Corticostriatal connections of the superior temporal region in rhesus monkeys

Corticostriatal Connectionsof the Superior TemporalRegion in Rhesus Monkeys

E.H. YETERIAN1,2* AND D.N. PANDYA2,3

1Department of Psychology, Colby College, Waterville, Maine 049012Department of Anatomy and Neurobiology, Boston University School of Medicine,

Boston, Massachusetts 021183Harvard Neurological Unit, Beth Israel Hospital, Boston, Massachusetts 02215

ABSTRACTCorticostriatal connections of auditory areas within the supratemporal plane and in

rostral and caudal portions of the superior temporal gyrus were studied by the autoradio-graphic anterograde tracing technique. The results show that the primary auditory cortex haslimited projections to the caudoventral putamen and to the tail of the caudate nucleus. Incontrast, the second auditory area within the circular sulcus has connections to the rostraland the caudal putamen and to the body of the caudate nucleus and the tail. The associationareas of the superior temporal gyrus collectively have widespread corticostriatal projectionscharacterized by differential topographic distributions. The rostral part of the gyrus projectsto ventral portions of the head of the caudate nucleus and of the body and to the tail. Inaddition, there are connections to rostroventral and caudoventral portions of the putamen.The mid-portion of the gyrus projects to similar striatal regions, but the connections to thehead of the caudate nucleus are less extensive. Compared with the rostral and middle parts ofthe superior temporal gyrus, the caudal portion has little connectivity to the tail of the caudatenucleus. It projects more dorsally within the head and the body and also more dorsally withinthe caudal putamen. These differential patterns of corticostriatal connectivity are consistentwith functional specialization at the cortical level. J. Comp. Neurol. 399:384–402, 1998.r 1998 Wiley-Liss, Inc.

Indexing terms: auditory cortex; temporal; striatum; caudate; putamen

The cortical auditory system is located in the superiortemporal region in macaque monkeys. The primary audi-tory area (auditory koniocortex, architectonic area KA, orphysiologically defined area AI) has been shown to occupythe caudal portion of the supratemporal plane (e.g., Adesand Felder, 1942; Walzl and Woolsey, 1943; Merzenich andBrugge, 1973; Morel et al., 1993). Area KA is surroundedby parakoniocortical belt areas (e.g., Pandya and Sanides,1973; Burton and Jones, 1976; Jones and Burton, 1976;Galaburda and Pandya, 1983; Morel et al., 1993). Physi-ological investigations have suggested that these beltareas contain auditory representations (e.g., Merzenichand Brugge, 1973; Morel et al., 1993). Several studies havedemonstrated that the belt areas have distinctive patternsof corticocortical connectivity (e.g., Pandya et al., 1969;Jones and Powell, 1970; Pandya and Sanides, 1973; Chavisand Pandya, 1976; Galaburda and Pandya, 1983; Petridesand Pandya, 1988; Morel et al., 1993) and have specificthalamic relationships (e.g., Mesulam and Pandya, 1973;

Burton and Jones, 1976; Morel et al., 1993; Pandya et al.,1994).

The striatal connections of different cortical regionshave been studied in recent years by a number of investiga-tors. Although the corticostriatal projections of frontal,parietal, occipital, and inferior temporal areas have beenexamined in detail, relatively little information is avail-able regarding the auditory-related cortices of the superior

Grant sponsor: Department ofAnatomy and Neurobiology, Boston Univer-sity School of Medicine; Grant sponsor: Audrey and Sheldon Katz ResearchFund of Colby College; Grant sponsor: Colby College Social Science; Grantnumber: 01 2270.

A preliminary report of these findings was presented at the meeting ofthe Society for Neuroscience, New Orleans, LA, October 1997 (Yeterian andPandya, 1997).

*Correspondence to: Edward H. Yeterian, Ph.D., Colby College, 4781Mayflower Hill, Waterville, ME 04901–8855.E-mail: [email protected]

Received 25 September 1997; Revised 14 May 1998; Accepted 20 May1998

THE JOURNAL OF COMPARATIVE NEUROLOGY 399:384–402 (1998)

r 1998 WILEY-LISS, INC.

temporal region. Previous studies using degeneration path-way tracing methods have demonstrated the existence ofrestricted projections from certain portions of the superiortemporal gyrus (STG) to caudal sectors of the putamen andto the tail of the caudate nucleus (Whitlock and Nauta,1956; Kemp and Powell, 1970). Subsequent investigationsusing the autoradiographic anterograde pathway tracingtechnique have shown that the rostral portion of the STGprojects to the head and the body of the caudate nucleusand to the rostral putamen as well as to the caudalputamen and to the tail of the caudate nucleus (Yeterianand Van Hoesen, 1978; Van Hoesen et al., 1981; Selemonand Goldman-Rakic, 1985). Each of these studies waslimited in scope with regard to the superior temporalregion by focusing mainly on rostral portions of the STG.The corticostriatal connectivity of the supratemporal plane(STP) and of the caudal portion of the STG remains to bedelineated.

In recent years, there has been increasing interest in thefunctional roles of specific portions of the superior tempo-ral region (e.g., Colombo et al., 1990, 1996; Morel et al.,1993; Rauschecker et al., 1995, 1997). In particular, Co-lombo et al. (1996) indicated that there may be functionalstreams of auditory processing analogous to those of thecortical visual system (e.g., Mishkin et al., 1983; Van Essenand Maunsell, 1983). To understand more fully the neuralunderpinnings of differential roles of the superior tempo-ral cortices, detailed information regarding the connec-tional relationships of these regions may be useful. Al-though certain aspects of the connectivity of superiortemporal cortical areas have been studied extensively,namely corticocortical and thalamic relationships, thereremains only limited information regarding the striatalconnections of these areas. In the present investigation,therefore, the corticostriatal projections of various subdivi-sions of the STP and STG were examined by the autoradio-graphic anterograde pathway tracing technique.

MATERIALS AND METHODS

Corticostriatal connections of the superior temporalregion were traced in 15 rhesus monkeys (Macaca mu-latta) by using radiolabeled amino acids. After anesthetiz-ing each animal with sodium pentobarbital (15 mg/kg), acraniotomy was performed under aseptic conditions toexpose the superior temporal region. The site for isotopeinjections, with the exception of cases involving the supra-temporal plane (cases 1–4), was determined by sulcallandmarks. In cases 1 and 3, the primary auditory areawas located by recording click-evoked potentials from thetip of a specially constructed injection electrode (Saundersand Rosene, 1988). Areas in the STP were identified aftercarefully separating the arachnoid membrane and expos-ing the region. At each site, injections of 0.6–0.8 µl of amixture of [3H]-proline and [3H]-leucine (specific activity40–60 µCi/µl) were made. Following a postsurgery sur-vival period of 7–10 days, the animals were deeply anesthe-tized with sodium pentobarbital and perfused transcardi-ally with isotonic saline followed by 10% formalin. Thebrains were removed, and each hemisphere was dividedinto two blocks in the coronal stereotactic plane. Eachbrain was photographed, and the blocks were embedded inparaffin and cut into 10-µm-thick sections. Every twenti-eth section was processed for autoradioagraphy (Cowan etal., 1972). Following exposure times of 3–6 months, the

emulsion was developed, and the sections were stainedthrough the emulsion with thionin to permit the identifica-tion of cortical architecture, localization of the injectionsite, and identification of the boundaries of the striatum.The distribution of terminal label, as shown under dark-field illumination, was mapped onto coronal tracings of thecaudate nucleus and the putamen. From these tracings,the distribution of label was reconstructed on standardsagittal profiles of the two nuclei.

The nomenclature used for architectonic areas of thesuperior temporal region is that of Galaburda and Pandya(1983; Fig. 1). The experimental cases described belowhave been used in other investigations (Galaburda andPandya, 1983; Petrides and Pandya, 1988; Pandya et al.,1994). Photomicrographs of certain injection sites of casespresented in the present study have been shown in Pandyaet al. (1994); for case 1, see Figure 11E of Pandya et al.; forcase 2, see Figure 11C; for case 8, see Figure 5A; for case10, see Figure 15A; for case 11, see Figure 11A; for case 14,see Figure 15C.

Animal care was provided in accordance with the NIHGuide for Care and Use of Laboratory Animals.

RESULTS

The auditory regions of the supratemporal plane and thesuperior temporal gyrus in macaque monkeys have beendivided on the basis of architectonic and physiologicalcharacteristics. Architectonic studies have indicated thatthere are central core areas surrounded by belt regions(Pandya and Sanides, 1973; Galaburda and Pandya, 1983;Morel et al., 1993). Physiological investigations have dis-cerned the existence of multiple auditory representationssurrounding a primary auditory region (e.g., Merzenichand Brugge, 1973; Morel et al., 1993). Many of thephysiological representations correspond to architectoni-cally defined sectors (e.g., Merzenich and Brugge, 1973;Morel et al., 1993). There are a number of schemas andcorresponding nomenclatures for the auditory-related cor-tices in macaque monkeys, as summarized by Morel et al.(1993). In describing the striatal projections of corticalauditory areas, we have attempted to relate the locationsof our isotope injections to the maps of Galaburda andPandya (1983) and Morel et al. (1993). Experimental cases1, 2, 4, 5, 8, 10, 11, 14, and 15 are illustrated, and cases 3, 6,7, 9, 12, and 13 are described but not illustrated. Theinjection sites for the nonillustrated cases are shown inFigure 11.

Injections of the supratemporal plane

In four cases, isotope injections were placed in differentportions of the supratemporal region. In case 1 (Fig. 2), theinjections were placed in the STP after auditory evokedresponses had been elicited, and involved predominantlyarea KA, or AI. There was some encroachment into theprokoniocortex (area proA) medially. In this case, label wasseen only in a restricted portion of the striatum. Thus, inthe caudate nucleus, grains were noted in a dorsomediallocation only in the tail. In the putamen, label was seen ina ventromedial location in the caudal part of the nucleus.In case 2 (Fig. 3), the injections were placed in themid-portion of the circular sulcus in the STP by way of aventral penetration through the upper bank of the supe-rior temporal sulcus. The injection site encompassed mostof area proA or AII, or area RM of Morel et al. (1993). Thedistribution of terminal label was more extensive than

SUPERIOR TEMPORAL CORTICOSTRIATAL CONNECTIONS 385

that in the preceding case (Fig. 12A,B). Grains wereobserved in the ventromedial portion of the head and bodyof the caudate nucleus and in the dorsomedial portion ofthe tail. In the putamen, unlike the preceding case, labelwas found in both rostral and caudal portions of thenucleus. Rostrally, grains were seen mainly in central andventral locations, whereas caudally they occupied theventromedial sector. In case 3 (Fig. 11), as in case 1, theinjections were placed in the STP after auditory evokedresponses had been elicited (case not illustrated). Theinjection site included most of area KA, or AI, and ex-tended medially into the circular sulcus to involve thesecond auditory area, proA or AII, corresponding to areaRM of Morel et al. (1993). Some isotope also spreadlaterally into the dorsal portion of the lateral parakoniocor-tex (area paAlt), or area PL of Morel et al. (1993). Terminallabel was observed in both the caudate nucleus and theputamen. In the caudate nucleus, label was noted in theventromedial portion of the body and in the dorsomedialportion of the tail. In the putamen, grains were observedmainly in a ventromedial location, in the caudal one-half ofthe nucleus. In case 4 (Fig. 4), the injections were placed inthe caudal portion of the lower bank of the Sylvian fissureand involved mainly the caudal parakoniocortex (areapaAc), corresponding in part to area C of Morel et al.(1993). The overall distribution of terminal grains differedfrom those of the preceding three cases. Thus, in thecaudate nucleus, there was a limited amount of terminallabel caudally in the head. Similarly, there was only arelatively small amount of label ventrally in the body. Onlya few grains were noted in the tail of the caudate nucleus.Terminal label was seen throughout the rostrocaudalextent of the putamen, in a mainly dorsal and laterallocation rostrally and in dorsomedial and ventromediallocations caudally.

Injections of the rostral STG

In four cases, injections were made in the rostral portionof the STG. In case 5 (Fig. 5), the injections involved

portions of the proisocortex (area Pro) and temporalissuperior 1 (area Ts1) and extended into the rostral part ofarea Ts2. In comparison with the preceding cases, therewas a more substantial amount of terminal label in boththe caudate nucleus and the putamen, especially in therostral portions of both nuclei. In the head of the caudatenucleus, extensive clusters of terminal label were seen inthe ventral portion, extending into the ventral striatum-olfactory tubercle region. In the body, grains were foundmainly in a ventromedial location and in the tail in themedial portion. In the putamen, clusters of terminal labelwere observed in a ventral location rostrally and in aventromedial location caudally. In cases 6 and 7 (Fig. 11),the isotope injections involved mainly the ventral part ofareas Ts1 and Ts2 of the STG and extended into the upperbank of the superior temporal sulcus (cases not illus-trated). The injection site in case 7 also extended rostrallyinto area Pro. The distribution of terminal label in thesetwo cases was very similar and resembled that of case 5.Thus, clusters of label occurred in the ventral part of thehead, extending into the ventral striatum–olfactory tu-bercle region (Fig. 12C), the body of the caudate nucleus,and the medial portion of the tail. In the putamen, labelwas observed mainly in a ventromedial location rostrallyand in a ventral location caudally. In case 8 (Fig. 6), theisotope injections were placed in the dorsal part of areaTs2, involving both the gyral and sulcal portions of thisarea, with additional involvement of area Ts3 and therostral parakoniocortex (area paAr). The injection sitecorresponded in part to area RT of Morel et al. (1993). Inthe caudate nucleus, terminal label occupied mainly theventromedial portion of the head and the body and themedial sector of the rostral part of the tail. In the putamen,label was seen mainly in the ventromedial portion ros-trally and primarily in the medial sector caudally.

Injections of the middle portion of the STG

In three animals, isotope injections were placed in theSTG caudal to the preceding four cases. In case 9 (Fig. 11),

Fig. 1. Diagrams showing the surface (A) and architectonic (B)regions of the superior temporal gyrus and supratemporal plane in therhesus monkey. The Sylvian fissure has been opened up to expose thecortex of the insula, circular sulcus, and supratemporal plane. AS,arcuate sulcus; CiS, circular sulcus; CS, central sulcus; IPS, intrapari-etal sulcus; KA, auditory koniocortex; LF, lateral fissure; LS, lunatesulcus; paAc, caudal parakoniocortex; paAlt, lateral parakoniocortex;

paAr, rostral parakoniocortex; paI, parinsular area; pAll, periallocor-tex; Pro, proisocortex; proA, prokoniocortex; PS, principal sulcus; reIt,retroinsular temporal area; STG, superior temporal gyrus; STP,supratemporal plane; STS, superior temporal sulcus; Tpt, temporopa-rietal cortex; Ts1, temporalis superior 1; Ts2, temporalis superior 2;Ts3, temporalis superior 3.

386 E.H. YETERIAN AND D.N. PANDYA

the injections involved area Ts3 and the adjoining rostralportion of area paAlt, corresponding in part to area AL ofMorel et al. (1993). In addition, the injection extended intothe rostral temporal parakoniocortical area paAr in thelower bank of the Sylvian fissure (case not illustrated). Inthe head of the caudate nucleus, grains were located moredorsally than in the preceding cases, which had morerostral injections. Likewise, in the body of the caudatenucleus, terminal label was seen in a more dorsal locationthan in the rostral cases, whereas in the tail it occupied themedial portion. In the putamen, grains were noted in apredominantly ventromedial location in both the rostraland the caudal portions of the nucleus. In case 10 (Fig. 7),the isotope injections involved area Ts3 and the adjoiningpart of area paAlt, corresponding in part to area AL ofMorel et al. (1993). Like the previous case, terminal label

was observed mainly in the dorsomedial portion of thehead of the caudate nucleus. Grains were seen in theventral sector of the body and in the medial portion of thetail of the caudate nucleus. In the putamen, terminal labelwas noted ventromedially in both the rostral and thecaudal portions. In case 11 (Fig. 8), the isotope injectionswere located mainly in the dorsal portion of area paAlt,with slight extension into the rostrally adjoining portion ofarea Ts3 and involving in part area AL of Morel et al.(1993). Unlike cases 9 and 10, only a limited amount ofgrains was noted laterally in the head and in the rostralportion of the body of the caudate nucleus. A few clusters oflabel were observed in the medial portion of the tail of thecaudate nucleus. In the putamen, label was seen in aventral location rostrally and in central and ventromediallocations more caudally (Fig. 12D).

Fig. 2. Diagrammatic representation of the lateral surface of thecerebral hemisphere in case 1 showing an isotope injection site(blackened area) in the auditory koniocortex (KA, or AI) of thesupratemporal plane, and coronal sections (A–C) depicting the distri-bution of terminal label (dots) in the caudate nucleus and theputamen. In this and subsequent figures (Figs. 3–10), the lowerright-hand figure shows the distribution of terminal label in thestriatum in the sagittal plane. Cd, caudate nucleus; GLd, dorsal

lateral geniculate nucleus; GP, globus pallidus; IOS, inferior occipitalsulcus; Pcn, paracentral nucleus; Pu, putamen; R, reticular nucleus;Re, reuniens nucleus; TO, optic tract; VA, ventral anterior nucleus;VL, ventral lateral nucleus. For other abbreviations and conventions,see Figure 1. The nomenclature for thalamic nuclei in this andsubsequent figures is according to Olszewski (1952). Scale bar 52,000 µm.


Fig. 3. Diagrammatic representation of the lateral surface of thecerebral hemisphere in case 2 showing an isotope injection site in theprokoniocortex (proA, or AII) in the circular sulcus, and coronalsections (A–G) depicting the distribution of terminal label in thecaudate nucleus and the putamen. CM, centromedian-parafascicular

complex; MD, mediodorsal nucleus; PL, lateral pulvinar nucleus; PM,medial pulvinar nucleus; VPI, ventroposteroinferior nucleus; VPL,ventroposterolateral nucleus; VPM, ventroposteromedial nucleus; X,nucleus X. For other abbreviations and conventions, see Figures 1 and2. Scale bar 5 2,000 µm.

Fig. 4. Diagrammatic representation of the lateral surface of thecerebral hemisphere in case 4 showing an isotope injection site in thecaudal parakoniocortex (paAc) of the supratemporal plane, and coro-nal sections (A–F) depicting the distribution of terminal label in the

caudate nucleus and the putamen. CA, anterior commissure; H,habenula. For other abbreviations and conventions, see Figures 1–3.Scale bar 5 2,000 µm.

Fig. 5. Diagrammatic representation of the lateral surface of thecerebral hemisphere in case 5 showing an isotope injection site in therostral portion of the superior temporal gyrus (Pro, proisocortex; Ts1,Ts2, temporalis superior 1 and 2), and coronal sections (A–F) depicting

the distribution of terminal label in the caudate nucleus and theputamen. CL, central lateral nucleus. For other abbreviations andconventions, see Figures 1–3. Scale bar 5 2,000 µm.

Fig. 6. Diagrammatic representation of the lateral surface of thecerebral hemisphere in case 8 showing an isotope injection site in therostrodorsal portion of the superior temporal gyrus (Ts2, Ts3, tempora-lis superior 2 and 3), and coronal sections (A–G) depicting the

distribution of terminal label in the caudate nucleus and the putamen.GM, medial geniculate nucleus; LP, lateral posterior nucleus; PI,inferior pulvinar nucleus; PO, oral pulvinar nucleus. For other abbre-viations and conventions, see Figures 1, 2, and 4. Scale bar 5 2,000 µm.


Fig. 7. Diagrammatic representation of the lateral surface of thecerebral hemisphere in case 10 showing an isotope injection site in themiddle portion of the superior temporal gyrus (Ts3, temporalis supe-rior 3; paAlt, lateral parakoniocortex), and coronal sections (A–G)

depicting the distribution of terminal label in the caudate nucleus andthe putamen. For abbreviations and conventions, see Figures 1–3 and6. Scale bar 5 2,000 µm.


Fig. 8. Diagrammatic representation of the lateral surface of thecerebral hemisphere in case 11 showing an isotope injection site in themiddle portion of the superior temporal gyrus (paAlt, lateral parako-niocortex; Ts3, temporalis superior 3), and coronal sections (A–F)

depicting the distribution of terminal label in the caudate nucleus andthe putamen. For abbreviations and conventions, see Figures 1–3.Scale bar 5 2,000 µm.

Injections of the caudal STG

In four animals, injections were placed in the caudalportion of the superior temporal gyrus. In case 12 (Fig. 11),the injections involved the caudal part of area paAlt andmost of the temporoparietal cortex (area Tpt), correspond-ing in part to area PL of Morel et al. (1993; case notillustrated). In the caudate nucleus, the terminal label inthe head was limited and was localized mainly in thedorsal portion. In the body, grains were seen primarily in adorsomedial location and extended into the genu. Clustersof terminal label in the tail of the caudate nucleus occurredmainly in the medial sector. In the putamen, grains wereseen predominantly in the ventromedial portion of thecaudal part of the nucleus. Only a limited amount of grainswas seen in the rostral putamen, in a dorsomedial location.In case 13 (Fig. 11), the injections were located mainly inarea Tpt and extended rostrally into the caudal part ofarea paAlt, involving in part area PL of Morel et al. (1993;case not illustrated). In the head of the caudate nucleus,terminal label occupied mainly a dorsolateral location.Clusters of grains were observed dorsally and ventrally inthe body of the caudate nucleus and medially in the tail. Inthe putamen, terminal label was seen in a dorsal locationin the rostral part of the nucleus and in ventromedial anddorsomedial locations in the caudal part. In case 14 (Fig.9), the isotope injections were placed in the dorsal part ofarea Tpt and extended into the adjoining lower bank of theSylvian fissure to involve the caudal parakoniocorticalarea paAc. The injection site corresponded in part to areasPL and C of Morel et al. (1993). In the caudate nucleus,grains were seen mainly in the dorsolateral portion of thehead, in central and ventral sectors of the body, in thedorsal part of the genu, and in a restricted dorsomedialportion of the tail. In the putamen, terminal label occupieda dorsal location rostrally and mainly a ventromediallocation caudally. In case 15 (Fig. 10), the injections wereplaced in the dorsal sector of area Tpt. In the caudatenucleus, a limited amount of terminal label was seen in themedial portion of the body and in the dorsal portion of thetail. Likewise, only a restricted amount of label was notedin the dorsomedial part of the caudal putamen. Thus,across these four cases, the pattern of corticostriatalconnections was similar. However, in case 15, with arestricted injection site, the distribution of terminal labelin the striatum was less extensive than that in thepreceding three cases.

DISCUSSION

Previous investigations of the corticostriatal con-nectivity of the superior temporal region in rhesus mon-keys have been limited to its rostral portion. According tothe present observations, as summarized in Figure 13,area KA (primary auditory area, or AI) of the supratempo-ral plane has limited projections to the dorsomedial part ofthe tail of the caudate nucleus and to the adjoiningcaudoventral sector of the putamen (see case 1). A similarfinding was reported by Kemp and Powell (1970). Incontrast to the primary auditory area, area proA in thecircular sulcus (second auditory area, or AII) has morewidespread corticostriatal projections, distributed to theventral portion of the body of the caudate nucleus, themedial sector of the tail, and rostroventral and caudoven-tral portions of the putamen (see case 2). Area paAc caudalto area KA in the supratemporal plane has somewhat more

extensive projections rostrocaudally, with a relatively moredorsal distribution, most notably in the head and the bodyof the caudate nucleus and in rostral and caudal portionsof the putamen (case 4).

The distribution of corticostriatal connections from thesuperior temporal gyrus is somewhat different from that ofthe supratemporal plane (Fig. 13). The rostral portion ofthe superior temporal gyrus (areas Pro, Ts1, and Ts2), incomparison with the regions of the supratemporal plane,has more marked connections to the rostral part of thestriatum (see cases 5 and 8). In general, the caudatenucleus projections are in ventral and medial locations. Inthe putamen, the projections are mainly ventromedial;however, those from the dorsal portion of area Ts2 alsoextend dorsally in the caudal part of the nucleus. Inaddition, the rostral portion of the superior temporal gyrushas connections to the ventral striatum-olfactory tubercleregion. A similar overall pattern of corticostriatal connec-tivity from the rostral STG has been shown by otherinvestigators (Whitlock and Nauta, 1956; Kemp and Pow-ell, 1970; Yeterian and Van Hoesen, 1978; Van Hoesen etal., 1981; Selemon and Goldman-Rakic, 1985; Goldman-Rakic and Selemon, 1986).

In comparison with the rostral portion of the superiortemporal gyrus, the corticostriatal projections of the middleportion, in particular those of area Ts3, are generally moredorsal in the head and the body of the caudate nucleus andare central and medial in the tail. Within the putamen, theconnections are predominantly ventral and medial inlocation (see case 10). Area paAlt of the middle portion ofthe STG has relatively few projections to the caudatenucleus, and its connections to the putamen are centraland ventral in location (see case 11). It is of interest to notethat Whitlock and Nauta (1956) described projections fromthe middle part of the STG to the ventromedial portion ofthe caudal putamen but did not report any connections tothe rostral putamen or to the caudate nucleus.

The pattern of corticostriatal connectivity from thecaudal portion of the superior temporal gyrus (caudal areapaAlt and area Tpt) differs overall from that of other partsof the superior temporal region (e.g., case 14). Thus, in thehead of the caudate nucleus, projections occupy dorsolat-eral and dorsomedial portions. In the body of the caudatenucleus, connections are directed to dorsal and ventrallocations and are mainly medial in the tail. In the puta-men, projections tend to be dorsal in the rostral part of thenucleus and predominantly ventromedial in its caudalportion.

It seems that among all of the areas of the superiortemporal region examined in the present study, the pri-mary auditory cortex has the most limited distribution ofstriatal connections. A similarly restricted pattern of corti-costriatal connectivity has been reported for the primaryvisual region (Kemp and Powell, 1970). In contrast, thesecond auditory area, the caudal supratemporal plane(area paAc), and the STG have more extensive striatalprojections (Fig. 13). Area proA (AII), area paAc, and theportion of the STG adjoining the primary auditory regionare considered to be parts of the parakoniocortical belt(e.g., Merzenich and Brugge, 1973; Pandya and Sanides,1973; Morel and Kaas, 1992; Morel et al., 1993; Jones etal., 1995). Thus, in the cortical auditory system, striatalconnections appear to be derived primarily from beltareas.


Fig. 9. Diagrammatic representation of the lateral surface of thecerebral hemisphere in case 14 showing an isotope injection site in thecaudal portion of the superior temporal gyrus (Tpt, temporoparietalcortex; paAc, caudal parakoniocortex), and coronal sections (A–G)

depicting the distribution of terminal label in the caudate nucleus andthe putamen. AM, anteromedial nucleus; AV, anteroventral nucleus; v,lateral ventricle. For other abbreviations and conventions, see Figures1–4 and 6. Scale bar 5 2,000 µm.


Fig. 10. Diagrammatic representation of the lateral surface of thecerebral hemisphere in case 15 showing an isotope injection site in thecaudal portion of the superior temporal gyrus (Tpt, temporoparietalcortex), and coronal sections (A–E) depicting the distribution of

terminal label in the caudate nucleus and the putamen. Cdc, centraldensocellular nucleus. For other abbreviations and conventions, seeFigures 1–3 and 9. Scale bar 5 2,000 µm.


Within the lateral belt areas of the superior temporalgyrus, there is a shift in the topographic distribution ofcorticostriatal projections from rostral to caudal regions.Thus, it seems that the rostral STG (areas Pro, Ts1, andTs2) projects primarily to the ventral part of the caudatenucleus and the putamen and to the medial part of the tail.A similar pattern of corticostriatal connectivity has beenreported for the ventral prefrontal and orbital cortices(Yeterian and Van Hoesen, 1978; Van Hoesen et al., 1981;Selemon and Goldman-Rakic, 1985; Saint-Cyr et al., 1990;Yeterian and Pandya, 1991; Haber et al., 1995), with whichthe rostral STG is reciprocally interconnected (e.g., Jonesand Powell, 1970; Chavis and Pandya, 1976; Markowitschet al., 1985; Moran et al., 1987; Barbas, 1988, 1993;Petrides and Pandya, 1988; Morecraft et al., 1992; Carmi-chael and Price, 1995). In contrast to the rostral STG, thecaudal STG (area Tpt) projects mainly to the dorsal part ofthe head and the body of the caudate nucleus, to dorsalportions of the putamen, and the medial part of the tail.This pattern of corticostriatal connectivity is similar tothat of caudal inferior parietal area PG (Yeterian and VanHoesen, 1978; Weber and Yin, 1984; Selemon and Goldman-Rakic, 1985; Cavada and Goldman-Rakic, 1991; Yeterianand Pandya, 1993) and caudal dorsolateral prefrontal area8 (Goldman and Nauta, 1977; Kunzle and Akert, 1977;Kunzle, 1978; Selemon and Goldman-Rakic, 1985; Stantonet al., 1988; Yeterian and Pandya, 1991; Parthasarathy etal., 1992). It is notable that area Tpt shares reciprocalconnections with both area PG and area 8 (e.g., Jones andPowell, 1970; Chavis and Pandya, 1976; Barbas andMesulam, 1981; Barbas, 1988; Petrides and Pandya, 1988;Cavada and Goldman-Rakic, 1989; Pandya and Yeterian,1996). For both the rostral and the caudal auditory associa-tion areas, the observation that these regions have cortico-striatal connectivity similar to that of other cortical areaswith which they are reciprocally interconnected is consis-tent with the organizational principle suggested by Yete-rian and Van Hoesen (1978) and recently supported byInase et al. (1996). That is, cortically interconnected areasproject in part to topographically similar portions of thestriatum.

A comparison of auditory corticostriatal projections withthe striatal connections of visual, somatosensory, motor,parietal association, and prefrontal regions of the cerebralcortex indicates that each of these regions has a distinctive

overall relationship with the caudate nucleus and theputamen. The auditory cortices tend to project moststrongly to the ventromedial portions of the head of thecaudate nucleus and the rostral putamen and to themedial portion of the tail. Extrastriate corticostriatalconnections are directed mainly to the dorsal portion of thehead and the body of the caudate nucleus, to the genu, andto the lateral portion of the tail (e.g., Saint-Cyr et al., 1990;Yeterian and Pandya, 1995). Inferotemporal corticostria-tal projections are mainly to the lateral sector of the tail ofthe caudate nucleus, the ventrolateral portion of thecaudal putamen, and to the rostral putamen (e.g., VanHoesen et al., 1981; Webster et al., 1993). Primary somato-sensory and motor regions have striatal connections mainlyto the putamen (e.g., Kunzle, 1975; Jones et al., 1977;Kunzle, 1977), whereas parietal association areas tend toproject to the caudate nucleus and to the putamen (e.g.,Cavada and Goldman-Rakic, 1991; Yeterian and Pandya,1993). Prefrontostriatal connections are directed predomi-nantly to the head and the body of the caudate nucleus,with lesser projections to the tail of the caudate nucleusand to the putamen (e.g., Selemon and Goldman-Rakic,1985; Yeterian and Pandya, 1991). Thus, it seems thatauditory cortices overall have a specific pattern of cortico-striatal connectivity compared with other cerebral corticalregions.

The differential corticostriatal projections seen amongthe auditory-related areas of the superior temporal regionsuggest that this connectivity could subserve specific func-tions. However, very few investigations have addressedthe role of the striatum in auditory processes. Availablestudies have demonstrated the existence of neurons in thehead of the caudate nucleus, in the rostral putamen, and inthe ventral striatum that respond to auditory stimuli, inparticular when such stimuli are cues for specific move-ments (Rolls et al., 1983; Hikosaka et al., 1989; Romo et al.,1992; Williams et al., 1993). Although the tail of thecaudate nucleus and the caudal putamen comprise asignificant projection zone of the superior temporal region,to our knowledge, no investigations have addressed theauditory role of this portion of the striatum. In view of thepaucity of information regarding the auditory functions ofthe striatum, it may be useful to consider the role ofauditory corticostriatal connectivity from the perspectiveof known functions of specific cortical regions.

Fig. 11. Diagrammatic representations of the lateral surface of the cerebral hemisphere showing thelocations of isotope injection sites for nonillustrated cases. For abbreviations and conventions, see Figures1 and 2.


Fig. 12. Photomicrographs showing the distribution of terminal label in the caudate nucleus and theputamen and in the ventral striatum-olfactory tubercle region, following isotope injections into differentportions of the superior temporal cortex. A,B: Case 2. C: Case 7. D: Case 11. For abbreviations andconventions, see Figures 2 and 9. Scale bar 5 2,000 µm.

A consideration of the literature regarding the functionsof the superior temporal region demonstrates the involve-ment of cortical auditory areas in processes such as soundfrequency and amplitude coding, sound localization, audi-tory pattern discrimination, auditory recognition, short-term memory, selective attention, species-specific commu-nication, and sensorimotor association (e.g., Dewson et al.,1970; Iversen and Mishkin, 1973; Merzenich and Brugge,1973; Miller et al., 1974; Beaton and Miller, 1975; Heffnerand Masterton, 1975; Cowey and Weiskrantz, 1976; Hocher-man et al., 1976; Wegener, 1976; Hupfer et al., 1977;Benson and Hienz, 1978; Strominger et al., 1980; Pfingstand O’Connor, 1981; Vaadia et al., 1982; Heffner andHeffner, 1984, 1986a,b, 1989a,b, 1990a,b; Gemba and

Sasaki, 1988; Gottlieb et al., 1989; Colombo et al., 1990,1996; Ahissar et al., 1992; Morel et al., 1993; Recanzone etal., 1993; Javitt et al., 1994; Rauschecker et al., 1995,1997; Wang et al., 1995; Bieser and Muller-Preuss, 1996).The primary auditory cortex is known to be involved in thecoding of frequency and amplitude, sound localization,selective attention, species-specific vocalization, and senso-rimotor association (e.g., Merzenich and Brugge, 1973;Heffner and Masterton, 1975; Hocherman et al., 1976;Benson and Hienz, 1978; Pfingst and O’Connor, 1981;Vaadia et al., 1982; Heffner and Heffner, 1986a,b, 1990a,b;Schwarz and Tomlinson, 1990; Ahissar et al., 1992; Morelet al., 1993; Recanzone et al., 1993; Wang et al., 1995;Bieser and Muller-Preuss, 1996; Kosaki et al., 1997).These functions of the primary auditory cortex, given therelatively modest connections between this area and thestriatum, may not depend heavily on a striatal relation-ship.

The belt areas surrounding the primary auditory region,in particular the superior temporal gyrus, are involved infunctions such as sound recognition, encoding of species-typical vocalizations, localization of sound sources, andsensorimotor association (e.g., Cowey and Weiskrantz,1976; Wegener, 1976; Leinonen et al., 1980; Strominger etal., 1980; Vaadia et al., 1982; Heffner and Heffner, 1989a,b).The substantial corticostriatal connectivity of the auditorybelt areas suggests that this circuitry may have a role inthese processes. The differential corticostriatal connectiv-ity of the STG may subserve the known differentialfunctional attributes of this region. Thus, for example, theconnectivity from the rostral part of the STG (areas Pro,Ts1, and Ts2) to ventral portions of the caudate nucleusand the putamen and to the ventral striatum-olfactorytubercle region may be involved specifically in auditoryperception (Heffner and Heffner, 1989b), auditory memory(Colombo et al., 1990), sound recognition (Colombo et al.,1996), and pattern discrimination (Wegener, 1976; Stro-minger et al., 1980). Although there is a paucity of studiesexamining the auditory role of the rostral part of the STG,the corticocortical (e.g., Galaburda and Pandya, 1983;Markowitsch et al., 1985; Moran et al., 1987; Morel andKaas, 1992) and corticothalamic (e.g., Markowitsch et al.,1985; Pandya et al., 1994) connectivity of this regionsuggests that it may in part serve auditory functions. Theconnectivity from the caudalmost portion of the STG (areaTpt) to dorsal portions of the head and the body of thecaudate nucleus and to the dorsal sector of the putamencould be involved in encoding the spatial locations ofsounds (Leinonen et al., 1980) and in the learning of handmovements in response to auditory cues (Gemba andSasaki, 1988). It is possible that the corticostriatal connec-tivity of area Tpt may have a general role in audiospatialfunctions. It is of interest to note that other parts of thecerebral cortex known to be involved in spatial processes,e.g., the dorsolateral prefrontal and posterior parietalcortices, also project to dorsal portions of the striatum(Goldman and Nauta, 1977; Kunzle and Akert, 1977;Kunzle, 1978; Yeterian and Van Hoesen, 1978; Weber andYin, 1984; Selemon and Goldman-Rakic, 1985; Stanton etal., 1988; Cavada and Goldman-Rakic, 1991; Yeterian andPandya, 1991, 1993). Finally, the mid- and caudal portionsof the STG (corresponding to areas Ts3, paAlt, and therostral portion of area Tpt) have been shown to have a rolein the encoding of species-specific communication sounds(Rauschecker et al., 1995). The corticostriatal connectivity

Fig. 13. Summary diagrams representing the overall pattern ofcorticostriatal connectivity of the superior temporal region in thesagittal plane. The upper diagram depicts striatal connections fromthe prokoniocortex (area proK or AII; A), auditory koniocortex (KA orAI; B), and the caudal parakoniocortex (paAc; C). The lower diagramdepicts striatal connections from rostral (A), middle (B), and caudal(C) portions of the superior temporal gyrus.


of this region, which is intermediate to that of the rostraland the caudalmost portions of the STG, may play a role inintegrating species-specific auditory communication withongoing motor behavior.

In a recent study, Colombo et al. (1996) proposed theexistence of two streams of auditory processing analogousto the ventral and dorsal streams in the cortical visualsystem (e.g., Mishkin et al., 1983; Van Essen and Maun-sell, 1983). Specifically, Colombo et al. suggested that therostral portion of the STG (areas Ts1, Ts2, and Ts3) isinvolved in sound recognition, whereas the caudal sector(area Tpt) subserves spatial localization of sound sources.The latter proposal is in agreement with the observationsof Leinonen et al. (1980). Rauschecker et al. (1997) simi-larly proposed that the caudal portion of the supratempo-ral plane (area CM) may be involved in sound localization.Thus, it seems that the differential corticostriatal connec-tivity discussed above for rostral versus caudal regions ofthe STG is consistent with the notion of dual functionalsystems at the cortical level. We recognize that this isspeculative in nature and that more specific functionalstudies relating to discrete portions of the superior tempo-ral region and of the striatum will be needed to gain afuller understanding of auditory corticostriatal connectiv-ity.

ACKNOWLEDGMENTS

We thank Ms. Helen Waldron for excellent technicalassistance.

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Corticostriatal connections of the superior temporal region in rhesus monkeys