Upload
adriana-veronica
View
215
Download
0
Embed Size (px)
Citation preview
7/29/2019 05cercetare
1/14
2000 John Wiley & Sons, Inc.
Peter M undyDepartment of Psychology
University of MiamiMiami, FL 33146
Judith Card
N athan FoxDepartment of Human Development
University of MarylandCollege Park, MD 20740
EEG Cor relates of the
D evelopm ent of I nfant Joint
Attention Skills
Received 19 August 1999; accepted 7 December 1999
ABSTRACT: The development of the capacity for social attention coordination, or jointattention, is a major milestone of infancy. Data from a recent study of handicapped infantshave raised the hypothesis that the tendency to initiate bids for joint attention may reflect
processes associated with the frontal cortex to a greater extent than other forms of infantattention coordination (R. Caplan et al., 1993). This hypothesis was examined in a longitudinalstudy of 32 normally developing infants. The results indicated that EEG data at 14 monthsindicative of left frontal, as well as left and right central cortical activity, was associated withthe tendency to initiate joint attention bids (IJA) at 14 and 18 months. In contrast, a patternof left parietal activation and right parietal deactivation at 14 months was associated with thedevelopment of the capacity to respond to the joint attention bids (RJA) of others at 14 and 18months. These results were interpreted to be consistent with a general anterior posterior modelof attention development (M. Posner & S. Petersen, 1990). The implications of these results
for current conceptualizations of joint attention development, as well as for understanding thedisturbance of joint attention skill development in autism are discussed. 2000 John Wiley &Sons Inc. Dev Psychobiol 36: 325338, 2000
Keywords: EEG; joint attention; infant development
The acquisition of the ability to coordinate attention
with a social partner is a major milestone of infancy
that is critical to infants active participation in social
learning opportunities (e.g., Adamson, 1995; Baldwin,
1993; Butterworth & Jarrett, 1991; Corkum & Moore,
1997; Mundy & Willoughby, 1998; Scaife & Bruner,
1975; Trevarthen, 1979; Tomasello, Kruger, & Ratner,
1993; Werner & Kaplan, 1963). Consistent with this
view, individual differences in this capacity among in-
fants have been observed to be significantly related to
Correspondence to: P. MundyContract grant sponsor: NICHDContract grant number: 26768Contract grant sponsor: NIDCDContract grant number: 00484
intellectual, language, and social development (e.g.,
Carpenter, Nagell, & Tomasello, 1998; Claussen,
Mundy, & Willoughby, 1999; Morales, Mundy, & Ro-
jas, 1998; Mundy & Gomes, 1998; Sheinkopf, Mundy,
Willoughby, & Claussen, 1999; Tomasello; 1995; Ul-
vund & Smith, 1996). Thus, understanding the nature
of individual differences in infant attention coordina-
tion is an important issue in the study of early devel-
opment (Mundy & Gomes, 1998).
Understanding these individual differences, how-
ever, is complicated by the observation that there are
different types of infant attention coordinating behav-
iors that may reflect distinct as well as common pro-
cesses (Mundy & Gomes, 1997). One category of be-
haviors has been referred to as protoimperative, or
7/29/2019 05cercetare
2/14
326 Mundy, Card, and Fox
requesting skills, in which infants initiate or respond
to bids for coordinated attention to elicit aid in obtain-
ing an object or event (Bates, Benigni, Bretherton, &
Camaioni, 1979; Bruner & Sherwood, 1983; Seibert,
Hogan, & Mundy, 1982). Examples include using eye
contact and reaching to obtain a distal toy, or respond-ing to a palm-up hand gesture to give an object to a
social partner. Another category of coordinated atten-
tion involves a less instrumental and more social func-
tion of sharing experience with others vis-a-vis an ob-
ject or event. These are called joint attention or
protodeclarative behaviors (Bates et al., 1979; Bruner
& Sherwood, 1983). As with requesting skill, infants
may initiate or respond to joint attention bids. In the
nomenclature of this article, responding to joint atten-
tion (RJA; Seibert et al., 1982) refers to the ability to
monitor and correctly follow gestures, such as point-
ing, and/or a shift in the direction of gaze and the head
orientation of others (Butterworth & Jarrett, 1991;Scaife & Bruner, 1975). Initiating joint attention skill
(IJA; Seibert et al., 1982) refers to the use of eye con-
tact and gestures, such as showing or alternating eye
contact, to spontaneously establish episodes of shared
attention with others vis-a-vis some object or event
(Bates, Camaioni, & Volterra, 1975; Mundy, Kasari,
& Sigman, 1992).
Recently, data have been presented that suggest that
individual differences in IJA may display a specific
association with frontal cortical processes. Caplan et
al. (1993) used Positron Emission Tomography (PET)
to examine cortical metabolism in a small sample of13 infants and toddlers prior to hemispherectomy for
intractable seizure disorder. Higher rates of preopera-
tive glucose metabolism in the prefrontal region, es-
pecially the left frontal region, was a positive predictor
of the postoperative tendency to initiate joint attention
bids but was not a predictor of other types of social
attention coordination skills. Thus, processes associ-
ated with the left frontal cortex may distinguish the
development of the tendency to initiate joint attention
bids relative to other infant attention coordinating be-
haviors. Several lines of theory are consistent with this
observation.
Working memory and related dual-task processing
(Stuss, Shallice, Alexander, & Picton, 1995), as well
as the representational encoding of stimuli (Goldman-
Rakic, 1987), may be a fundamental function of the
frontal cortex. Initiating joint attention skill may also
involve a working memory and representational de-
mands wherein infants hold information on line about
their own focus of interest (e.g., a toy) while attending
to and interacting with a social partner. Moreover,
these demands may be greater in IJA than in other
types of social attention coordinating bids, such as re-
questing acts (Baron-Cohen, 1989, 1995).
Frontal functioning may also be involved in the de-
velopment of infants ability to inhibit responses. For
example, infants are increasingly able to tolerate delay
in the A not B task in the first year of life (Diamond,1988) and this has been related to increased left frontal
EEG activation (Bell & Fox, 1992). Initiating joint
attention may involve inhibiting visual regard for an
object in order to share attention to a greater extent
than requesting skills (McEvoy, Rogers, & Penning-
ton, 1993). Indeed, behavioral response inhibition has
been associated with initiating joint attention skill, but
not other forms of infant attention coordination be-
haviors, in developmentally disordered children
(McEvoy et al., 1993; Giffith, Pennington, Wehner, &
Rogers, 1999).
Finally, in addition to cognitive processes, the de-
gree to which spontaneously sharing attention be-comes rewarding for infants may effect their tendency
to initiate joint attention bids (Mundy, 1995; Mundy
et al., 1992; Mundy & Willoughby, 1998). Alterna-
tively, social reward sensitivity or experience may
play a lesser role in the more instrumental functions
of requesting bids (Mundy, 1995). Frontal systems, in
turn, may play a role in integrating the reinforcement
value of the stimuli or motivational processes with
cognitive factors in the regulation of behavior
(Thorpe, Rolls, & Maddison, 1983). Moreover, a func-
tional lateralization has been observed such that, by
10 months, behaviors associated with positive indicesof social motivation, including social orienting, posi-
tive affect, and approach behaviors, are also related to
left frontal processes (Fox, 1991; Fox & Davidson,
1987). Thus, individual differences in a left frontal
system involved in the mediation of positive social
motivation may play a more important role in the de-
velopment of the capacity to initiate joint attention
bids than in other forms of infant attention coordina-
tion (Mundy, 1995; Mundy & Willoughby, 1998).
These elements of theory make a cogent case for
the involvement of frontal processes in IJA develop-
ment. However, the results of Caplan et al. (1993),
which provide an initial basis for this hypothesis, may
only be viewed as preliminary because they were
based on a small sample whose development was com-
plicated by severe neurological disturbance. If bona
fide, though, the observation of a specific linkage be-
tween frontal functions and initiating joint attention
skill development would be important for several rea-
sons. Such an observation may be important to under-
standing the nature of the robust disturbance in initi-
ating joint attention skill development that is a cardinal
7/29/2019 05cercetare
3/14
Cortical Activity and Joint Attention 327
symptom of autism (Mundy, 1995). Furthermore, it
may also enrich the understanding of the observed
connections between individual differences in infant
IJA skill and childhood IQ (Ulvund & Smith, 1996),
language development (Mundy & Gomes, 1998), at-
tachment (Claussen et al., 1999), and childhood socialcompetence (Sheinkopf et al., 1999; Sigman & Rus-
kin, 1999). Therefore, this study was designed to pro-
vide an a priori test of the frontal mediation hypothesis
of initiating joint attention in a sample of infants who
were not effected by neurological disturbance.
The question arises, however, as to how best to
investigate this putative brainbehavior relation.
Caplan et al. (1993) observed neurological predic-
tors of IJA development using baseline rather than
event-related measures of brain activity. Therefore, to
maintain consistency with the methodology of Caplan
et al. (1993), baseline measure of brain activity were
used in this study. However, here baseline EEG ratherthan PET data were utilized.
In this regard, it has been argued that baseline EEG
data may be a valid marker of important aspects of
brain maturation and integration that precedes the
emergence of skills at different points in infancy (Fi-
scher & Rose, 1994; Hudspeth & Pribram, 1992;
Thatcher, 1994), especially visual attention skills (Par-
melee et al., 1994). Thatcher (1994) has also argued
for the use of measures of baseline EEG coherence to
examine aspects of brain and behavior maturation. Co-
herence is a measure of phase synchrony or shared
activity between spatially separated [EEG] generators(Thatcher, 1994, p. 233). A two-component model of
coherence has been proposed in which maturation of
the left hemisphere may be reflected in a pattern of
integration of differentiation or a reduction in co-
herence among proximal cortical sites, followed by an
increase in coherence among more distant cortical sites
in baseline EEG (pp. 251254). Maturation of right
hemisphere functions may be characterized by dif-
ferentiation of integration (pp. 251254) or a reduc-
tion of distal coherence followed by an increase in
proximal coherence among cortical areas. Further-
more, coherence measures are assumed to reflect the
integration or organization of brain processes that are
involved in the acquisition phase of a skill. Thus, co-
herence measures may be markers of differences in
brain integration processes that precede the acquisition
or consolidation of a skill (Bell & Fox, 1996; Fischer
& Rose, 1994).
In accordance with this literature, baseline EEG
measures of brain activity and cortical coherence were
used in this study to examine the frontal mediation
hypothesis of initiating joint attention skill develop-
ment in the 14- to 18-month period, a period of con-
solidation for this skill (Adamson, 1995).
M ETH O D S
Participants
Thirty-six healthy, full-term 14-month-olds (18 girls,
18 boys) participated in this study. All of these tod-
dlers were born within 2 weeks of their due dates.
They required no oxygen or major medical interven-
tion after birth and were negative for neurological dis-
orders or complications. The toddlers were recruited
from a major metropolitan area via mailing lists com-
posed of parents with middle to upper-middle SES and
a minimum education of graduation from high school.
Of the mothers of children in this study, 3 (9%) had
advanced degrees or training, 25 (78%) had completedsome or all of college, and 4 (13%) had completed
high school. Ethnicity of the mothers was primarily
Caucasian American (29, 91%), two were Black
American and one was Latin American. Only toddlers
born to two-right handed parents were recruited for
this study. Missing or compromised EEG data on 4
infants reduced the sample to 32 infants (14 girls, 18
boys) with complete longitudinal data on all measures.
Procedures
The electrophysiological and joint attention data col-lection required approximately 90 min, and the tod-
dlers were seen within 10 days of each of their 14-,
16-, and 18-month birthdays.
Electrophysiological Recording. Brain electrical ac-
tivity (EEG) was recorded during the 14-month visit
from 12 head sites: frontal, central, temporal, parietal,
and occipital regions for both the left and right hem-
ispheres (F3, F4, F7, F8, C3, C4, T3, T4, P3, P4, O1,
O2) referenced to the vertex (Cz). Facial activity, such
as mouth and jaw movements, crying, or changes in
facial affect, may be expected to affect data from F7,
F8, T3, and T4 to a greater extent than from other sites.
Visual inspection from these sites confirmed that in a
number of instances these data were confounded with
high-frequency motor artifact. Therefore, data from
these sites were eliminated from the analyses.
Baseline EEG was recorded for 3 min while the
toddler sat quietly in a highchair next to his or her
mother. During EEG recording, the toddler attended
to a novel display of a rotating bingo wheel with
brightly colored balls. This procedure has been found
7/29/2019 05cercetare
4/14
328 Mundy, Card, and Fox
to be successful in garnering extended bouts of visual
attention while keeping the toddler quiet with reduced
eye movement and motor activity during the 3-min
period. The mother was instructed to refrain from talk-
ing or moving during the recording. The EEG was
recorded using a stretch lycra cap containing elec-trodes in the 10/20 placement system pattern (Jasper,
1958). After measuring the toddlers head to determine
the appropriate cap size and placing the cap on the
toddler, small amounts of abrasive gel and conductive
gel were inserted into the electrodes of interest. The
blunt end of a q-tip was used to gently abrade the scalp
after inserting each type of gel. Electrode impedances
were measured and accepted if below 5K ohms. Ad-
ditional abrading was sometimes necessary if initial
impedances measured greater than 5K ohms. Eye
movement (EOG) was recorded using Beckman min-
iature electrodes placed on the external canthus and
the supra orbit of the right eye.Prior to the recording of each subject, a 10-Hz .477
Vrms sine wave was input through each amplifier of
the polygraph. The amplifiers were set so that output
of the signal represented 50 uV peak to peak, with a
gain of 10,000. The EEG from each site of interest
was amplified using separate Grass amplifiers (Model
7P11) and bandpassed from 1 to 100 Hz, with a notch
filter at 60 Hz. The EEG signal was digitized on-line
at 512 samples per second for each channel to ensure
the data were not affected by aliasing. The raw data
were stored for later analysis. The EEG data were an-
alyzed using software by James Long Company. First,the EEG data were re-referenced via software to an
average reference configuration. The average refer-
enced EEG data were scored for eye movement and
motor artifact, and epochs containing artifacts were
eliminated from analysis. The data were analyzed with
a Discrete Fourier Transform (DFT) using a Hanning
window of 1 s with a 50% overlap. Prior to the com-
putation of the DFT, the mean voltage was subtracted
from each data point to eliminate any power results
due to DC offset. Power was computed for the 4- to
6-Hz and the 6- to 9-Hz frequency band. Past research
with infants has demonstrated that the majority of
spectral power can be found in this range, and espe-
cially these two bandwidths (see Calkins, Fox, & Mar-
shall, 1996). The power was expressed as mean square
microvolts and the data were transformed using the
natural log (ln) to normalize the distribution.
EEGANAL software was used to perform spectral
coherence calculations across EEG sites by averaging
the normalized complex cross-spectral density with
bands and epochs after the method of Saltzberg,
Burton, Burch, Fletcher, and Michaels (1986). Two
types of coherence variables were considered in this
study. A short-distance coherence variable between
frontal and central sites was computed within the 4-
to 6-Hz and 6- to 9-Hz bands for the 14-month EEG
data, as was a long-distance coherence variable be-
tween frontal and occipital sites. These two coherence
variables were computed separately for left and righthemisphere sites. Similar to previously used methods
(Thatcher, Krause, & Hrybyk, 1986), a summary co-
herence score for each hemisphere was calculated re-
flecting the ratio of short-distance coherence divided
by long-distance coherence (FrontalCentral Coher-
ence/FrontalOccipital Coherence).
Joint Attention Measures. Data on nonverbal joint at-
tention and requesting behaviors were collected with
the revised Early Social Communication Scales
(ESCS; Mundy, Hogan, & Doehring, 1996; Seibert et
al., 1982). The ESCS is a 20-min videotaped struc-
tured assessment designed to measure the develop-ment of a variety of nonverbal communication skills
in the 6- to 30-month period. For this assessment an
experimenter and an infant, sitting in his caregivers
lap or independently in a child chair, are seated facing
each other across a small table. A set of toys is visible
to the child but out of reach on the experimenters side
of the table. Posters are placed on the walls 90 degrees
to the childs left and right, and 180 degrees behind
the child. A video camera is positioned approximately
10 feet behind the experimenter. The camera is ori-
ented to capture a three-fourths face image of the child
with a profile view of the experimenter as well as theposition of the toys and posters.
The experimenter presents the child with a se-
quence of three activated wind-up toys (three trials
each), three hand-operated mechanical toys (three tri-
als each), opportunities to play a tickle, turn-taking
game (two trials), opportunities to play an object turn-
taking game, such as catch with a ball (two trials),
opportunities to take turns wearing a hat, comb, and
glasses (three trials), and an opportunity to look at pic-
tures in a book with the tester (one trial). The tester
also presents the child with multiple requests to give
toys to the tester. Finally, the tester presents the child
with two sets of three trials in which the tester attracts
the childs attention, and then turns to visually fixate
a wall poster while pointing at the poster and saying
the childs name three times with increasing emphasis.
Trials to the left, right, and behind the child are con-
ducted in each set.
Observations of the testerchild interaction in the
ESCS yielded frequency of behavior scores in six cat-
egories: Initiating Joint Attention (IJA); Responding
to Joint Attention (RJA), Initiating Behavioral Re-
questing (IBR), Responding to Behavioral Requesting
7/29/2019 05cercetare
5/14
Cortical Activity and Joint Attention 329
Table 1. Brief Description of the Early Social
Communication Scale Variables
INITIATES JOINT ATTENTION
(a) Makes eye contact while manipulating toy; (b) alter-
nates eye contact between active mechanical toy and tes-
ter; (c) points to active mechanical toy or distal objects intesting room; (d) shows objects (raises objects toward the
testers face).
RESPONDS TO JOINT ATTENTION
The percentage of trials the child correctly turns head and
eyes in direction of testers point. On side trials, direction
of gaze must shift beyond the testers extended finger (ap-
proximately 45 degrees off midline). On behind trials, the
child must turn head more than 90 degrees off midline.
INITIATES BEHAVIOR REQUESTS
(a) Makes eye contact when object moved out of reach or
reaches to objects out of reach; (b) Makes eye contact
while reaching to objects out of reach; (c) Points to inac-
tive objects on the table or to the collection of visible but
out-of-reach toys; (d) Gives inactive toys to the tester
(e.g., moves toys toward testers hands).
RESPONDS TO BEHAVIOR REQUESTS
The frequency of trials on which the child correctly re-
sponds to testers gestural (i.e., palm-up hand extended)
and verbal request to give it to me.
(RBR), Initiating Social Interaction (ISI), and Re-
sponding to Social Interaction (RSI). Both the Joint
Attention and Behavioral Requesting involve the co-
ordination of attention to objects and events. Alter-
natively, the Social Interaction scales assess turn-tak-
ing and interaction maintenance but not necessarilycoordination of attention to objects and events. There-
fore, given the focus of this study, only data from the
former will be considered in analyses. Briefly, these
are operationalized in the following manner. IJA
scores refer to the frequency with which the child
spontaneously points, shows, and uses eye contact to
share the experience of an active mechanical toy with
the tester. In the age range in this study, the sponta-
neous use of eye contact to alternate attention between
an object and social partner is the most common be-
havior scored on this measure. RJA refers to the per-
centage of trials on which a child correctly turns her
visual regard in the direction of the testers visual re-gard and pointing gesture. IBR scores refer to the fre-
quency with which the child uses eye contact, reach-
ing, giving, and pointing to elicit aid in obtaining
objects or reactivating objects. RBR refers to the fre-
quency of trials on which a child correctly responds
to the experimenters hand out, palm up gesture and
verbalization of give it to me while the child is hold-
ing or examining a toy. A more complete description
of the behaviors observed within each category is pre-
sented in Table 1. The raters were blind to the other
data collection procedures as well as the hypotheses
of this study.Reliability for the ESCS measures used in this
study are well established (e.g., Mundy & Gomes,
1998; Mundy, Kasari, Sigman, & Ruskin, 1995;
Mundy, Sigman, & Kasari, 1994). Estimates of inter-
rater reliability based on 12 independent paired obser-
vations of data for this study yielded rs .87, .95,
.82, & .79, p .001, for the total frequency scores for
IJA, RJA, IBR, and RBR, respectively. IJA displayed
a significant degree of stability (test-retest reliability)
in this study with correlations among the 14-, 16-, and
18-month IJA measures ranging from r(31) .57 to
.83, p .001. RJA also displayed evidence of stability
between the 14-month and 18-month measure,
r(31) .51, p .002. The relations between the 14-
and 16-month RJA measure and 16- and 18-month
measure approached significance, r(31) .25 and .28,
p .08 and .06, respectively. The IBR and RBR mea-
sures displayed no evidence of significant stability in
this study, r(31) range .13 to .24. Thus, the IJA
and RJA measures displayed more optimal psycho-
metric characteristics than did IBR and RBR in this
study.
Covariance among the different types of infant at-
tention coordination measures was modest. Of the pos-
sible 54 interscale correlations among the 14-, 16-, and18-month ESCS measures, just 12 were significant.
Across the types of joint attention measures, only 14-
month RJA was correlated with 14-month IJA, r
.36, p .05 (one tailed), and 16-month IJA, r .33,
p .05. However, at 18 months the IJA and RJA
correlation was r .05. IJA and IBR were not signif-
icantly correlated, but IJA was correlated with RBR at
18 months, r .34, p .05. Thus, the different ESCS
measures appeared to assess unique or distinct aspects
of the development of social attention coordination
skill in this study.
RESU LTS
D evelopment of Joint Attention Skil ls
The means of the four types of infant attention coor-
dination skills at the three ages of assessment are pre-
sented in Table 2. Preliminary analyses were con-
ducted to evaluate the effect of gender and age-related
changes on these measures. Because of their difference
in scaling (percentage data), RJA scores were first con-
7/29/2019 05cercetare
6/14
330 Mundy, Card, and Fox
Table 2. Means, with Standard Deviations in Parentheses, for the ESCS Variables at 14, 16, and 18 Months of Age
ESCS Variables 14 Months 16 Months 18 Months
Initiates joint attention (IJA)
Girls 19.5 (10.4) 16.1 (9.5) 19.8 (8.8)
Boys 15.9 (8.6) 14.7 (10.2) 16.3 (8.2)
Total 16.5 (8.0) 15.4 (10.1) 17.5 (8.6)Responds to joint attention (RJA)
Girls 87% (12%) 78% (25%) 81% (27%)
Boys 76% (25%) 81% (20%) 83% (23%)
Total 82% (20%) 81% (21%) 83% (24%)
Initiates behavior regulation (IBR)
Girls 33.6 (11.3) 35.0 (10.2) 41.5 (7.3)
Boys 30.5 (13.2) 33.6 (10.6) 36.1 (14.4)
Total 32.4 (12.0) 34.0 (10.7) 38.2 (12.4)
Responds to behavior regulation (RBR)
Girls 2.9 (1.2) 3.2 (1.3) 3.5 (1.4)
Boys 3.5 (1.5) 3.2 (1.7) 4.1 (2.3)
Total 3.4 (1.4) 3.2 (1.5) 3.9 (2.1)
sidered in a separate ANOVA using arc sine transfor-
mations. This analysis revealed no effects of gender
or age for RJA in this study. Next, a 2 3 3 (Gen-
der Age ESCS Scores) ANOVA was computed
for the IJA, IBR, and RBR variables. No effects as-
sociated with gender were significant. The main effect
for age was significant, F(2, 62) 3.68, p .05, but
the Age ESCS Scores interaction was not signifi-
cant.
The main effect for age indicated that the children
displayed a general increase in facility with coordi-nated attention bids with age (see Table 2). Pairwise
bonferronni comparisons for the main effect for age
revealed that 18-month-olds displayed significantly
higher ESCS scores than did 14-or 16-month-olds,
p .05. The 14- and 16-month-olds did not differ,
p .74. Within individual scales of the ESCS, this
effect reached significance for IBR on the 18-versus
14-month comparison, p .05. Therefore, to reduce
the data and constrain the number of analyses, only
data from the 14- and 18-month measures were con-
sidered in examinations of the relations between EEG
and ESCS variables in this study.
EEG Prediction of Joint Attention and O therN onverb al Skil ls
The covariance among the EEG data from the eight
leads (two frontal, two central, two parietal, and two
occipital) was considerable. For example, the average
correlation among the eight leads for the 4- to 6-Hz
band data was: r(30) .65, range .30 to .87. Av-
erage covariance for 6- to 9-Hz data was even
stronger: r .72, range .42 to .92. Consequently,
hierarchical multiple regression analyses (Cohen &
Cohen, 1983) were conducted to determine if 14-
month baseline EEG indices of left frontal activity
would display significant and unique predictive rela-
tions with the development of individual differences
in 18-month IJA. Analyses were also computed to
compare the associations of 14-month EEG data with
the three other ESCS measures at 18 monthsRJA,
IBR, and RBR. In each analysis, data from the left and
right hemisphere ratio EEG coherence scores (frontal
central coherence/frontal/occipital coherence) wereentered on Step 1. On Steps 2, 3, 4, and 5, the log
power data from the eight EEG leads (left and right
frontal, central, parietal, and occipital pairs) were en-
tered, respectively. This set order of data entry re-
flected the a priori emphasis in examining the relations
of ratio coherence and frontal EEG data with individ-
ual differences in joint attention. In addition, the 14-
month IJA and RJA scores were significantly corre-
lated with their respective 18-month scores (see
Methods) and were entered on the first step of analyses
of the 18-month IJA and RJA scores, respectively.
These regression analyses yielded a set of significant
equations for several of the different types of infant
attention coordination skills using EEG data from the
4- to 6-Hz band. However, none of the regression
equations using the 6- to 9-Hz band EEG data were
significant. Therefore, only the results of the former
have been reported in this article.
The results of the analyses for IJA and RJA are
presented in Tables 3 and 4. To be considered signif-
icant, a step in these analyses needed to be associated
both with a significant increase in R2 as well as a sig-
nificant overall effect for the regression equation. Data
7/29/2019 05cercetare
7/14
Cortical Activity and Joint Attention 331
Table 3. Significant 14-Month EEG Predictors of the 18-Month Initiating Joint Attention
Steps and Variables R R2a p
Step 1 (df 3/28) .67 .39 .001*
Left hemisphere coherence .37 .02*
Right hemisphere coherence .03
14-month IJA .49 .002*Step 2 (df 5/26) .69 .38 .003*
Left hemisphere coherence .35 .04*
Right hemisphere coherence .06
14-month IJA .53 .002*
Left frontal EEG .28
Right frontal EEG .30
Step 3 (df 7/24)b .77 .48 .001* (.05*)
Left hemisphere coherence .30 .05*
Right hemisphere coherence .09
14-month IJA .61 .001*
Left frontal EEG .80 .025*
Right frontal EEG .18
Left central EEG .02
Right central EEG .70 .05*
Follow-up (df 4/27) .77 .52 .007*
Left hemisphere coherence .28 .05*
14-month IJA .61 .001*
Left frontal EEG .68 .012*
Left central EEG .73 .007*
aR2 estimate adjusted for sample size. bThe p value for a significant change in R2 is presented in parentheses after the p value for the entire
equation.
are presented up through those steps that met these
criteria. Follow-up analyses are also presented for
equations obtained after the removal of blocks of var-iables with nonsignificant, p .10, standardized re-
gression coefficients.
Step 1 of the analyses of 18-month IJA was signif-
icant (see Table 3). The 14-month IJA score was a
significant positive predictor of 18-month IJA. In ad-
dition, the left hemisphere ratio coherence score dis-
played a significant negative . On Step 2 of these
analyses, the addition of the left and right frontal EEG
power data did not yield a significant increase in R2.
However, on Step 3 a significant increase in R2 was
observed in the analyses of 18-month IJA with the
addition of 14-month central EEG power data (see Ta-
ble 3). A positive (hypoactivation) right central EEG
component at 14 months was a significant predictor of
18-month IJA scores. Moreover, a suppressor effect
was evident so that a unique and significant relation
of left frontal activation at 14 months with 18-month
IJA became apparent on this step after considering var-
iance in coherence and central EEG data. Thus, Step
3 of these analyses, as well as the follow-up analyses
(see Table 3), revealed that a combination of 14-month
baseline EEG measures including the left hemisphere
ratio coherence measure, left frontal activation, and
right central hypoactivation displayed unique paths of
association with subsequent individual differences in
IJA.To better understand the nature of the correlation
between 18-month IJA and 14-month EEG coherence,
we examined the individual components of this ratio
measure. Coherence between left frontal and occipital
sites at 14 months was not correlated with 18-month
IJA, r .11, but coherence between left frontal and
central sites was negatively correlated with 18-month
IJA, r .48, p .005. This negative correlation
suggests that lower coherence between left frontal and
central cortical sites at 14 months, possibly indicative
of individual differences in differentiation of left cor-
tical activity (Thatcher, 1994), was related to IJA de-
velopment at 18 months in this sample.
The data in Table 4 revealed that the pattern of
significant EEG predictors of RJA appeared to be quite
different from the pattern of predictors of IJA. Aside
from significant effects associated with 14-month RJA
observed on Step 1, these analyses revealed a signifi-
cant effect at Step 4 with the addition of the log power
EEG data from the parietal electrodes. As can be seen
most clearly in the follow-up analysis, after removing
other EEG variables in the EEG data set, both indices
of left parietal activation and right parietal hypoacti-
7/29/2019 05cercetare
8/14
332 Mundy, Card, and Fox
Table 4. Significant 14-Month EEG Predictors of the 18-Month Responding to Joint Attention
Steps and Variables R R2a p
Step 1 (df 3/28) .56 .24 .012*
Left hemisphere coherence .19
Right hemisphere coherence .20
14-month RJA .56 .002*Step 2 (df 5/26) .58 .21 .05*
Left hemisphere coherence .18
Right hemisphere coherence .15
14-month RJA .55 .003*
Left frontal EEG .08
Right frontal EEG .19
Step 3 (df 7/24)b .62 .21 .075
Left hemisphere coherence .17
Right hemisphere coherence .13
14-month RJA .62 .001*
Left frontal EEG .48
Right frontal EEG .19
Left central EEG .44
Right central EEG .03
Step 4 (df 9/22) .72 .33 .05* (.05*)
Left hemisphere coherence .07
Right hemisphere coherence .08
14-month RJA .41 .05*
Left frontal EEG .19
Right frontal EEG .06
Left central EEG .33
Right central EEG .10
Left parietal 1.10 .05*
Right parietal .51
Follow-up (df 3/28) .63 .33 .003*
14-month RJA .40 .025*
Left parietal .89 .025*Right parietal .85 .03*
aR2 estimate adjusted for sample size. bThe p value for a significant change in R2 is presented in parentheses after the p value for the entire
equation.
vation displayed significant paths of association with
RJA at 18 months (see Table 4).
The analyses of IBR and RBR also revealed distinct
patterns of data. None of the steps in the analyses of
IBR approached significance. In these analyses, only
activation of the left parietal EEG power data at 14
months approached significance in predicting 18-
month scores, .87, p .10. In contrast, a sig-
nificant regression equation, R .57, F(4, 28) 3.32,
p .025, and a significant increase in adjusted R2,
R2 .16, F 4.01, p .03, was observed for the
18-month RBR variable, on Step 2, with the entry of
the frontal EEG log power data. However, unlike with
the IJA data, a right frontal activation component,
.82, p .009, and a left frontal hypoactivation,
.72, p .02, were associated with IBR. Follow-
up analyses revealed that these two frontal variables
alone were associated with RBR, R .49, adjusted
R2 .19, p .02; right frontal activation, .89,
p .004, and left frontal hypoactivation, .71,
p .02.
Concurrent Correlat ions Betw een the EEG
and ESCS VariablesThe patterns of concurrent multiple correlations be-
tween the EEG and ESCS variables were also exam-
ined at 14 and 18 months using hierarchical regression
analyses with the same order of data entry as previ-
ously described for the predictive regression equa-
tions. The analyses of concurrent correlates of IJA at
14 months yielded a marginally significant regression
equation (see Table 5). Nevertheless, a combination of
the left hemisphere frontal coherence ratio, as well as
7/29/2019 05cercetare
9/14
Cortical Activity and Joint Attention 333
Table 5. Concurrent EEG Correlates of IJA at 14 Months Initiating Joint Attention
Steps and Variables R R2a p
Step 1 (df 2/29) .25 .01
Left hemisphere coherence .26
Right hemisphere coherence .11
Step 2 (df 4/27) .38 .03Left hemisphere coherence .29
Right hemisphere coherence .10
Left frontal EEG .52
Right frontal EEG .42
Step 3 (df 6/25)b .53 .13 .078* (.078*)
Left hemisphere coherence .35 .05*
Right hemisphere coherence .11
Left frontal EEG .42
Right frontal EEG .20
Left central EEG .68 .07*
Right central EEG .78 .04*
Follow-up (df 3/28) .49 .16 .007*
Left hemisphere coherence .30 .06*
Left central EEG .85 .009*
Right central EEG .76 .02*
aR2 estimate adjusted for sample size. bThe p value for a significant change in R2 is presented in parentheses after the p value for the entire
equation.
left central EEG hypoactivation and right central EEG
activation, displayed unique paths of association with
14-month IJA (see Table 5).
In these data, though, neither of the individual com-
ponents of the coherence measure were correlatedwith
14-month IJA: left frontal and left central component,r .14, left frontal and left occipital component,
r .13.
The results of the other 14-month concurrent anal-
yses may be summarized as follows. For RJA, a sig-
nificant effect associated with the increase in adjusted
R2, R .58, R2 .20, adjusted R .10, p .05,
was again observed for Step 4 of the analyses with the
addition of the parietal data. Left parietal activation,
1.2, p .02, and right parietal hypo-activation,
.88, p .065, were associated with 14-month
RJA. However, follow-up analyses did not reveal ef-
fects for parietal processes when considered in isola-
tion from the other EEG variables. Analyses of IBR
at 14 months yielded a significant effect for Step 1,
R .43, p .055, with follow-up analyses indicating
that relatively greater short distance left frontal to cen-
tral coherence was associated with IBR at 14 months,
r .39, p .03. Alternatively, a marginally signifi-
cant effect on Step 1 for the analyses of RBR was also
observed, R .41, p .07, due to an association
between greater right hemisphere long distance frontal
to occipital coherence, r .34, p .056.
Only two significant effects were observed for the
concurrent 18-month analyses, and both of these sug-
gested a shift from 14 to 18 months in the brain activ-
ity correlates of IJA and RJA. For the analyses of both
IJA and RJA, marginal to significant increases in ad-
justed R2
were observed for Step 5 with the additionof the 18-month occipital data, R .63, R2 .20,
adjusted R2 .09, p .06 for IJA, and R .63,
R2 .24, adjusted R2 .10, p .05 for RJA. Fol-
low-up analyses revealed that only left occipital hy-
poactivation was associated with 18-month IJA, r
.44, p .015. Alternatively, a pattern of right occipital
hypoactivation, .60, p .01, and right central
activation, .66, p .006, was associated with
RJA at 18 months, R .51, adjusted R2 .21, p
.015.
D ISCU SSIO N
An important feature of the results of this study was
that individual differences in baseline measures of left
frontal brain activity were uniquely and specifically
related to the subsequent development of infant IJA in
this study of normally developing infants. This obser-
vation was consistent with the findings of Caplan et
al. (1993) and provides further support for the hypoth-
esized involvement of frontal process in IJA devel-
7/29/2019 05cercetare
10/14
334 Mundy, Card, and Fox
opment (Mundy, 1995). Unexpectedly, though, left
central activity was also associated with IJA devel-
opment. Furthermore, different types of infant social
attention coordination skills were related to different
patterns of cortical activity. Because aspects of this
pattern of results were not anticipated, it may be usefulto go beyond theory reviewed in the Introduction on
the frontal processes that may be associated with IJA
and consider theory on the early development of at-
tention regulation more broadly conceived.
The emergence of attention regulation in infancy
has been described in terms of an anteriorposterior
model of development (Posner & Petersen, 1990;
Rothbart, Posner, & Rosicky; 1994; Stuss et al., 1995).
The posterior component of this system is thought to
develop before the anterior component (Rothbart et al.,
1994). Between 3 and 6 months of age, infants become
capable of shifting attention by inhibiting or disengag-
ing attention from an immediate focus ( Johnson, Pos-ner, & Rothbart, 1991). The development of this ca-
pacity is thought to reflect a posterior orienting
attention system regulated, in part, by components of
the parietal cortex as well as associated midbrain and
thalamic areas (Posner & Petersen, 1990). The regu-
lation of behavior via this system may be best thought
of in terms of implicit learning, where this refers to
the action of relatively less voluntary neurobehavioral
processes (Rothbart et al., 1994).
From this theoretical perspective, the data in this
study suggest that responding to joint attention skill
development may reflect the operations of this poste-riorparietal attention system to some significant ex-
tent. The parietal lobe function of enabling shifts of
attention by disengaging attention from its current fo-
cus (Rothbart et al., 1994, p. 637) may be employed
when an infant redirects his or her attention in re-
sponse to the head and gaze shift of an experimenter
on an RJA trial. Furthermore, RJA functions appear
to become part of many infants behavioral repertoire
by 6 months of age (Butterworth, 1995; Morales et al.,
1998; Scaife & Bruner, 1975), and data also suggest
that the parietal orienting system becomes functional
just prior to this age, in the 4- to 6-month period (John-
son et al., 1991).
Other circumstantial evidence points to a link be-
tween RJA and parietal lobe functioning. The parietal
lobes, in conjunction with occipital functions, may
serve to encode spatial location of stimuli relative to
body position and eye orientation (Andersen &
Mountcastle, 1983; Goldman-Rakic, 1987; Motter,
Steinmetz, Duffy, & Mountcastle, 1987). This is con-
sistent with the hypothesized importance of spatial an-
alytic skill in the acquisition and development of RJA
skill (Butterworth, 1995; Butterworth & Cochran,
1980; Butterworth & Jarrett, 1991). In addition, recall
that RJA skill has been linked to early receptive lan-
guage development (Baldwin, 1991, 1993; Morales et
al., 1998; Mundy & Gomes, 1998; Mundy et al.,
1995). Similarly, cortical evoked response data sug-
gest that the left parietal as well as the left temporalprocesses are involved in the discrimination of com-
prehended versus noncomprehended words in the sec-
ond year (Mills, Coffey-Corina, & Neville, 1994).
Thus, there are numerous strands of theory and re-
search that are consistent with the linkage observed
here between parietal EEG and RJA.
Alternatively, the frontal correlates of IJA, and to
a lesser extent IBR and RBR, may reflect the influence
and maturation of an anterior attention regulation net-
work. This network becomes functional after the pos-
terior parietal system, and is manifest in increasing
volitional control of attention deployment (Rothbart et
al., 1994). The anterior attention system plays a centralrole in the capacity to share attention across dual tasks
or foci of attention (Stuss et al., 1995), as well as in
the regulation of voluntary, goal-directed orienting as
affected by both cognitive and motivational constraint
and activation parameters (Neafsey, Terreberry, Hur-
ley, Ruit, & Frysztak, 1993; Rothbart et al., 1994).
Thus, consistent with theory espoused in the Introduc-
tion, the connection of IJA to a frontal anterior atten-
tion system may reflect cognitive, executive, and/or
motivational processes.
There is also some evidence that the dorsolateral
and midfrontal cortex, including the anterior cingulategyrus, may contribute to this anterior executive atten-
tion network (Cummings, 1995; Rothbart et al., 1994;
Stuss et al., 1995). This area, especially the cingulate
gyrus, has interconnections to the limbic system as
well as the central motor areas (Rothbart et al., 1994),
including those involved in head and eye movements
involved in attention and orienting (Neafsey et al.,
1993). The latter connections may provide a starting
point in considering why an integrated pattern of 14-
month left frontal and central cortical components was
associated with 18-month IJA, and to a lesser degree
14-month IJA. The results suggested that, at 14
months, a pattern of right central deactivation and left
frontal activation as well as a decrease in the syn-
chrony of activation of left frontal and central cortical
sites was related to IJA development. This pattern, es-
pecially the latter component, suggests that IJA in the
second year may be related to developmental brain-
maturation processes involving the differentiation of
left cortical functions (Thatcher, 1994). In particular,
IJA development at 18 months may have been pre-
saged by the differentiation and emphasis of frontal
relative to central contributions to attention regulation.
7/29/2019 05cercetare
11/14
Cortical Activity and Joint Attention 335
Alternatively, concurrent correlations at 14 months
suggested that, although IJA was beginning to become
associated with a frontal central differentiation, central
components were primary to IJA at this point in de-
velopment.
Of course, such a rich interpretation of a single dataset may be premature. Caution should be exercised in
interpreting this relatively unprecedented data set.
Nevertheless, this analysis serves to facilitate a poten-
tially edifying integration between more general as-
pects of research on human attention processes (e.g.,
Posner & Petersen, 1990; Rothbart et al., 1994) and
contemporary research on infant social attention co-
ordination (e.g., Baldwin, 1991; Baron-Cohen, 1995;
Corkum & Moore, 1997; Mundy & Gomes, 1998)
that, heretofore, has gone unrecognized. For example,
the notion that IJA and RJA may, respectively, reflect
a later developing anterior attention regulation net-
work versus an earlier arising parietal attention regu-lation network may assist in understanding why these
measures have been observed to display different pat-
terns of behavioral correlates in typical and atypical
samples (Claussen et al., 1999; Mundy & Gomes,
1998; Sigman & Ruskin, 1999; Ulvund & Smith,
1996).
This dual neural-network hypothesis of joint atten-
tion development may also have implications for un-
derstanding the disturbance in this skill domain that is
characteristic of autism (Mundy, 1995). Children with
autism display deficits in both IJA and RJA, with the
former being more robust with development than thelatter (Mundy et al., 1994; Sigman & Ruskin, 1999).
The data in this study lead to the suggestion that both
left frontal and parietal processes may be involved in
this area of disturbance for children with autism. This
notion is consistent with other research on autism. For
example, abnormal seretonin synthesis in the left fron-
tal hemisphere may be characteristic of a substantial
number of children with autism (Chugani et al., 1997).
Recent functional MRI (fMRI) data have also sug-
gested that socialcognitive task performance may be
associated with a left medial frontal system of activity,
and that individual disorders related to autism may
display a disturbance in the functions of this medial
frontal system (Fletcher et al., 1995; Happe et al.,
1996; for discussion see Mundy & Neal, in press).
Indeed, the combination of results of these fMRI stud-
ies and this study provides some support for the hy-
pothesis that deficits observed in children with autism
in joint attention skill as well as in later socialcog-
nitive, or so-called Theory of Mind facility, may be
linked in some fundamental fashion (Baron-Cohen,
1995; Mundy & Neal, in press). Finally, studies have
also reported observations of parietal lobe abnormal-
ities in individuals with autism (Piven, Arndt, Bailey,
& Andreasen, 1996), as well as individuals with the
often-related disorder of fragile X syndrome (Schapiro
et al., 1995).
This dual neural-network hypothesis of joint atten-
tion development may also prove instructive with re-gard to a prevailing notion that all forms of infant so-
cial attention coordination primarily reflect a common
epistemological process, such as understanding inten-
tions in self and other (Carpenter et al., 1998; Toma-
sello, 1995; Wellman, 1993), or a single modular sys-
tem of socialcognitive development (Baron-Cohen,
1995). In contrast, the relative lack of significant cor-
relations among infant social attention coordination
measures observed here, and the differential pattern of
their correlations with EEG data, was consistent with
theory that suggests that different types of infant at-
tention coordination acts may reflect distinct constel-
lations and integrations of neurological, psychologi-cal, and experiential processes as well as common
processes (Mundy, 1995; Mundy & Gomes, 1997).
Thus, in the study of the development of infant atten-
tion coordination skills, it may be useful to consider
the possibility that different skills reflect divergent as
well as convergent processes in their development.
The data also provided some support for Fischer
and Roses (1994) notion that, at different points in
the development of a skill, different integrations of
frontal, central, parietal, and occipital EEG associa-
tions may be manifest. Indeed, based on data from
Hudspeth and Pribram (1992), Fischer and Rose sug-gested that more anterior brain functions may be in-
volved in the early phases of skill development,
whereas more posterior brain functions may underpin
later phases of consolidation. The transition from con-
current and predictive associations with a frontal/cen-
tral system for IJA and a parietal system for RJA at
14 months to concurrent associations with an occipital
activity for both variables by 18 months in this study
was consistent with this view of a complex, shifting
pattern of cortical correlates of behavioral develop-
ment.
Finally, several methodological issues bear men-
tion. First, all the parents of infants in this study were
right-handed. Perhaps, then, the left hemisphere as-
sociations in this study reflected a bias in infants use
of their right hands to point or gesture. This issue war-
rants further consideration. However, similar behav-
iors, such as pointing, were observed in both the IJA
and IBR measures in this study (see Table 1), but these
measures had different patterns of cortical correlates.
Hence, it seems unlikely that a right-handed bias could
fully account for left hemisphere brainbehavior re-
lations observed in this study.
7/29/2019 05cercetare
12/14
336 Mundy, Card, and Fox
Second, it is important to note that the 14- to 18-
month period of this study may be especially sensitive
to consolidation of individual differences in IJA skills.
If frontal functions are generally prominent during
sensitive periods of skill development (Fischer &
Rose, 1994), then the specific association of IJA withleft frontal EEG activation and frontal EEG coherence
may have been observed only because of the devel-
opmental window chosen for study. For example, the
peak consolidation period for RJA may be somewhere
in the 6- to 15-month period (Butterworth & Jarrett,
1991; Morales et al., 1998; Scaife & Bruner, 1975).
Perhaps examination of the EEG correlates of RJA in
that period would yield a different and comparably
complex pattern of cortical correlates.
Finally, the IJA measure displayed the strongest
and most consistent evidence of longitudinal stability
or test-retest reliability in this study. This difference
in the psychometric properties of the variables understudy could have effected the pattern of the results.
However, the stability of the IJA measure may also
attest to its relative importance. IJA may be a valid
index of a variety of cognitive, temperamental, and
environmental factors that culminate in individual dif-
ferences in infants tendencies to self-organize and
contribute to opportunities for social observational
learning (Claussen et al., 1999; Mundy & Neal, in
press; Ulvund & Smith, 1996) and these opportunities
may be critical to fostering young childrens cognitive
assimilation of cultural information and adaptive so-
cial development (e.g., Adamson, 1995; Bruner, 1975;Mundy & Willoughby, 1998; Tomasello et al., 1993;
Trevarthen, 1979; Ulvund & Smith, 1996). As such,
IJA, and the capacity to initiate sharing of information
with others, may be a major milestone of early devel-
opment that serves as a behavioral fulcrum around
which multiple domains are integrated and organized
early in development (Mundy, 1995). Hence, the
unique frontal component and relative complexity of
the pattern of cortical correlates of IJA observed in
this study may be consistent with the hypothesized
central importance of this domain for early develop-
ment.
REFEREN CES
Adamson, L. (1995). Communication development during
infancy. Madison, WI: Brown & Benchmark.
Andersen, R., & Mountcastle, V. (1983). The influence of
angle of gaze upon the sensitivity of light-sensitive neu-
rons of the posterior parietal cortex. Journal of Neurosci-
ence, 3, 532548.
Baldwin, D. (1991). Infants contribution to the achievement
of joint reference. Child Development, 63, 875 890.
Baldwin, D. (1993). Early referential understanding: Infants
ability to recognize referential acts for what they are. De-
velopmental Psychology, 29, 832 843.
Baron-Cohen, S. (1989). Joint attention deficits in autism:
Towards a cognitive analysis. Development and Psycho-pathology, 1, 185189.
Baron-Cohen, S. (1995). Mindblindness. Cambridge, MA:
MIT Press.
Bates, E., Benigni, L., Bretherton, I., & Camaioni, L. (1979).
The emergence of symbols: Cognition and communica-
tion in infancy. New York: Academic Press.
Bates, E., Camaioni, L., & Volterra, V. (1975). The acqui-
sition of performatives prior to speech. Merrill-Palmer
Quarterly, 21, 205224.
Bell, M. A., & Fox, N. A. (1992). The relations between
frontal brain electrical activity and cognitive development
during infancy. Child Development, 63, 1142 1163.
Bell, M. A., & Fox, N. A. (1996). Crawling experience isrelated to changes in cortical organization during infancy:
Evidence from EEG coherence. Developmental Psycho-
biology, 29, 551561.
Bruner, J. (1975). From communication to language: A psy-
chological perspective. Cognition, 3, 255 287.
Bruner, J., & Sherwood, V. (1983). Thought, language, and
interaction in infancy. In J. Call, E. Galenson, & R. Tyson
(Eds.), Frontiers of infant psychiatry (pp. 5 25). New
York: Basic Books.
Butterworth, G. (1995). Origins of mind in perceptions and
action. In C. Moore & P. Dunham (Eds.), Joint attention:
Its origins and role in development (pp. 29 40). Hillsdale,
NJ: Erlbaum.
Butterworth, G., & Cochran, E. (1980). Towards a mecha-
nism of joint visual attention in human infancy. Interna-
tional Journal of Behavioral Development, 3, 253 272.
Butterworth, G., & Jarrett, N. (1991). What minds have in
common is space: Spatial mechanisms in serving joint
visual attention in infancy. British Journal of Develop-
mental Psychology, 9, 5572.
Calkins, S. D., Fox, N. A., & Marshall, T. R. (1996). Be-
havioral and physiological antecedents of inhibited and
uninhibited behavior. Child Development, 67, 523 540.
Caplan, R., Chugani, H., Messa, C., Guthrie, D., Sigman,
M., Traversay, J., & Mundy, P. (1993). Hemispherectomy
for early onset intractable seizures: Presurgical cerebral
glucose metabolism and postsurgical nonverbal commu-nication patterns. Developmental Medicine and Child
Neurology, 35, 574581.
Carpenter, M., Nagell, K., & Tomasello, M. (1998). Social
cognition, joint attention, and communicative competence
from 9 to 15 months of age. Monographs of the Society
of Research in Child Development, 63(Serial No. 4).
Chugani, D., Muzik, O., Rothermel, R., Behen, M., Chak-
raborty, P., Mangner, T., da Silva, E., & Chugani, H.
(1997). Altered serotonin synthesis in the denatothlamo-
cortical pathway in autistic boys. Annals of Neurology,
42, 666 669.
7/29/2019 05cercetare
13/14
Cortical Activity and Joint Attention 337
Claussen, A., Mundy, P., & Willoughby, J. (submitted).
Joint attention and attachment in infants at risk. (Paper
originally presented at the International Society on Infant
Studies, April, 1998, Atlanta).
Cohen, J., & Cohen, P. (1983). Applied multiple regression/
correlation analysis for the behavioral sciences. Hillsdale,
NJ: Erlbaum.Corkum, V., & Moore, C. (1997). The origins of joint atten-
tion. Developmental Psychology, 34, 28 38.
Cummings, J. (1995). Anatomic and behavioral aspects of
frontal-subcortical circuits. In G. Jordan, K. Holyoak, et
al. (Eds.), Annals of the New York Academy of Sciences,
769, (pp. 113). New York: New York Academy of Sci-
ences.
Diamond, A. (1988). Abilities and neural mechanisms un-
derlying AB performance. Child Development, 59, 523
527.
Fischer, K., & Rose, S. (1994). Dynamic development of
coordination of components in brain and behavior: A
framework for theory and research. In G. Dawson & K.Fischer (Eds.), Human behavior and the developing brain
(pp. 366). New York: Guilford Press.
Fletcher, P., Happe, F., Frith, U., Baker, S., Sloan, R., Frac-
kowiak, R., & Frith, C. (1995). Other minds in the brain:
A functional imaging study of theory of mind in story
comprehension. Cognition, 57, 109 128.
Fox, N. (1991). Its not left, its right: Electroencephalo-
graph asymmetry and the development of emotion. Amer-
ican Psychologist, 46, 863872.
Fox, N., & Davidson, R. (1987). EEG asymmetry in 10-
month-old infants in response to approach of a stranger
and maternal separation. Developmental Psychology, 23,
233240.
Griffith, E., Pennington, B., Wehner, E., & Rogers, S.
(1999). Executive functions in children with autism. Child
Development, 70, 817832.
Goldman-Rakic, P. (1987). Circuitry of primate prefrontal
cortex and regulation of behavior by representational
memory. In B. Plum (Ed.), The handbook of physiology,
the nervous system, and higher brain functions (pp. 373
417). Bethesda, MD: American Physiological Society.
Happe, F., Ehlers, S., Fletcher, P., Frith, U., Johansson, M.,
Gillberg, C., Dolan, R., Frackowiak, R., & Frith, C.
(1996). Theory of mind in the brain. Evidence from a PET
scan study of Asperger syndrome. Neuroreport: An Inter-
national Journal for the Rapid Communication of Re-
search in Neuroscience, 8, 197201.Hudspeth, W., & Pribram, K. (1992). Psychophysiological
indices of cerebral maturation. International Journal of
Psychophyiosology, 12, 19 29.
Jasper, H. (1958). The 10/20 international electrode system.
EEG and Clinical Neurophysiology, 10, 371375.
Johnson, M., Posner, M., & Rothbart, M. (1991). Compo-
nents of visual orienting in early infancy: Contingency
learning, anticipatory looking, and disengaging. Journal
of Cognitive Neuroscience, 3, 335 344.
McEvoy, R., Rogers, S., & Pennington, R. (1993). Executive
function and social communication deficits in young au-
tistic children. Journal of Child Psychology and Psychi-
atry, 34, 563578.
Mills, D., Coffey-Corina, S., & Neville, H. (1994). Varia-
bility in cerebral organization during primary language
acquisition. In G. Dawson & K. Fischer (Eds.), Human
behavior and the developing brain (pp. 427455). New
York: Guilford Press.Morales, M., Mundy, P., & Rojas, J. (1998). Gaze following
and language development in 6-month-olds. Infant Be-
havior and Development, 21, 373377.
Motter, B., Steinmetz, M., Duffy, C., & Mountcastle, V.
(1987). Functional properties of parietal visual neurons:
Mechanism of directionality along a single axis. Journal
of Neuroscience, 7, 154176.
Mundy, P. (1995). Joint attention and socialemotional ap-
proach behavior in children with autism. Development
and Psychopathology, 7, 6382.
Mundy, P., & Gomes, A. (1997). A skills approach to com-
munication development: Lessons learned from research
with children with developmental disabilities. In L. Ad-amson & M. Romski (Eds.), Research on communication
and language disorders (pp.107132). New York: Paul
Brookes.
Mundy, P., & Gomes, A. (1998). Individual differences in
joint attention skill development in the second year. Infant
Behavior and Development, 21, 469482.
Mundy, P., Hogan, A., & Doehring, P. (1996). A preliminary
manual for the abridged Early Social-Communication
Scales. Coral Gables, FL: University of Miami,
www.psy.miami.edu/ faculty/pmundy.
Mundy, P., Kasari, C., & Sigman, M. (1992). Joint attention,
affective sharing, and intersubjectivity. Infant Behavior
and Development, 15, 377381.
Mundy, P., Kasari, C., Sigman, M., & Ruskin, E. (1995).
Nonverbal communication and early language in Down
syndrome and in normally developing children. Journal
of Speech and Hearing Research, 38, 157167.
Mundy, P., & Neal, R. (in press). Neural plasticity, joint
attention, and autistic developmental pathology. In L.
Glidden (Ed.), International Review of Mental Retarda-
tion Research, Vol. 27.
Mundy, P., Sigman, M., & Kasari, C. (1994). Joint attention,
developmental level, and symptom presentation in autism.
Development and Psychopathology, 6, 389 402.
Mundy, P., & Willoughby, J. (1998). Nonverbal communi-
cation, affect, and social emotional development. In A.
Wetherby, S. Warren, & J. Reichle (Eds.), Transitions inprelinguistic communication: Preintentional to intentional
and presymbolic to symbolic (pp. 111134). Baltimore,
MD: Brookes.
Neafsey, E., Terreberry, R., Hurley, K., Ruit, K., & Frysztak,
R. (1993). Anterior cingulate cortex of rodents: Connec-
tions, visceral control functions, and implications for
emotion. In B. Vogt & M. Gabriel (Eds.), Neurobiology
of the cingulate cortex and limbic thalamus: A Compre-
hensive handbook (pp. 206 223). Boston: Birkhauser.
Parmelee, A., Sigman, M., Garbanati, J., Cohen, S., Beck-
with, L., & Asarnow, R. (1994). Neonatal electroenceph-
7/29/2019 05cercetare
14/14
338 Mundy, Card, and Fox
alographic organization and attention in early adoles-
cence. In G. Dawson & K. Fischer (Eds.), Human
behavior and the developing brain (pp. 537554). New
York: Guilford Press.
Piven, J., Arndt, S., Bailey, J., & Adreasen, N. (1996). Re-
gional brain enlargement in autism: A magnetic resonance
imaging study. Journal of the American Academy ofChild and Adolescent Psychiatry, 35, 530536.
Posner, M., & Petersen, S. (1990). The attention system of
the human brain. Annual Review of Neuroscience, 13,
2542.
Rothbart, M., Posner, M., & Rosicky, J. (1994). Orienting
in normal and pathological development. Development
and Psychopathology, 6, 635652.
Saltzberg, B., Burton, D. B., Burch, N. R., Fletcher, J., &
Michaels, R. (1986). Electro-physiological measures of
regional neural interactive coupling. Linear and nonlinear
dependence relationships among multiple channel electro-
encephalographic recordings. International Journal of
Bio-Medical Computing, 18, 77 87.
Scaife, M., & Bruner, J. (1975). The capacity for joint visual
attention in the infant. Nature, 253, 265266.
Schapiro, M., Murphy, D., Hagerman, R., Azari, N., Alex-
ander, G., Miezejeski, C., Hinton, V., Horowitz, B.,
Haxby, J., & Kumar, A. (1995). Adult fragile X syn-
drome: Neuropsychology, brain anatomy, and metabo-
lism. American Journal of Medical Genetics, 60, 480
493.
Seibert, J. M., Hogan, A. E., & Mundy, P. C. (1982). As-
sessing interactional competencies: The early social-com-
munication scales. Infant Mental Health Journal, 3, 244
245.
Sheinkopf, S., Mundy, P., Willoughby, J., & Claussen. A.
(1999, April). Joint attention in cocaine infants and 36-month behavioral outcome. Paper presented at the meet-
ing of the Society for Research in Child Development,
Albuquerque, NM.
Sigman, M. & Ruskin, E. (1999). Continuity and change in
the social competence of children with autism, Down
Syndrome, and developmental delays. Monographs of
the Society for Research in Child Development, 64,
Vol. 114.
Stuss, D., Shallice, T., Alexander, M., & Picton, T. (1995).
A multidisciplinary approach to anterior attentional func-
tions. In G. Jordan, K. Holyoak, & Boller, F. (Eds.), An-
nals of the New York Academy of Sciences, 769, (pp.191211). New York: New York Academy of Sciences.
Thatcher, R. (1994). Cyclical cortical reorganization: Ori-
gins of human cognitive development. In G. Dawson &
K. Fischer (Eds.), Human behavior and the developing
brain (pp. 232268). New York: Guilford Press.
Thatcher, R., Krause, P., & Hrybyk, M. (1986). Cortico-
cortical association fibers and EEG coherence: A two-
compartmental model. Electroencephalography and Clin-
ical Neurophy, 64, 123143.
Thorpe, S., Rolls, E., & Maddison, S. (1983). The orbitof-
rontal cortex: Neuronal activity in the behaving monkey.
Experimental Brain Research, 49, 93 115.
Tomasello, M. (1995). Joint attention as social cognition. In
C. Moore & P. Dunham (Eds.), Joint attention: Its origins
and role in development (pp. 103130). Hillsdale, NJ:
Erlbaum.
Tomasello, M., Kruger, A., & Ratner, A. (1993). Cultural
learning. Behavioral and Brain Sciences, 16, 495552.
Trevarthen, C. (1979). Communication and cooperation in
infancy: A description of primary intersubjectivity. In M.
Bullowa (Ed.), Before speech: The beginning of human
communication (pp. 321347). London: Cambridge Uni-
versity Press.
Ulvund, S., & Smith, L. (1996). The predictive validity of
nonverbal communication skills in infants with perinatal
hazards. Infant Behavior and Development, 19, 441449.
Wellman, H. (1993). Early understanding of mind: The nor-mal case. In S. Baron-Cohen, H., Tager-Flusberg, & D.
Cohen (Eds.), Understanding other minds (pp. 1039).
Oxford, England: Oxford University Press.
Werner, H., & Kaplan, S. (1963). Symbol formation. New
York: Wiley.