Corticothalamic connections of extrastriate visual areas in rhesus monkeys

Corticothalamic Connectionsof Extrastriate Visual Areas

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

ABSTRACTCorticothalamic connections of extrastriate visual areas were studied by using the

autoradiographic anterograde tracing technique. The results show that the medial extrastri-ate region above the calcarine sulcus projects mainly to the lateral pulvinar (PL), medialpulvinar (PM), and lateral posterior (LP) nuclei. In addition, the dorsal portion of the medialregion has connections to the lateral dorsal (LD) as well as to intralaminar nuclei. Thedorsolateral extrastriate region projects strongly to the PL and LP nuclei, to the PM andinferior pulvinar (PI) nuclei, and to the LD and intralaminar nuclei. The lateral extrastriateregion above the inferior occipital sulcus (IOS) has strong connections to both the PL and PInuclei and has minor projections to the PM and oral pulvinar nuclei. The ventrolateralextrastriate region below the IOS projects mainly to the PI nucleus and to the caudal portionof the PL nucleus and has some projections to the PM nucleus. The ventromedial extrastriateregion medial to the occipitotemporal sulcus has strong connections with the ventral andmedial sectors of the PI nucleus. This region also projects to the caudal portion of the PLnucleus and has minor connections to the LP nucleus. Finally, the annectant gyrus projects tothe PL nucleus and to the rostral portion of the PI nucleus and has minor connections to thePM nucleus. Thus, the medial and dorsolateral extrastriate regions are related mainly to thePL and LP nuclei as well as to intralaminar nuclei. In contrast, the ventrolateral andventromedial regions are connected strongly with the PI nucleus. This connectional organiza-tion appears to reflect functional differentiation at the cortical level. J. Comp. Neurol.378:562-585, 1997. r 1997 Wiley-Liss, Inc.

Indexing terms: cortex; occipital; thalamus; pulvinar

The visual cortex of higher primates has been shown tocontain several anatomically and functionally distinctareas. In recent years, these regions have been conceptual-ized as belonging to distinct streams of visual informationprocessing (see, e.g., Mishkin et al., 1983; Van Essen andMaunsell, 1983; Boussaoud et al., 1990). The dorsolateraland medial occipital areas have been viewed as parts of adorsal stream that is involved mainly in the visuospatialor peripheral visual sphere. The ventrolateral occipitalareas, in contrast, are considered to be components of apathway that serves central or object vision. A thirdstream involving the middle temporal (MT) and medialsuperior temporal (MST) areas of the caudal superiortemporal sulcus is thought to be involved in the perceptionof visual motion. The three visual streams as well asspecific areas within each pathway have been shown tohave distinctive patterns of cortical and subcortical connec-

tivity in primates. With specific regard to the corticotha-lamic projections of extrastriate regions, a number ofstudies have been carried out in macaque monkeys (Ben-evento and Davis, 1977; Trojanowski and Jacobson, 1977;Ungerleider et al., 1984; Kikuchi et al., 1987; Squatrito

A preliminary report of these findings was presented at the meeting ofthe Society for Neuroscience, San Diego, CA, November 1995 (Yeterian andPandya, 1995a).Contract grant sponsor: Department of Veterans Affairs; Contract grant

sponsor: National Institutes of Mental Health; Contract grant number:16841; Contract grant sponsor: Colby College Social Science; Contractgrant numbers: 01 2220, 01 2239; Contract grant sponsor: Audrey andSheldon Katz Research Fund of Colby College.*Correspondence to: Edward H. Yeterian, Ph.D., Department of Psychol-

ogy, Colby College, 5557 Mayflower Hill, Waterville, ME 04901-8855.E-mail: [email protected] 15 May 1996; Revised 17 October 1996; Accepted 21 October 1996

THE JOURNAL OF COMPARATIVE NEUROLOGY 378:562–585 (1997)

r 1997 WILEY-LISS, INC.

et al., 1988; Tanaka et al., 1990; Boussaoud et al., 1992;Webster et al., 1993). Collectively, however, these investi-gations have focused mainly on the lateral extrastriateregion and the rostrally adjoining portion of the inferiortemporal cortex. These studies have revealed that themain projections of the lateral extrastriate cortices are tothe lateral pulvinar (PL) and inferior pulvinar (PI) nuclei,with differential topographic distributions within thesenuclei. Additional projections have been demonstrated tothe medial pulvinar, lateral posterior, lateral dorsal, anddorsal lateral geniculate nuclei from the lateral extrastri-ate regions.The corticothalamic connections of a relatively large

expanse of the extrastriate cortex, including the medialand ventral areas as well as the annectant gyrus, remainto be delineated. In recent years, there has been increasedinterest in the role of thalamic relationships in higherneural processes (see, e.g., Crick, 1984; Sillito et al., 1994;Guillery, 1995; Steriade, 1995). Therefore, it may be usefulto have a more complete knowledge of the connectionsbetween visual regions of the cerebral cortex and specificthalamic nuclei. In the present investigation, the autora-diographic anterograde tracing method was used to exam-ine the corticothalamic projections of dorsomedial, dorsolat-eral, annectant, ventrolateral, and ventromedialextrastriate areas. The results indicate that these regionshave distinctive overall patterns of connectivity to the PLand PI nuclei. In addition, medial as well as lateralextrastriate areas have projections to the lateral posterior,lateral dorsal, and intralaminar nuclei.

MATERIALS AND METHODS

The corticothalamic connections of extrastriate areaswere traced in 18 rhesus monkeys (Macaca mulatta) byusing radioactively labeled amino acids. A craniotomy wasperformed under sodiumpentobarbital anesthesia (approxi-mately 20 mg/kg administered intravenously as intermit-tent boluses), and two discrete injections (3H-leucine and3H-proline, total volume 0.4–1.0 µl; specific activity 40–80µCi) were made in a selected portion of the extrastriatecortex in each case. Following a survival time of 7–10 days,the animals were administered a lethal dose of sodiumpentobarbital and were perfused transcardially with iso-tonic saline followed by 10% formalin. The brains wereremoved, photographed, and processed for autoradiogra-phy according to the method of Cowan et al. (1972).Exposure times ranged from 3 to 6 months.Each hemisphere was divided coronally into two or three

blocks in the stereotactic plane. The blocks were embeddedin paraffin and cut into 10-µm-thick sections in the coronalplane. Every tenth section was processed for autoradiogra-phy and stained with thionin. This stain permitted theanalysis of cortical architecture, localization of the injec-tion site, and identification of the boundaries of thalamicnuclei. The precise location of each injection site wasdetermined by observing the cortical architecture aroundthe labeled area and comparing this with the architectureof the corresponding nonlabeled area in the cortex of theopposite hemisphere. The pattern of terminal label asrevealed under darkfield illumination was charted onto

Abbreviations

7a caudal inferior parietal areaAD anterior dorsal nucleusAITd anterior inferotemporal area (dorsal)AITv anterior inferotemporal area (ventral)AS arcuate sulcusBSC brachium of the superior colliculusCC corpus callosumCd caudate nucleusCF calcarine fissureCINGS cingulate sulcusCITd central inferotemporal area (dorsal)CITv central inferotemporal area (ventral)CL central lateral nucleusCM centromedian nucleusCM-Pf centromedian-parafascicular nucleusCS central sulcusCSL central lateral superior nucleusDP dorsal prelunate areaFST floor of superior temporal sulcusGLd dorsal lateral geniculate nucleusGM medial geniculate nucleusHb habenulaIOS inferior occipital sulcusIPS inferior parietal sulcusLD lateral dorsal nucleusLF lateral fissureLi limitans nucleusLIP lateral intraparietal areaLOS lateral orbital sulcusLP lateral posterior nucleusLS lunate sulcusMD medial dorsal nucleusMDP medial dorsal parietal areaMIP medial intraparietal areaMOS medial orbital sulcusMSTd medial superior temporal area (dorsal)MSTl medial superior temporal area (lateral)MT middle temporal areaOTS occipitotemporal sulcusPcn paracentral nucleus

Pf parafascicular nucleusPI inferior pulvinar nucleusPIP posterior intraparietal areaPITd posterior inferotemporal area (dorsal)PITv posterior inferotemporal area (ventral)PL lateral pulvinar nucleusPM medial pulvinar nucleusPO parietooccipital areaPO oral pulvinar nucleusPOMS medial parietooccipital sulcusPS principal sulcusR thalamic reticular nucleusRhF rhinal fissureSG suprageniculate nucleusSTPa superior temporal polysensory area (anterior)STPp superior temporal polysensory area (posterior)STS superior temporal sulcusTF posterolateral parahippocampal cortexTH posteromedial parahippocampal cortexTHI habenulointerpeduncular tractV lateral ventricleV1 visual area 1V2d dorsal visual area 2V2v ventral visual area 2V3 visual area 3V3a visual area V3aV4d dorsal visual area 4V4t V4 transitional areaV4v ventral visual area 4VIP ventral intraparietal areaVL ventrolateral nucleusVLm ventrolateral nucleus, medial portionVLps ventrolateral nucleus, pars postremaVOT ventral occipitotemporal areaVP ventral posterior areaVPI ventroposteroinferior nucleusVPL ventroposterolateral nucleusVPM ventroposteromedial nucleusVPMpc ventroposteromedial nucleus, parvocellular portionX area X

EXTRASTRIATE CORTICOTHALAMIC CONNECTIONS 563

coronal tracings of the thalamus. The experimental mate-rial analyzed in this study has been used in other investi-gations (Schmahmann and Pandya, 1993; Yeterian andPandya, 1995b). Animal care was provided in accordancewith the NIH Guide for Care and Use of LaboratoryAnimals.

RESULTS

In describing the isotope injection sites in the extrastri-ate region, we have specified the locations in terms ofsubregions that have been defined recently on the basis ofphysiology as well as architecture and connections (see,e.g., Van Essen and Maunsell, 1983; Ungerleider andDesimone, 1986; Boussaoud et al., 1990; Colby andDuhamel, 1991; Felleman and Van Essen, 1991; Krubitzerand Kaas, 1993; Stepniewska and Kaas, 1996). Althoughthere is basic agreement among these various schemas forthe visual cortices, nevertheless, certain regions differsomewhat in terms of both location and nomenclature. Inaddition, we have referred to the classical nomenclature ofBrodmann (1909). Figure 1 depicts the organizationalschema of Felleman and Van Essen (1991). Experimentalcases 1–3, 5, 7–12, and 15–18 are illustrated, whereascases 4, 6, 13, and 14 are described but are not illustrated.The injection sites for these latter cases are shown inFigure 17. Photomicrographs of representative isotopeinjection sites have been presented in another study(Schmahmann and Pandya, 1993).With regard to the thalamus, we have specified indi-

vidual nuclei according to the terminology of Olszewski(1952). Recently, Gutierrez et al. (1995) have modified theborders of the PI and PL nuclei. We have determined theborders of these two nuclei on the basis of differentialcellular morphology and density, referring to both theclassical and the recent findings. The differences betweenthe borders of these nuclei in the present study and thosedelineated by other investigators may be due in part to thedifferent histological methods employed.

Injections of medial extrastriate cortex

In four cases, isotope injections were placed in variousregions of the medial extrastriate cortex. In case 1 (Fig. 2),the injection was placed in the ventral part of the medialpreoccipital gyrus and in the anterior bank of the medialparietooccipital sulcus (areas 18, 19). The main bulk ofterminal label was observed in the PL nucleus. At caudallevels of the nucleus, grains occupied a dorsolateral loca-tion, whereas, at rostral levels, they were seen in a ventrallocation. In addition, terminal label was noted in thedorsomedial sector of the PI nucleus at levels caudal to aswell as contiguous with the dorsal lateral geniculatenucleus. Occasional grains were observed in the oralpulvinar (PO) nucleus. In case 2 (Fig. 3), the isotopeinjection involved the rostral and central part of medialarea 19, in a location both somewhat rostral and dorsal tothat of the preceding case (in the descriptions of theresults, the medial and lateral extrastriate cortices aredivided into dorsal, central, and ventral regions in thedorsoventral dimension). This injection also encroachedupon the adjacent part of area PGm (Pandya and Seltzer,1982). Like the previous case, patches of terminal labelwere observed in the dorsal portion of the PL nucleus. Inaddition, grains were seen in the lateral sectors of themedial pulvinar (PM) and PO nuclei and in the lateral

posterior (LP) nucleus. In contrast to the preceding case,no evidence of terminal label was noted in the PI nucleus.In case 3 (Fig. 4), the injection was located in the dorsome-dial portion of area 19 in a region corresponding to area M(see, e.g., Kaas, 1997) or the parietooccipital area (Colby etal., 1988), with isotope extending rostrally up to area PGmof the medial parietal cortex. In contrast to the precedingtwo cases, this injection site was more dorsal in location. Alarge amount of terminal label was observed in the dorsalportion of the PL nucleus and in the LP nucleus (Fig. 16A).Distinct patches of grains were seen in the lateral portionof the PM nucleus, in the PO nucleus, in the dorsal part ofthe ventrolateral (VL) nucleus, and in the pars postrema ofthe ventrolateral (VLps) nucleus. Unlike the two preced-

Fig. 1. Diagrams of the locations of extrastriate visual areas asdelineated by Felleman and Van Essen (1991). On the right, a lateraland a medial view of the cerebral hemisphere of the macaque monkeyshow the visual areas on the cortical surface. On the left, an unfoldedmap of the posterior cortex depicts the various visual areas on themedial, lateral, and ventral surfaces of the hemisphere.AITd, anteriorinferotemporal area (dorsal); AITv, anterior inferotemporal area (ven-tral); CITd, central inferotemporal area (dorsal); CITv, central infero-temporal area (ventral); DP, dorsal prelunate area; FST, floor ofsuperior temporal sulcus; LIP, lateral intraparietal area; MDP, medialdorsal parietal area; MIP, medial intraparietal area; MSTd, medialsuperior temporal area (dorsal); MSTl, medial superior temporal area(lateral); MT, middle temporal area; PIP, posterior intraparietal area;PITd, posterior inferotemporal area (dorsal); PITv, posterior inferotem-poral area (ventral); PO, parietooccipital area; STPa, superior tempo-ral polysensory area (anterior); STPp, superior temporal polysensoryarea (posterior); TF, posterolateral parahippocampal cortex; TH, pos-teromedial parahippocampal cortex; V1, visual area 1; V2d, dorsalvisual area 2; V2v, ventral visual area 2; V3, visual area 3; V3a, visualarea V3a; V4d, dorsal visual area 4; V4t, V4 transitional area; V4v,ventral visual area 4; VIP, ventral intraparietal area; VOT, ventraloccipitotemporal area; VP, ventral posterior area; 7a, caudal inferiorparietal area.

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

ing cases, label was also noted in the dorsal portion of thecentral lateral (CL) nucleus and in the central lateralsuperior (CSL) nucleus as well as in the lateral dorsal (LD)nucleus. In case 4 (Fig. 17), the isotope injection was placed inthedorsalmost portion ofmedial area19 corresponding to areaMDPofColby et al. (1988). The resulting distribution of grainswas quite similar to that of case 3. However, the density ofterminal label in the LP and PM nuclei was greater thanthat of the preceding case, and the grains in the PLnucleustended to be located more medially.

Injections of dorsolateral extrastriate cortex

In six cases, isotope injections were placed in variousregions of the dorsolateral preoccipital gyrus dorsal to theinferior occipital sulcus (IOS). In case 5 (Fig. 5), theinjection was placed in the dorsalmost portion of thelateral extrastriate region in dorsal area 19 correspondingto the dorsal prelunate area (DP; Andersen et al., 1985).The resulting distribution of grains greatly resembled thatof dorsomedial cases 3 and 4. Thus, terminal label waslocated mainly in the PL nucleus throughout almost all ofits rostrocaudal extent. Additional zones of terminationwere noted in the PM, PO, and LPnuclei (Fig. 16B). Unlikethe dorsomedial cases, but similar to case 1, there was alimited amount of terminal label in the dorsomedial sectorof the PI nucleus at a level caudal to and contiguous withthe dorsal lateral geniculate nucleus (GLd). In this case,label was also noted in the LD, CSL, and paracentral (Pcn)nuclei as well as in the dorsal portion of the CL nucleus. Incase 6 (Fig. 17), an injection was placed in the centralportion of lateral area 19, extending into the adjacentrostral bank of the lunate sulcus and corresponding to partof area V3 and the dorsal portion of visual area 4 (V4; see,e.g., Felleman and Van Essen, 1991), or area DM, thedorsomedial extrastriate area (see, e.g., Stepniewska andKaas, 1996). The main bulk of terminal label was observedin the caudal portion of the PL nucleus. In addition, somepatches of grains were seen in the PI nucleus centrally andin the PM nucleus laterally. In case 7 (Fig. 6), the isotopeinjection was located in the dorsal portion of area 19corresponding in part to dorsal visual area 4 (V4d; see, e.g.,Felleman and Van Essen, 1991) or the dorsal portion ofarea DL, the dorsolateral extrastriate area (see, e.g.,Stepniewska and Kaas, 1996). Compared with case 6, theinjection was larger and had greater ventral extent. Thegreatest proportion of terminal label in this case was seenin the dorsal sector of the caudal two-thirds of the PLnucleus.Additional label was observed in the lateral sectorof the PM nucleus and in the LP nucleus, with only alimited amount in the dorsal portion of the PI nucleus.Some grains also were noted in the dorsal portion of the CLnucleus as well as in the CSL nucleus (not shown). In case8 (Fig. 7), the isotope injection was located in the centralpart of area 19 corresponding to the ventral portion of areaV4d or area DL. The main bulk of terminal label was seenin the caudal two-thirds of the PL nucleus.Additional labelwas seen in dorsal and lateral sectors of the PI nucleus. Asmall amount of grains also was noted in the PM and in theVLps nuclei. In case 9 (Fig. 8), the isotope injection involvedthe central portion of lateral area 19 corresponding to aportion of area V4 or DL and was located more ventrally thanin case 8. Overall, the distribution of terminal label wassomewhat more ventral than in any of the preceding cases. InthePLnucleus, the bulk of grains occupiedmedial and ventralsectors in the caudal two-thirds of the structure. Somepatches

of terminal label were seen in the lateral sectors of the POandPM nuclei. A notable amount of terminal label occurredmainly in a dorsal location in the PI nucleus throughout itsrostrocaudal extent (Fig. 16C).In case 10 (Fig. 9), the isotope injection was placed in the

caudal portion of the lower bank of the superior temporalsulcus (STS). This region corresponds in location to therostral portion of area V4d and to the caudal portion ofarea MT. It also corresponds to the V4 transitional area(V4t; Desimone and Ungerleider, 1986), or MTc, the caudalmiddle temporal area (see, e.g., Kaas, 1997). The bulk ofterminal label was seen in the ventral sector of the caudaltwo-thirds of the PL nucleus and in the dorsal portion ofthe PI nucleus throughout its rostrocaudal extent. Inaddition, patches of label were observed in the ventrolat-eral sector of the PM nucleus (Fig. 16D). A limited amountof grains was noted in the CSL (not shown) and Pcn nuclei.In three cases, injections were placed in the rostral bank

and the depths of the lunate sulcus. In case 11 (Fig. 10), theinjection occupied the dorsal portion of the rostral bank ofthe lunate sulcus corresponding in location to area V4dand the dorsal portion of area V3 or area DM. The bulk ofterminal label was observed in medial and ventral sectorsof the PL nucleus and in the dorsal portion of the PInucleus. In addition, some grains were noted in the lateralsector of the PM nucleus and in the LP nucleus. In cases 12(Fig. 11) and 13 (Fig. 17), isotope injections were placed inthe rostral portion of the annectant gyrus corresponding inlocation to dorsal portions of areas V4 and V3a (see, e.g.,Felleman and Van Essen, 1991) or DM. Overall, thedistribution of terminal label in these two cases was quitesimilar. The bulk of grains was seen in the PL and the PInuclei. In the PL nucleus, the terminal label was locateddorsally and laterally in the caudal part and ventrally andmedially in the rostral portion. In the PI nucleus, terminallabel was seen mainly in the dorsal sector. A limitedamount of grains was noted in the PM nucleus.

Injections of ventrolateralextrastriate cortex

In cases 14 and 15, the isotope injections were located inthe ventrolateral portion of the extrastriate region belowthe IOS. In case 14 (Fig. 17), the injection involved theventral part of area 19 corresponding in location to thedorsal portion of ventral area V4 (V4v; see, e.g., Fellemanand Van Essen, 1991) and also ventral area V3 (V3v; see,e.g., Boussaoud et al., 1990) or the ventral posterior area(VP; Newsome et al., 1986). In case 15 (Fig. 12), theinjection was located mainly on the ventral surface of thehemisphere in the region of ventral area 19 or area V4vand also in area V3v or VP. The distribution of terminallabel in these cases was quite similar. The main bulk ofgrains was seen in the PL and PI nuclei. In the PL nucleus,patches of terminal label were found predominantly in thecaudal one-third of the structure in ventrolateral andventromedial locations. Grains also extended into thelateral region of the PM nucleus. A significant amount oflabel occurred throughout the entire rostrocaudal extent ofthe PI nucleus, predominantly in a ventral and centrallocation (Fig. 16E). The one notable difference in thepattern of thalamic labeling in these two cases was thatthe grains in case 15 tended to be relatively more dense inthe PI nucleus than those in case 14. In case 16 (Fig. 13),the injection was placed in the ventral portion of area 19corresponding in location to the caudal portions of area


Fig. 2. Diagrammatic representation of the medial surface of thecerebral hemisphere showing an isotope injection site (blackened area)in the medial extrastriate region and coronal sections (A–G) depictingthe distribution of terminal label (dots) in the thalamus. BSC,brachium of the superior colliculus; CC, corpus callosum; Cd, caudatenucleus; CF, calcarine fissure; CINGS, cingulate sulcus; CL, centrallateral nucleus; CM, centromedian nucleus; CM-Pf, centromedian-parafascicular nucleus; GLd, dorsal lateral geniculate nucleus; GM,medial geniculate nucleus; Hb, habenula; LD, lateral dorsal nucleus;

Li, limitans nucleus; LP, lateral posterior nucleus; MD, medial dorsalnucleus; OTS, occipitotemporal sulcus; Pf, parafascicular nucleus; PI,inferior pulvinar nucleus; PL, lateral pulvinar nucleus; PM, medialpulvinar nucleus; PO, oral pulvinar nucleus; POMS, medial parietooc-cipital sulcus; R, thalamic reticular nucleus; RhF, rhinal fissure; SG,suprageniculate nucleus; THI, habenulointerpeduncular tract; VL,ventrolateral nucleus; VLps, ventrolateral nucleus, pars postrema;VPI, ventroposteroinferior nucleus; VPL, ventroposterolateral nucleus;VPM, ventroposteromedial nucleus.


Fig. 3. Diagrammatic representation of the medial surface of the cerebral hemisphere showing anisotope injection site in the dorsomedial extrastriate region (rostral to that of case 1) and coronal sections(A–F) depicting the distribution of terminal label in the thalamus. VPMpc, ventroposteromedial nucleus,parvocellular portion. For other abbreviations and conventions, see Figure 2.


Fig. 4. Diagrammatic representation of the medial surface of the cerebral hemisphere showing anisotope injection site in the dorsomedial extrastriate region (dorsal to that of case 1) and coronal sections(A–G) depicting the distribution of terminal label in the thalamus. CSL, central lateral superior nucleus.For other abbreviations and conventions, see Figures 2 and 3.


Fig. 5. Diagrammatic representation of the lateral surface of thecerebral hemisphere showing an isotope injection site in the dorsal-most portion of the lateral extrastriate region and coronal sections(A–F) depicting the distribution of terminal label in the thalamus.AD,anterior dorsal nucleus; AS, arcuate sulcus; CS, central sulcus; IOS,

inferior occipital sulcus; IPS, intraparietal sulcus; LF, lateral fissure;LS, lunate sulcus; Pcn, paracentral nucleus; PS, principal sulcus; STS,superior temporal sulcus. For other abbreviations and conventions,see Figures 2 and 4.

Fig. 6. Diagrammatic representation of the lateral surface of the cerebral hemisphere showing anisotope injection site in the dorsal portion of the lateral extrastriate region and coronal sections (A–G)depicting the distribution of terminal label in the thalamus. For abbreviations and conventions, seeFigures 2 and 5.


Fig. 7. Diagrammatic representation of the lateral surface of the cerebral hemisphere showing aisotope injection site in the central portion of the lateral extrastriate region and coronal sections (A–E)depicting the distribution of terminal label in the thalamus. For abbreviations and conventions, seeFigures 2 and 5.


Fig. 8. Diagrammatic representation of the lateral surface of the cerebral hemisphere showing aisotope injection site in the central portion of the lateral extrastriate region (ventral to that of case 8) andcoronal sections (A–G) depicting the distribution of terminal label in the thalamus. For abbreviations andconventions, see Figures 2 and 5.


Fig. 9. Diagrammatic representation of the lateral surface of the cerebral hemisphere showing anisotope injection site in the caudal bank of the superior temporal sulcus and coronal sections (A–F)depicting the distribution of terminal label in the thalamus. X, area X; VLm, ventrolateral nucleus,medial portion. For other abbreviations and conventions, see Figures 2 and 5.


Fig. 10. Diagrammatic representation of the lateral surface of the cerebral hemisphere showing anisotope injection site in the dorsal portion of the rostral bank of the lunate sulcus and coronal sections(A–E) depicting the distribution of terminal label in the thalamus. For abbreviations and conventions, seeFigures 2 and 5.


Fig. 11. Diagrammatic representation of the lateral surface of the cerebral hemisphere showing anisotope injection site in the anterior portion of the annectant gyrus and coronal sections (A–F) depictingthe distribution of terminal label in the thalamus. For abbreviations and conventions, see Figures 2 and 5.


V4v and of area V3v or VP. The injection occupied alocation medial as well as lateral to the occipitotemporalsulcus. Compared with cases 14 and 15, this injectionextended more ventromedially. The main bulk of terminallabel was seen in the PL and PI nuclei. In the PL nucleus,grains occupied a lateral location in the caudal part of thestructure. In contrast, terminal label in the PI nucleusoccurred throughout its rostrocaudal extent and was local-ized mainly in the ventral sector. A few grains also werenoted in the LP nucleus. In case 17 (Fig. 14), the injectionoccupied area 19 medial to the occipitotemporal sulcus,corresponding in location to the ventral portion of area V2v(see, e.g., Felleman and Van Essen, 1991). The main bulkof terminal label was found in the ventral portion of the PInucleus throughout its entire rostrocaudal extent (Fig.16F). Label also was seen in the caudal portion of the PLnucleus in a lateral location. In addition, a few smallclusters of grains were noted in the LP nucleus. In case 18(Fig. 15), the injection involved the ventromedial portion ofarea 19 corresponding in location to the ventral portion ofarea V2v. This injection was somewhat more medial anddorsal than that of the preceding case. A limited amount ofterminal label was seen in a lateral location in thecaudalmost part of the PL nucleus. Likewise, a smallamount of grains was observed in a lateral locationcaudally in the PI nucleus and in a medial locationrostrally in the nucleus.

DISCUSSION

The major thalamic projections of the extrastriate corti-ces are directed to the pulvinar, lateral posterior, intralami-nar, and LD nuclei. The present results indicate that thereare different patterns of corticothalamic connectivity fromvarious regions of the extrastriate cortex (see Table 1).Thus, the dorsomedial extrastriate region (cases 1–3)projects mainly to the PL nucleus, with lesser projectionsto the PI, PM, and PO nuclei. The dorsal part of the medialextrastriate region (cases 2, 3) also projects to the LP, theLD, and the intralaminar nuclei (CL and CSL). Likewise,the dorsal portion of the lateral extrastriate region (e.g.,cases 5, 7) has strong connections with the PL and lesserconnections with the PI, PM, and PO nuclei. In addition,this region projects to the LP and LD nuclei as well as tothe intralaminar nuclei (CL, CSL, and Pcn). The centralportion of the preoccipital gyrus (cases 8, 9) has connec-tions with the PL and the PI nucleus. However, in contrastto the medial and dorsal preoccipital cortices, this regionhas stronger connections with the PI nucleus, relativelylittle connectivity with the LP and the intralaminar nuclei,and no projections to the LD nucleus. The ventralmostpart of the lateral preoccipital region (e.g., case 15) hasstronger connections with the PI than with the PL nucleusand also has relatively minor connections to the PMnucleus. This region has no projections to the LP, LD, orintralaminar nuclei. The ventromedial part of the extrastri-ate cortex (e.g., cases 16, 17) also has a stronger connec-tional relationship with the PI than with the PL nucleusand has no connectivity with either the PM or the POnucleus. In contrast to the ventrolateral extrastriate cor-tex, but similar to the dorsomedial and the dorsolateralcortices, the ventromedial region has some projections tothe LP and the intralaminar nuclei. Area V4t, or MTc, ofthe STS (case 10) has thalamic projections that are similarto those of the dorsal extrastriate region, that is, strong

connections to the PL and PI nuclei and relatively limitedprojections to the PM and intralaminar nuclei. Finally, theannectant gyrus (e.g., case 12) projects strongly to the PLand PI nuclei and less so to the PM nucleus.The main bulk of corticothalamic connections from the

extrastriate region is directed toward the PL and PI nuclei,and a differential topography of these projections appearsto be evident in both nuclei. Within the PL nucleus, theextrastriate region occupying the central portion of themedial surface of the hemisphere (cases 1, 18) projectsmainly to the lateral and ventral portions of the nucleus.In contrast, the dorsomedial and dorsolateral regions(cases 2, 3, 5, 7) have connections clustered mainly in thedorsal portion of the PL nucleus. The central portion of thelateral extrastriate region (cases 8, 9) tends to haveprojections concentrated in more ventral and medial sec-tors of the PL nucleus, a pattern also seen from area V4t,or MTc (case 10), and the annectant gyrus (e.g., case 12).The ventralmost part of the lateral preoccipital region(case 15) tends to project to the ventromedial sector of thePL nucleus, whereas the ventromedial extrastriate region(cases 16, 17) has the bulk of its projections in thecaudalmost part of the nucleus in a more lateral location.With regard to the PI nucleus, the central portion of themedial extrastriate cortex (cases 1, 18) projects to themedial sector of this structure. The dorsolateral andcentral portions of the lateral extrastriate cortex as well asarea V4t, orMTc, and the annectant gyrus project predomi-nantly to dorsal and central sectors of the PI nucleus. Incontrast, the ventral and ventromedial extrastriate corti-ces project mainly to ventral and medial sectors of the PInucleus. These observations regarding differential inputfrom extrastriate cortices to various sectors of the PInucleus are supportive of the recent proposal of theexistence of discrete subdivisions within the nucleus (Guti-errez et al., 1995).Only a limited number of studies have examined the

corticothalamic connectivity of the extrastriate region, andthese have dealt mainly with the cortex of the lateralportion of the hemisphere. Our observations essentiallyare in agreement with those of previous investigations, butthey provide additional information. Benevento and Davis(1977) have shown that the dorsalmost portion of theextrastriate region has strong connections to the PLnucleus and more limited projections to the PI and PMnuclei. They also reported projections to the LP and LDnuclei from this region. Our findings (see cases 5 and 7)demonstrate further that the dorsalmost extrastriate cor-tex has connections to the PO nucleus as well as tointralaminar nuclei, specifically, to CL, CSL, and Pcn.With regard to the central sector of the lateral extrastriatecortex, the present results indicate that this region projectsto the PL, PI, PM, and LP nuclei, consistent with thefindings of Benevento and Davis (1977). Moreover, ourobservations show that this region has connections to thePO and VLps nuclei. The present data indicate that, as oneprogresses into the ventral sector of the lateral extrastri-ate cortex below the IOS, the connections to the PI nucleusseem to be more marked than those to the PL nucleus.Similar findings have been reported by Benevento andDavis (1977), but, in contrast to those investigators, we didnot note any projections to the LP nucleus from this regionof the extrastriate cortex. With regard to the cortex of thecaudal bank of the STS, the projections of area V4t, orMTc,resemble those of the central portion of the lateral extrastri-


Fig. 12. Diagrammatic representation of the ventral surface of thecerebral hemisphere showing an isotope injection site in the ventrolat-eral extrastriate region and coronal sections (A–F) depicting thedistribution of terminal label in the thalamus. IOS, inferior occipital

sulcus; LOS, lateral orbital sulcus; MOS, medial orbital sulcus; STS,superior temporal sulcus; V, lateral ventricle; VPMpc, ventropostero-medial nucleus, parvocellular portion. For other abbreviations andconventions, see Figure 2.


Fig. 13. Diagrammatic representation of the medial surface of the cerebral hemisphere showing anisotope injection site involving the cortex on both sides of the occipitotemporal sulcus and coronal sections(A–F) depicting the distribution of terminal label in the thalamus. For abbreviations and conventions, seeFigure 2.


Fig. 14. Diagrammatic representation of the ventral surface of the cerebral hemisphere showing anisotope injection site in the ventromedial extrastriate region and coronal sections (A–G) depicting thedistribution of terminal label in the thalamus. For abbreviations and conventions, see Figures 2 and 12.


Fig. 15. Diagrammatic representation of the ventral surface of the cerebral hemisphere showing anisotope injection site in the ventromedial extrastriate region (medial to that of case 17) and coronalsections (A–F) depicting the distribution of terminal label in the thalamus. For abbreviations andconventions, see Figure 2.


Fig. 16. Photomicrographs showing the distribution of terminallabel in the thalamus following isotope injections in various extrastri-ate regions. A: Case 3 following an injection in the medial extrastriateregion.B:Case 5 following an injection in the dorsolateral extrastriateregion. C: Case 9 following an injection in the lateral extrastriateregion. D: Case 10 following an injection in the caudal portion of the

superior temporal sulcus. E: Case 14 following an injection in theventrolateral extrastriate region. F: Case 17 following an injection inthe ventromedial extrastriate region. LP, lateral posterior nucleus; PI,inferior pulvinar nucleus; PL, lateral pulvinar nucleus; PM, medialpulvinar nucleus; PO, oral pulvinar nucleus. Scale bar 5 1 mm.

ate cortex. This sulcal region has strong projections to thePL nucleus, somewhat less marked connections to the PInucleus, and much less extensive projections to the PMnucleus. Ungerleider et al. (1984) and Squatrito et al.(1988) have described connections from the caudal part ofareaMT, which adjoins area V4t, orMTc, rostrally, to thesesame thalamic nuclei. However, those investigators haveshown that area MT projects predominantly to the PInucleus.The present study demonstrates that, in addition to the

connections from the lateral preoccipital region to thethalamus, there are sizable corticothalamic projectionsfrom the dorsomedial, ventromedial, and annectant por-tions of the extrastriate cortex. Whereas the dorsomedialregion (cases 2, 3) projects strongly to the PL nucleus andhas virtually no connections to the PI nucleus, the ventro-medial region (cases 16, 17) has extensive projections to

the PI nucleus and less marked connections to the PLnucleus. The existence of connections from the medialextrastriate region to the pulvinar complex is consistentwith the corticothalamic connectivity of the PL nucleus, asshown by retrograde tracing methods (Trojanowski andJacobson, 1977) and with observations of the corticotha-lamic connectivity of the PI nucleus using anterogradetracing methods (Mizuno et al., 1983). Both the dorsome-dial and the ventromedial extrastriate regions have connec-tions to the PM, LP, and CL nuclei. Although the dorsome-dial region projects to the LD, VL, and CSL nuclei, theventromedial region appears to have no such connectivity.The projections from the annectant gyrus resemble thoseof the dorsolateral extrastriate region, except that thereappears to be no connectivity to the LP, LD, and intralami-nar nuclei. Finally, it appears that the corticothalamicconnections to the pulvinar nuclei that were observed in

Fig. 17. Diagrammatic representations of the medial, lateral, andventral surfaces of the cerebral hemisphere showing the locations ofisotope injection sites for nonillustrated cases. AS, arcuate sulcus; CS,central sulcus; IOS, inferior occipital sulcus; IPS, intraparietal sulcus;

LF, lateral fissure; LS, lunate sulcus; MOS, medial orbital sulcus; PS,principal sulcus; STS, superior temporal sulcus. For other abbrevia-tions and conventions, see Figure 2.

TABLE 1. Summary of Extrastriate-Thalamic Projections

Extrastriate area(s)

Thalamic nuclei1

Pulvinar Intralaminar

LP VLps VL LD VLPL PI PM PO CL CSL Pcn

Medial 18/19 (case 1) 111 1Medial 19 (case 2) 11 1 1 11Dorsomedial 19 (PO, case 3) 11 1 1 1 1 11 1 1 1 1Dorsal 19 (DP, case 5) 111 1 1 1 1 1 1 11 1Dorsal 19 (V4d, case 7) 111 1 1 1Central 19 (V4, case 9) 111 11 1 1Caudal STS (V4t, case 10) 111 11 1 1Dorsal lunate sulcus (V4d-V3, case 11) 11 11 1 1Annectant gyrus (V4-V3a, case 12) 111 11 1Ventral 19 (V4v-V3/VP, case 15) 11 111 1Ventromedial 19 (ventral V2v, case 17) 11 111 1 1Ventromedial 19 (ventromedial V2v, case 18) 1 11

1CL, central lateral nucleus; CSL, central lateral superior nucleus; DP, dorsal prelunate area; LD, lateral dorsal nucleus; LP, lateral posterior nucleus; Pcn, paracentral nucleus; PI,inferior pulvinar nucleus; PL, lateral pulvinar nucleus; PM, medial pulvinar nucleus; PO, oral pulvinar nucleus; PO, parietooccipital area; V2v, ventral visual area 2; V3, visual area3; V3a, visual area 3a; V4, visual area 4; V4d, dorsal visual area 4; V4v, ventral visual area 4; V4t, V4 transitional area; VL, ventrolateral nucleus; VLps, ventrolateral nucleus, parspostrema; VP, ventral posterior area.


the present study reciprocate the thalamocortical projec-tions that have been demonstrated by other investigators(Benenvento and Rezak, 1976; Trojanowski and Jacobson,1976; Kikuchi et al., 1985; Tanaka et al., 1990; Baleydierand Morel, 1992).Within the extrastriate region, several anatomically and

physiologically distinct visual areas have been identified(see, e.g., Colby and Duhamel, 1991; Felleman and VanEssen, 1991; Kaas, 1997). Although our injections are notlimited strictly to such specific regions, nevertheless, itseems that discrete visual areas have differential overallpatterns of connectivity with the thalamus. Thus, forexample, area DP of the dorsolateral extrastriate regionhas sizable projections to the PL nucleus and, in addition,has connections with the PI, PM, PO, LP, intralaminar,and LD nuclei. In contrast, area V4d or DLhas connectionsto the PL, PI, and PM nuclei and to the VLps nucleus.AreaV4t, or MTc, has connections to the PL, PI, and PM nucleias well as to the Pcn nucleus. The rostral portion of theannectant gyrus has connections only to the pulvinarnucleus, specifically to the lateral, inferior, and medialdivisions. Area V4v projects to the PL and PI nuclei.Finally, whereas areas DP, V4d, and V4t (or MTc) all havepreferential projections to the PLnucleus, areaV4v projectsstrongly to the PI nucleus.The differential thalamic connectivity of extrastriate

areas shown in the present study can be viewed in terms ofquadrantic visual field topography at the cortical andthalamic levels (Bender, 1981, 1982; Gattass et al., 1988).Thus, areas that lie within the lower visual field represen-tation in the dorsal extrastriate cortex (see, e.g., cases 1, 5)tend to project to the dorsal sector of the PI nucleus, whichcontains the lower visual field representation. In contrast,areas located within the upper visual field representationin the ventral extrastriate cortex (see, e.g., cases 15, 17)are related preferentially to the ventral portion of the PInucleus, which contains the upper visual field representa-tion. These observations are consistent with the report ofBenevento and Davis (1977).The extrastriate areas have been conceptualized as

being comprised of distinct dorsal and ventral streams ofvisual information processing. From our observations, itappears that these visual pathways have different overallpatterns of corticothalamic connectivity, particularly withthe pulvinar complex. The dorsal stream, which includesareas of the dorsomedial and dorsolateral extrastriatecortex and which has been linked with the peripheralvisual field and with visuospatial processes (see, e.g.,Mishkin et al., 1983; Van Essen et al., 1992), projectsstrongly to the PL nucleus and has relatively less connec-tivity to the PI, PM, and PO nuclei. In contrast, the ventralstream, which includes areas of the ventral extrastriatecortex and which has been shown to serve the centralvisual field and visual object identification (see, e.g.,Mishkin et al., 1983; DeYoe et al., 1994), projects preferen-tially to the PI nucleus and has less marked connections tothe PL and PM nuclei. In this regard, it should be pointedout that Baleydier and Morel (1992) have demonstrated adichotomous pattern of thalamocortical projections to dor-sal and ventral stream visual areas beyond the extrastri-ate cortex.The existence of differential patterns of corticothalamic

connectivity from extrastriate regions is consistent withthe connectional relationships described for the efferentprojections of these regions to other cortical and subcorti-

cal forebrain structures. For example, it has been shownthat the dorsal extrastriate region projects preferentiallyto the dorsal portions of the prefrontal and premotorcortices both directly and indirectly via the posteriorparietal cortex (Jones and Powell, 1970; Jacobson andTrojanowski, 1977; Mesulam et al., 1977; Petrides andPandya, 1984; Barbas, 1988; Colby et al., 1988; CavadaandGoldman-Rakic, 1989;Morel andBullier, 1990; Tanakaet al., 1990; Baizer et al., 1991). In contrast, the ventralextrastriate region has been shown to project strongly tothe ventral portions of the prefrontal and premotor corti-ces directly as well as indirectly via the inferotemporalcortex (Kuypers et al., 1965; Jones and Powell, 1970;Chavis and Pandya, 1976; Jacobson and Trojanowski,1977; Desimone et al., 1980; Huerta et al., 1987; Barbas,1988; Morel and Bullier, 1990; Baizer et al., 1991; Distleret al., 1993). A similarly dichotomous organization hasbeen shown for the corticostriatal connections of theextrastriate regions. Thus, the dorsal extrastriate regionprojects preferentially to the dorsal and lateral portions ofthe head and body of the caudate nucleus and to thecaudodorsal sector of the putamen (Saint-Cyr et al., 1990;Yeterian and Pandya, 1995b). The ventrolateral extrastri-ate region projects mainly to the ventral sector of the bodyand to the genu and the tail of the caudate nucleus and thecaudal portion of the putamen (Whitlock and Nauta, 1956;Kemp and Powell, 1970; Graham et al., 1979; Van Hoesenet al., 1981; Saint-Cyr et al., 1990; Baizer et al., 1993;Steele and Weller, 1993; Webster et al., 1993; Yeterian andPandya, 1995b). Thus, it seems that the connectionalorganization of the extrastriate region with regard tocorticothalamic as well as corticocortical and corticostria-tal pathways reflects the concept of parallel distributedcircuitry within the forebrain (see, e.g., Alexander et al.,1986; Goldman-Rakic, 1988).It is of interest to view the differential corticothalamic

connectivity of the extrastriate region in the context ofphysiological studies of specific divisions of the pulvinar.In the PI and the adjoining ventral portion of the PLnucleus of macaque monkeys, retinotopic organization hasbeen demonstrated (Bender, 1981, 1982), as mentionedabove. Moreover, the PI nucleus has been shown to have arole in processes such as visual fixation, visual patterndiscrimination, and attending to salient stimuli (see, e.g.,Gould et al., 1974; Chalupa et al., 1976; Acuna et al., 1983;Robinson and Petersen, 1992). In contrast, the dorsalportion of the PL nucleus has no clear-cut retinotopicorganization, contains neurons that are directionally sen-sitive, and appears to have a different functional role inprocesses such as visuospatial attention and spatiallydirected reaching (see, e.g., Benevento and Miller, 1981;Acuna et al., 1983; Petersen et al., 1985, 1987; Beneventoand Port, 1995). The differential connectivity to the PL andPI nuclei from the dorsal and ventral extrastriate regionsmay play a role in this functional differentiation of visualprocesses.

ACKNOWLEDGMENTS

We are very grateful to Andrew Doolittle for excellenttechnical assistance. This study was supported by theDepartment of Veterans Affairs, Edith Nourse RogersMemorial Veterans Hospital, Bedford, Massachusetts; byNIH grant 16841; by Colby College Social Science grants


01 2220 and 01 2239; and by theAudrey and Sheldon KatzResearch Fund of Colby College.

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Corticothalamic connections of extrastriate visual areas in rhesus monkeys

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