functional mapping of verbal memory and lan-

guage. Trends in Neuroscience, 17 , 109–115.

Frey, S. H., Vinton, D., Norlund, R., & Grafton, S. T. (2005). Cortical

topography of human anterior intraparietal cortex active during visu-

ally guided grasping. Cognitive Brain Research, 23, 397–405.

Friederici, A. D. (2004). The neural basis of syntactic processes. In M. S.

Gazzaniga (Ed.), The cognitive neurosciences III . Cambridge, MA: MIT

Press.

Fuster, J. M. (1995a). Memory in the cerebral cortex. Cambridge, MA:

MIT Press.

Fuster, J. M. (1995b). Memory in the cortex of the primate. Biological

Research, 28, 59–72.

Fuster, J. M. (2003).Cortex and mind

. Oxford: Oxford University Press.Fuster, J. M., & Alexander, G. E. (1971). Neuron activity related to short-

term memory. Science, 173, 652–654.

Gallese, V. (2003). A neuroscientiWc grasp of concepts: From control to

representation. Philosophical Transactions of the Royal Society of Lon-

don B Biological Sciences, 358, 1231–1240.

Gannon, P. J., Kheck, N. M., Braun, A. R., & Holloway, R. L. (2005). Pla-

num parietal of chimpanzees and orangutans: A comparative reso-

nance of human-like planum temporal asymmetry. Anatomical Records

A. Discoveries in Molecular and Cellular Evolutionary Biology, 287 ,

1128–1141.

Gathercole, S. E., & Baddeley, A. D. (1990). The role of phonological

memory in vocabulary acquisition: A study of young children learning

new names. British Journal of Psychology, 81, 439–454.

Gemba, H., Miki, N., & Sasaki, K. (1997). Cortical Weld potentials preced-

ing vocalizations in monkeys. Acta Otolaryngologica Supplemental,532, 96–98.

Geschwind, N. (1965). Disconnexion syndromes in animals and man.

Brain, 88, 237–294 585-644.

Gibson, E. (1998). Linguistic complexity: Locality of syntactic dependen-

cies. Cognition, 68, 1–76.

Gibson, E. (2000). The dependency locality theory: A distance-based the-

ory of linguistic complexity. In Y. Miyashita, A. Marantaz, & W.

O’Neill (Eds.), Image, language, brain. Cambridge, MA: MIT Press.

Gil-da-Costa, R., Braun, A., Lopes, M., Hauser, M. D., Carson, R. E.,

Herscovitch, P., et al. (2004). Toward an evolutionary perspective on

conceptual representation: Species-speciWc calls activate visual and

aV ective processing systems in the macaque. Proceedings of the

National Academy of Sciences of the United States of America, 101,

17516–17521.

Glassman, R. B. (2003). Topology and graph theory applied to corticalanatomy may help explain working memory capacity for three or four

simultaneous items. Brain Research Bulletin, 60, 25–42.

Goldenberg, G. (1997). Disorders of body perception. In T. E. Feinberg &

M. J. Farah (Eds.), Behavioral neurology and neuropsychology. New

York: McGraw-Hill.

Goldenberg, G. (2001). Imitation and matching of hand and Wnger pos-

tures. NeuroImage, 14, S132–S136.

Goldenberg, G., & Hagmann, S. (1997). The meaning of meaningless ges-

tures: A study of visuo-imitative apraxia. Neuropsychologia, 35, 333–341.

Goldin-Meadow, S., & Wagner, S. M. (2005). How our hands help us learn.

Trends in Cognitive Sciences, 9, 234–241.

Goldman-Rakic, P. S. (1996). The prefrontal landscape: Implications of

functional architecture for understanding human mentation and the

central executive. Philosophical Transactions of the Royal Society of

London B Biological Sciences, 351, 1445–1453.

http://lings.ln.man.ac.uk/info/staff/DE/cultgram.pdf












Goldman-Rakic, P. S. (2000). Localization of function all over again. Neu-

roimage, 11, 451–457.

Gottlieb, Y., Vaadia, E., & Abeles, M. (1989). Single unit activity in the

auditory cortex of a monkey performing a short term memory task.

Experimental Brain Research, 74, 139–148.

Grodzinsky, J. (2000). The neurology of syntax: Language use without

Broca’s area. Behavioral and Brain Sciences, 23, 1–71.

Grodzinsky, J. (in press). A blueprint for a brain map of syntax. In K.

Amunts & Y. Grodzinsky (Eds.), Broca’s area. Oxford: Oxford Univer-

sity Press.

Habib, M., Demonet, J. F., & Frackowiak, R. (1996). Cognitive neuroanat-

omy of language: Contribution of functional cerebral imaging. Revue

Neurologique, 152, 249–260.

Hackett, T. A., Stepniewska, I., & Kaas, J. H. (1998). Subdivisions of audi-

tory cortex and ipsilateral cortical connections of the parabelt auditory

cortex in macaque monkeys. Journal of Comparative Neurology, 394,

475–495.

Hackett, T. A., Stepniewska, I., & Kaas, J. H. (1999). Prefrontal connec-

tions of the parabelt auditory cortex in macaque monkeys. Brain

Research, 817 , 45–58.

Hagoort, P. (2003). How the brain solves the binding problem for lan-

guage: A neurocomputational model of syntactic processing. Neuroim-

age, 20(Suppl. 1), 18–29.Hagoort, P. (2005). On Broca, brain, and binding: A new framework.

Trends in Cognitive Sciences, 9, 416–423.

Hamilton, C. R., & Vermeire, B. A. (1988). Complementary hemispheric

specialization in monkeys. Science, 242, 1691–1694.

Hanlon, R. E., Brown, J. W., & Gerstmen, L. J. (1990). Enhancement of

naming in nonXuent aphasia through gesture. Brain and Language, 32,

298–314.

Hast, M. H., Fischer, J. M., Wetzel, A. B., & Thompson, V. E. (1974). Corti-

cal motor representation of the laryngeal muscles in Macaca mulatta.

Brain Research, 73, 229–240.

Hauser, M. D., Chomsky, N., & Fitch, W. T. (2002). The faculty of language:

What is it, who has it, and how did it evolve? Science, 298, 1569–1579.

Henshilwood, C., d’Errico, F., Vanhaeren, M., van Niekerk, K., & Jacobs,

Z. (2004). Middle Stone Age shell beads from South Africa. Science,

304, 404.Hickok, G. (2000). The left frontal convolution plays no special role in

syntactic comprehension. Behavioral and Brain Sciences, 23, 35–36.

Hickok, G., Buchsbaum, B., Humphries, C., & Muftuler, T. (2003). Audi-

tory-motor interaction revealed by fMRI: Speech, music, and working

memory in area Spt. Journal of Cognitive Neuroscience, 15, 673–682.

Hickock, G., & Poeppel, D. (2000). Towards a functional neuroanatomy of

speech perception. Trends in Cognitive Sciences, 4, 131–138.

Hillis, A. E., Work, M., Barker, P. B., Jacobs, M. A., Breese, E. L., &

Maurer, K. (2004). Re-examining the brain regions crucial for orches-

trating speech articulation. Brain, 127 , 1479–1487.

Hopkins, W. D., & Leavens, D. A. (1998). Hand use and gestural commu-

nication in chimpanzees (Pan troglodytes). Journal of Comparative Psy-

chology, 112, 95–99.

Hopkins, W. D., Russell, J., Freeman, H., Buehler, N., Reynolds, E., &

Schapiro, S. J. (2005). The distribution and development of handednessfor manual gestures in captive chimpanzees (Pan troglodytes). Psycho-

logical Science, 16 , 487–493.

Hostetter, A. B., Cantero, M., & Hopkins, W. D. (2001). DiV erential use of

vocal and gestural communication by chimpanzees (Pan troglodytes) in

response to the attentional status of a human (Homo sapiens). Journal

of Comparative Psychology, 115, 337–343.

Ide, A., Dolezal, C., Fernández, M., Labbé, E., Mandujano, R., Montes, S.,

et al. (1999). Hemispheric diV erences in variability of Wssural patterns

in parasylvian and cingulate regions of human brains. Journal of Com-

parative Neurology, 410, 235–242.

Ide, A., Rodríguez, E., Zaidel, E., & Aboitiz, F. (1996). Bifurcation patterns

in the human sylvian Wssure: Hemispheric and sex diV erences. Cerebral

Cortex, 6 , 717–725.

Izumi, A., & Kojima, S. (2004). Matching vocalizations to vocalizing faces

in a chimpanzee, Pan troglodytes. Animal Cognition, 7 , 179–184.

Janik, V. M. (2000). Whistle matching in wild bottlenose dolphins, Tursi-

ops truncatus. Science, 289, 1355–1357.

Jarvis, E. D. (2004). Learned birdsong and the neurobiology of human lan-

guage. Annals of the New York Academy of Sciences, 1016 , 749–777.

Jürgens, U. (2003). From mouth to mouth and hand to hand: On language

evolution. Behavioral and Brain Sciences, 26 , 229–230.

Jürgens, U., & Alipour, M. (2002). A comparative study on the cortico-

hypoglossal connections in primates, using biotin dextranamine. Neu-

roscience Letters, 328, 245–248.

Just, M. A., & Carpenter, P. A. (1992). A capacity theory of comprehen-

sion: Individual diV erences in working memory. Psychological Review,

99, 122–149.

Kaan, E., & Swaab, T. Y. (2002). The brain circuitry of syntactic compre-

hension. Trends in Cognitive Sciences, 6 , 350–356.

Kaas, J. H., & Hackett, T. A. (1999). ‘What’ and ‘where’ processing in

auditory cortex. Nature Neuroscience, 2, 1045–1047.

King, J., & Just, M. A. (1991). Individual diV erences in syntactic compre-

hension: The role of working memory. Journal of Memory and Learn-

ing, 30, 580–602.

King, J. M., & Kutas, M. (1995). Who did what and when? using word-

and clause-level ERPs to monitor working memory usage in reading.

Journal of Cognitive Neuroscience, 7 , 376–396.

Kirzinger, A., & Jürgens, U. (1982). Cortical lesion eV

ects and vocalizationin the squirrel monkey. Brain Research, 233, 299–315.

Kohler, E., Keysers, C., Umilta, M. A., Fogassi, L., Gallese, V., & Rizzol-

atti, G. (2002). Hearing sounds, understanding actions: Action repre-

sentation in mirror neurons. Science, 297 , 846–848.

Krubitzer, L., & Kahn, D. M. (2003). Nature versus nurture revisited: An

old idea with a new twist. Progress in Neurobiology, 70, 33–52.

Kuhl, P. K. (1992). Psychoacoustics and speech perception: Internal stan-

dards, perceptual anchors, and prototypes. In L. A. Werner & E. W.

Rubel (Eds.), Developmental psychoacoustics. Washington: American

Psychological Association.

Kuhl, P. K. (2003). Human speech and birdsong: Communication and the

social brain. Proceedings of the National Academy of Sciences USA,

100, 9645–9646.

Kumashiro, M., Ishibashi, H., Uchiyama, Y., Itakura, S., Murata, A., &

Iriki, A. (2003). Natural imitation induced by joint attention in japa-nese macaques. International Journal of Psychophysiology, 50, 81–99.

Langacker, R. W. (1987). Foundations of cognitive grammar: Theoretical

prerequisites . Stanford: Stanford University Press.

Langacker, R. W. (2000). Grammar and conceptualization. Berlin: Mouton

de Gruyer.

Leavens, D. A., & Hopkins, W. D. (1998). Intentional communication by

chimpanzees: A cross-sectional study of the use of referential gestures.

Developmental Psychology, 34, 813–822.

Leavens, D. A., Hopkins, W. D., & Thomas, R. K. (2004). Referential com-

munication by chimpanzees, Pan troglodytes. Journal of Comparative

Psychology, 118, 48–57.

Levy, R., & Goldman-Rakic, P. S. (2000). Segregation of working memory

functions within the dorsolateral prefrontal cortex. Experimental Brain

Research, 133, 23–32.

Liebal, K., Call, J., & Tomasello, M. (2004). Use of gesture sequences inchimpanzees. American Journal of Primatology, 64, 377–396.

Liberman, A. M., & Mattingly, I. G. (1985). The motor theory of speech

perception revised. Cognition, 21, 1–36.

Lieberman, P. (2002). Human language and our reptilian brain. Cambridge:

Harvard Press.

MacDougall, I., Brown, F. H., & Fleagle, J. G. (2005). Stratigraphic placement

and age of modern humans from Kibish, Ethiopia. Nature, 433, 733–736.

Mandler, J. M. (2004). Thought before language. Trends in Cognitive Sci-

ences, 8, 508–513.

Marshall, A. J., Wrangham, R. W., & Acardi, A. C. (1999). Does learning

aV ect the structure of vocalizations in chimpanzees? Animal Behavior,

58, 825–830.

Martin, R. C. (1987). Articulatory and phonological deWcits in short-term

memory and their relation to syntactic processing. Brain and Language,

32, 159–192.




Martin, N., & SaV ran, E. M. (1997). Language and Auditory-verbal short-

term memory impairments: Evidence for common underlying pro-

cesses. Cognitive Neuropsychology, 14, 641–682.

Mayberry, R. I., Jacques, J., & DeDe, G. (1998). What stuttering reveals

about the development of gesture–speech relationship. New Directions

in Child Development, 79, 77–87.

Mekel-Bobrov, N., Gilbert, S. L., Evans, P. D., Vallender, E. J., Anderson,

J. R., Hudson, R. R., et al. (2005). Ongoing adaptive evolution

of ASPM, a brain size determinant in Homo sapiens. Science, 309,

1720–1722.

Miklósi, A. (1999). From grasping to speech: Imitation might provide a

missing link. Trends in Neurosciences, 22, 151–152.

Miller, G. A., & Chomsky, N. (1963). Finitary models of language users. In

D. Luce, R. Bush, & E. Galanter (Eds.), Handbook of mathematical psy-

chology (Vol. 2). New York: Wiley.

Mitani, J. C., Hunley, K. L., & Murdoch, M. E. (1999). Geographic varia-

tion in the calls of wild chimpanzees: A reassessment. American Journal

of Primatology, 47 , 133–151.

Müller, R. A. (2000). A big “housing” problem and a trace of neuroimag-

ing: Broca’s area is more than a transformation center. Behavioral and

Brain Sciences, 23, 42.

Müller, R. A., & Basho, S. (2004). Are nonlinguistic functions in “Broca’s

area” prerequisites for language acquisition. FMRIW

ndings from anontogenetic viewpoint. Brain and Language, 89, 329–336.

Myowa-Yamakoshi, M., Tomonaga, M., Tanaka, M., & Matsuzawa, T.

(2004). Imitation in neonatal chimpanzees, Pan troglodytes. Develop-

mental Science, 7 , 437–442.

Nelissen, K., Luppino, G., VanduV el, W., Rizzolatti, G., & Orban, G. A.

(2005). Observing others: Multiple action representation in the frontal

lobe. Science, 310, 332–336.

Ojemann, G. A. (1978). Organization of short-term verbal memory in lan-

guage areas of human cortex: Evidence from electrical stimulation.

Brain and Language, 5, 331–340.

Ojemann, G. A. (1991). Cortical organization of language. Journal of Neu-

roscience, 11, 2281–2287.

Ojemann, G. A. (2003). The neurobiology of language and verbal memory:

Observations from awake neurosurgery. International Journal of Psy-

chophysiology, 48, 141–146.Ojemann, G. A., & Mateer, C. (1979). Human language cortex: Localiza-

tion of memory, syntax, and sequential motor-phoneme identiWcation

systems. Science, 205, 1401–1403.

Ojemann, G. A., SchoenWeld-McNeill, J., & Corina, D. P. (2002). Anatomic

subdivisions in human temporal cortical neuronal activity related to

recent verbal memory. Nature Neuroscience, 5, 64–71.

Okanoya, K. (2004). The Bengalese Wnch: A window on the behavioral

neurobiology of birdsong syntax. Annals of the New York Academy of

Sciences, 1016 , 724–735.

Palva, J. M., Palva, S., & Kaila, K. (2005). Phase synchrony among neuronal

oscillations in the human cortex. Journal of Neuroscience, 25, 3962–3972.

Parker, G. J. M., Luzzi, S., Alexander, D. C., Wheeler-Kingshott, C. A. M.,

Ciccarelli, O., & Lambon Ralph, M. A. (2005). Lateralization of ventral

and dorsal auditory-language pathways in the human brain. NeuroIm-

age, 24, 656–666.Pasternak, T., & Greenlee, M. W. (2005). Working memory in primate sen-

sory systems. Nature Reviews Neuroscience, 6 , 97–107.

Patel, A. D. (2003). Language, music, syntax and the brain. Nature Neuro-

science, 7 , 674–681.

Patel, A. D., Gibson, E., Ratner, J., Besson, M., & Holcomb, P. J. (1998).

Processing syntactic relations in language and music: An event-related

potential study. Journal of Cognitive Neuroscience, 10, 717–733.

Paulesu, E., Frith, C. D., & Frackowiak, R. S. (1993). The neural correlates

of the verbal component of working memory. Nature, 362, 342–345.

Paus, T. (2001). Primate anterior cingulate cortex: Where motor control,

drive and cognition interface. Nature Reviews Neuroscience, 2, 417–424.

Peigneux, P., Salmon, E., Van der Linden, M., Garraux, G., Aerts, J., DelW-

ore, G., et al. (2000). The role of lateral occipitotemporal junction and

area MT/V5 in the visual analysis of upper limb postures. NeuroImage,

11, 644–655.

Petrides, M. (in press). Broca’s area in the human and the non-human pri-

mate brain. In K. Amunts & Y. Grodzinsky (Eds.), Broca’s area.

Oxford: Oxford University Press.

Petrides, M., & Pandya, D. N. (1984). Projections to the frontal cortex

from the posterior parietal region in the rhesus monkey. Journal of

Comparative Neurology, 228, 105–116.

Petrides, M., & Pandya, D. N. (1988). Association Wber pathways to the

frontal cortex from the superior temporal region in the rhesus monkey.

Journal of Comparative Neurology, 273, 52–66.

Petrides, M., & Pandya, D. N. (1999). Dorsolateral prefrontal cortex:

Comparative cytoarchitectonic analysis in the human and the macaque

brain and corticocortical connection patterns. European Journal of

Neuroscience, 11, 1011–1036.

Petrides, M., & Pandya, D. N. (2001). Comparative cytoarchitectonic anal-

ysis of the human and the macaque ventrolateral prefrontal cortex and

corticocortical connection patterns in the monkey. European Journal of

Neuroscience, 16 , 291–310.

Petrides, M., Cadoret, G., & Mackey, S. (2005). Orofacial somatomotor

responses in the macaque monkey homologue of Broca’s area. Nature,

435, 1235–1238.

Pika, S., Liebal, T., Call, J., & Tomasello, M. (in press). The gestural com-

munication of apes. Gesture.

Pinker, S. (1995).The language instinct: How the mind creates language

.New York: Harper Perennial.

Pinker, S., & JackendoV , R. (2005). The faculty of language: What’s special

about it? Cognition, 95, 201–236.

Pizzamiglio, L., Aprile, T., Spitoni, G., Pitzalis, S., Bates, E., D’Amico, S., et

al. (2005). Separate neural systems for processing action- or non-

action-related sounds. Neuroimage, 24, 852–861.

Poole, J. H., Tyack, P. L., Stoeger-Horwath, A. S., & Watwood, S. (2005).

Elephants are capable of vocal learning. Nature, 434, 455–456.

Preuss, T., & Goldman-Rakic, P. S. (1991a). Myelo and cytoarchitecture of

the granular frontal cortex and surrounding regions in the strepsirhine

primate Galago and the anthropoid primate Macaca. Journal of Com-

parative Neurology, 310, 429–474.

Preuss, T., & Goldman-Rakic, P. S. (1991b). Architectonics of the parietal

and temporal association cortex in the strepsirhine primate Galago

compared to the anthropoid primate Macaca. Journal of ComparativeNeurology, 310, 475–506.

Preuss, T., & Goldman-Rakic, P. S. (1991c). Ipsilateral cortical connections

of granular frontal cortex in the strepsirhine primate Galago, with

comparative comments on anthropoid primates. Journal of Compara-

tive Neurology, 310, 507–549.

Pulvermüller, F. (1999). Words in the brain’s language. Behavioral and

Brain Sciences, 22, 253–336.

Pulvermüller, F. (2005). Brain mechanisms linking language and action.

Nature Reviews Neuroscience, 6 , 576–582.

Pulvermüller, F., Lutzenberger, W., & Preissl, H. (1999). Nouns and verbs

in the intact brain: Evidence from event-related potentials and high-

frequency cortical responses. Cerebral Cortex, 9, 497–506.

Rauschecker, J. P., & Tian, B. (2000). Mechanisms and streams for pro-

cessing of “what” and “where” in auditory cortex. Proceedings of the

National Academy of Sciences of the United States of America, 97 ,11800–11806.

Rizzolatti, G., & Arbib, M. A. (1998). Language within our grasp. Trends

in Neuroscience, 21, 188–194.

Rizzolatti, G., & Arbib, M. A. (1999). From grasping to speech: Imitation may

provide a missing link. Reply to Miklósi. Trends in Neuroscience, 22, 152.

Rizzolatti, G. W., & Craighero, L. (2004). The mirror-neuron system.

Annual Reviews in Neuroscience, 27 , 169–192.

Romanski, L. M., Averbeck, B. B., & Diltz, M. (2005). Neural representa-

tion of vocalizations in the primate ventrolateral prefrontal cortex.

Journal of Neurophysiology, 93, 734–747.

Romanski, L. M., Bates, J. F., & Goldman-Rakic, P. S. (1999). Auditory

belt and parabelt projections to the prefrontal cortex in the rhesus

monkey. Journal of Comparative Neurology, 403, 141–157.

Romanski, L. M., & Goldman-Rakic, P. S. (2002). An auditory domain in

primate prefrontal cortex. Nature Neuroscience, 5, 15–16.




Romanski, L. M., Tian, B., Fritz, J. B., Mishkin, M., Goldman-Rakic, P. S.,

& Rauschecker, J. P. (2000). ‘What, ‘where’ and ‘how’ in auditory cor-

tex. Reply to Belin & Zatorre. Nature Neuroscience, 3, 966.

Romanski, L. M., Tian, B., Mishkin, M., Goldman-Rakic, P. S., & Raus-

hecker, J. P. (1999). Dual streams of auditory aV erents target multiple

domains in the primate prefrontal cortex. Nature Neuroscience, 2,

1131–1136.

Ruchkin, D. S., Grafman, J., Cameron, K., & Berndt, R. S. (2003). Working

memory retention systems: A state of activated long-term memory.

Behavioral and Brain Sciences, 26 , 709–728.

Salmon, E., Van der Linden, M., Collette, F., DelWore, G., Maquet, P., Deg-

ueldre, C., et al. (1996). Regional brain activity during working mem-

ory tasks. Brain, 119, 1617–1625.

Schoenemann, P. T. (1999). Syntax as an emergent characteristic of the

evolution of semantic complexity. Minds and Machines, 9, 309–346.

Scott, S. K., & Johnsrude, I. S. (2003). The neuroanatomical and functional

organization of speech perception. Trends in Neuroscience, 26 , 100–107.

Seyfarth, R. M., & Cheney, D. L. (2003). Meaning and emotion in animal

vocalizations. Annals of the New York Academy of Science, 1000,

32–55.

Shapiro, A. D., Slater, P. J., & Janik, V. M. (2004). Call usage learning in

gray seals, Halichoerus grypus. Journal of Comparative Psychology, 118,

447–454.Singer, W. (1999). Neuronal synchrony: A versatile code for the deWnition

of relations? Neuron, 24, 49–65.

Singer, W. (2001). Consciousness and the binding problem. Annals of the

New York Academy of Sciences, 929, 123–146.

Slocombe, K. E., & Zuberbuhler, K. (2005). Agonistic screams in wild

chimpanzees (Pan troglodytes schweinfurthii ) vary as a function of

social role. Journal of Comparative Psychology, 119, 67–77.

Smith, E. E., & Jonides, J. (1998). Neuroimaging analyses of human work-

ing memory. Proceedings of the National Academy of Sciences of the

United States of America, 95, 12061–12068.

Stowe, L. A. (2000). Sentence comprehension and the left inferior frontal

gyrus: Storage, not comprehension. Behavioral and Brain Sciences, 23, 51.

Stromswold, K., Caplan, D., Alpert, N., & Rauch, S. (1996). Localization

of syntactic comprehension by positron emission tomography. Brain

and Language, 52, 452–473.

Subiaul, F., Cantlon, J. F., Holloway, R. L., & Terrace, H. S. (2004). Cogni-

tive imitation in rhesus macaques. Science, 305, 407–410.

Szelag, E., & Pöppel, E. (2000). Temporal perception: A key to understand

language. Behavioral and Brain Sciences, 23, 52.

Tallon-Baudry, C., Bertrand, O., & Fischer, C. (2001). Oscillatory syn-

chrony between human extrastriate areas during visual short-term

memory maintenance. Journal of Neuroscience, 21, RC177.

Tallon-Baudry, C., Mandon, S., Freiwald, W. A., & Kreiter, A. K. (2004).

Oscillatory synchrony in the monkey temporal lobe correlates with

performance in a visual short-term memory task. Cerebral Cortex, 14,

713–720.

Tian, B., Reser, D., Durham, A., Kustov, A., & Rauschecker, J. P. (2001).

Functional specialization in rhesus monkey auditory cortex. Science,

292, 290–293.

Vogel, G. (1999). Chimps in the wild show stirrings of culture. Science, 284,

2070–2073.

Webster, R. I., & Shevell, M. I. (2004). Neurobiology of speciWc language

impairment. Journal of Child Neurology, 19, 471–481.

Whiten, A. (2005). The second inheritance system of chimpanzees and

humans.Nature, 437

, 52–55.Whiten, A., Horner, V., & de Waal, F. B. (2005). Conformity to cultural

norms of tool use in chimpanzees. Nature, 437 , 737–740.

Wilson, S. M., Saygin, A. P., Sereno, M. I., & Iacoboni, M. (2004). Listening

to speech activates motor areas involved in speech production. Nature

Neuroscience, 7 , 701–702.

Wise, R. J., Scott, S. K., Blank, S. C., Mummery, C. J., Murphy, K., & War-

burton, E. A. (2001). Separate neural subsystems within ‘Wernicke’s

area’. Brain, 124, 83–95.

Yuste, R., MacLean, J. N., Smith, J., & Lansner, A. (2005). The cortex as a

central pattern generator. Nature Reviews Neuroscience, 6 , 477–483.

Zatorre, R. J., & Belin, P. (2001). Spectral and temporal processing in

human auditory cortex. Cerebral Cortex, 11, 946–953.

Documents

Aboitiz, F & Al -Language Origins - Catalogo- 3-5906 (0117) IMPRESION PENDIENTE