prefrontostriatal connections in relation to cortical architectonic organization in rhesus monkeys

THE JOURNAL OF COMPARATIVE NEUROLOGY 312:43-67 (1991)

Prefrontostriatal Connections in Relation to Cortical Architectonic Organization in

Rhesus Monkeys

EDWARD H. YETERIAN AND DEEPAK N. PANDYA Department of Psychology, Colby College, Waterville, Maine 04901 (E.H.Y.); Edith Nourse Rogers Memorial Veterans Hospital, Bedford 01730 (E.H.Y., D.N.P.), and Departments of

Anatomy and Neurology, Boston University School of Medicine, Boston 02118 (D.N.P.) and Harvard Neurological Unit, Beth Israel Hospital, Boston 02215 (D.N.P.), Massachusetts

ABSTRACT Prefrontostriatal connections were investigated in rhesus monkeys using the autoradio-

graphic technique to examine whether there are systematic relationships with regard to the architectonic organization of the prefrontal cortex. On the basis of progressive laminar elaboration, the different regions of the prefrontal cortex can be grouped into two architectonic trends. The dorsal trend, which begins in the medial proisocortical areas, can be followed through the dorsolateral prefrontal cortex, culminating in the dorsal arcuate region. The ventral trend, which originates in the orbital proisocortex, can be traced through the inferior prefrontal convexity to the ventral arcuate region. The results show that the main connections from the prefrontal cortex to the striatum are to the head and body of the caudate nucleus. These connections are topographically organized. Medial and dorsal prefrontal areas project predominantly to the dorsal and central portion of the head and body of the caudate nucleus, whereas orbital and inferior prefrontal areas are related mainly to the ventral and central portion. Moreover, prefrontostriatal connections have a medial-lateral topography. Medial and orbital prefrontal areas project medially in the head and body of the caudate nucleus, whereas the dorsal and ventral arcuate regions project laterally, adjacent to the internal capsule. The prefrontal regions above and below the principal sulcus project mainly to the intermediate sector of the head and body of the nucleus. However, there appears to be some degree of overlap of corticostriatal projections from the dorsal and ventral prefrontal regions, as well as within each trend. Relatively minor projections are directed to the putamen as well as to the tail of the caudate nucleus from certain subregions of the prefrontal cortex. Thus the distribution of prefrontostriatal connections seems to reflect the architectonic organization of the prefrontal cortex, Possible functional aspects of prefrontostriatal connectivity are considered in the light of behavioral and physiological studies.

Key words: cortex, prefrontal, striatum, caudate, putamen

Corticostriatal connections in primates have been stud- ied by a number of investigators in recent years in an attempt to provide overall principles of organization. Kemp and Powell ('70), using the silver impregnation technique, suggested that cortical projections to the striatum follow a simple topography based on the proximity of a given cortical area to a specific striatal region. Subsequent studies based on the autoradiographic method have revealed a more widespread distribution of corticostriatal connections and have provided further insight into organizational features (Goldman and Nauta, '77; Jones et al., '77; Yeterian and Van Hoesen, '78; Van Hoesen et al., '81; Selemon and Goldman-Rakic, '85; Stanton et al., '88). Thus, Yeterian

and Van Hoesen ('78) suggested that cortical areas that are reciprocally interconnected project, in part, to similar regions of the striatum. More recently, Selemon and Goldman- Rakic ('85) have shown a longitudinal organization of corticostriatal connections. These investigators have also emphasized that the striatal connections of cortically interconnected areas are organized predominantly in an interdig- itating manner. Alexander et al. ('86) have proposed that corticostriatal projections can be viewed as components of partially closed functional loops interrelating specific re-

Accepted June 6,1991.

o 1991 WILEY-LISS, INC.

44

gions of the cerebral cortex, basal ganglia, and thalamus. Corticostriatal connectivity has also been related to the intrinsic architectonic composition of the striatum, that is, to island and matrix compartments. It is suggested that these compartments may receive differential cortical connections and may have specific neurochemical properties (e.g., Goldman-Rakic, '82, '83).

A number of investigators have addressed corticostriatal connectivity from the standpoint of specific cortical regions (Whitlock and Nauta, '56; DeVito and Smith, '64; Nauta, '64; Johnson et al., '68; Kemp and Powell, '70; Goldman and Nauta, '77; Jones et al., '77; Kunzle and Akert, '77; Jacobson et al., '78; Kunzle, '78; Yeterian and Van Hoesen, '78; Van Hoesen et al., '81; Selemon and Goldman-Rakic, '85; Huerta et al., '86; Stanton et al., '88; Saint-Cyr et al., '90). It has been shown that there are substantial connections from various regions of the prefrontal cortex to the striatum and that these connections have differential topographic distributions (DeVito and Smith, '64; Nauta, '64; Johnson et al., '68; Kemp and Powell, '70; Goldman and Nauta, '77; Kunzle and Akert, '77; Jacobson et al., '78; Kunzle, '78; Yeterian and Van Hoesen, '78; Selemon and Goldman-Rakic, '85; Huerta et al., '86; Stanton et al., '88). For example, the dorsolateral prefrontal region projects heavily to the dorsal portion of the head of the caudate nucleus, whereas the orbital region has major connections to the ventral sector of the head of the caudate (Nauta, '64; Johnson et al., '68; Kemp and Powell, '70; Goldman and Nauta, '77; Kunzle, '78; Yeterian and Van Hoesen, '78; Selemon and Goldman-Rakic, '85). None of these studies, however, has specifically examined relationships between the overall architectonic organization of the prefrontal region and patterns of corticostriatal connectivity.

Recent studies have shown that cortical (Petrides and Pandya, '84, '88; Barbas, '86; Barbas and Pandya, '89) and thalamic (Giguere and Goldman-Rakic, '88; Siwek and Pandya, in press) connections of the prefrontal region are related systematically to patterns of cortical architectonic organization. It is of interest to see whether the organization of prefrontostriatal connections also parallels architectonic differentiation at the cortical level. In the present study, we have examined patterns of connectivity from the

E.H. YETERIAN AND D.N. PANDYA

AS CA cc Cd CF CING S cs Gld GP IC 10s IPS LF LS MOS OTS POMS PS Pu Rh F STS Th TO V

Abbreviations

arcuate sulcus anterior commissure corpus callosum caudate nucleus calcarine fissure cingulate sulcus central sulcus dorsal lateral geniculate nucleus globus pallidus internal capsule inferior occipital sulcus intraparietal sulcus lateral fissure lunate sulcus medial orbital sulcus occipitotemporal sulcus medial parietooccipital sulcus principal sulcus putamen rhinal fissure superior temporal sulcus thalamus optic tract lateral ventricle

prefrontal cortex to the caudate nucleus and the putamen following isotope injections in different architectonic regions on the medial, orbital, and lateral surfaces. The data suggest that there is a dorsal-ventral and medial-lateral topography of corticostriatal connections related systematically to the architectonic features of prefrontal regions.

MATERIALS AND METHODS The corticostriatal connections of the prefrontal cortex

were traced in 19 rhesus monkeys (Macaca mulatta) by using radioactively labeled amino acids. A craniotomy was performed under sodium pentobarbital anesthesia, and two discrete injections (3H-leucine and 3H-proline, total volume 0.4-1.0 pl; specific activity 40-80 $31) were made in a specific sector of the prefrontal cortex in each case. Follow- ing a survival time of 7-10 days, the animals were anesthe- tized deeply with sodium pentobarbital and perfused tran- scardially with isotonic saline followed by 10% formalin. The brains were removed, photographed, and processed for autoradiography according to the method of Cowan et al. ('72). Exposure times ranged from 3 to 6 months.

Each hemisphere was divided coronally into two or three blocks in the stereotaxic plane. The blocks were embedded in paraffin and cut into 10-km-thick sections in the coronal plane. Every tenth section was processed for autoradiography and stained with thionin. This stain permitted the analysis of cortical architecture, localization of the injection site, and identification of the boundaries of the striatum. The precise location of each injection site was determined by observing the cortical architecture around the labeled area, and comparing this with the architecture of the corresponding nonlabeled area in the cortex of the opposite hemisphere. The distribution of terminal label as revealed under darkfield illumination was charted onto coronal tracings of the striatum. From these tracings, the distribution of label was reconstructed in the sagittal profile of the caudate nucleus. The experimental material analyzed in this study has been used in other investigations (Barbas and Pandya, '89; Siwek and Pandya, in press).

RESULTS The most commonly used architectonic parcellation of

the prefrontal cortex in macaque monkeys is that of Walker ('40) (Fig. 1, upper diagrams), which has been the mainstay of many physiological, behavioral, and anatomical studies. More recently, Walker's schema has been reassessed according to the concept of the dual nature of cortical architectonic organization (Sanides, '69, '72; Barbas and Pandya, '89). Thus the basal and ventrolateral prefrontal regions (paleocortical trend) show progressive laminar differentiation beginning in the orbital paleocortex (Fig. lA, lower diagram). In contrast, the medial and dorsal prefrontal regions (archicortical trend) are characterized by progressive laminar differentiation beginning in the medial proisocortical regions (Fig. lB, lower diagram).

Isotope injections of medial and dorsolateral prefrontal regions

In case 1, the isotope injections were placed in the ventral portion of the medial prefrontal cortex, and involved portions of areas 14 and 25 (Fig. 2). The resulting label was observed in the head and body of the caudate nucleus, as

PREFRONTOSTRIATAL CONNECTIONS

ME

45

u VENTROLATERAL

BASAL

B MEDIAL

Fig. 1. Diagrams of the lateral, orbital (inferior or basal), and medial prefrontal regions of the rhesus monkey showing architectonic subdivisions according to Walker ('40) (upper three diagrams) and Barbas and Pandya ('89) (lower diagrams A and B).

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

3

Fig. 2. Diagrammatic representation of the medial surface of the cerebral hemisphere showing the injection site (dark area) in case 1, and the distribution of terminal label (shown as dots) in six representative rostral-to-caudal coronal sections through the caudate nucleus and

the putamen. In this and subsequent figures, the lower righthand diagram depicts the distribution of label reconstructed from coronal sections on a standard sagittal view of the caudate nucleus.

shown in sagittal profile in Figure 2 (lower right). Within the head of the caudate nucleus, grains were located in the medialmost Dortion (see Fin. 14A). occuDvinn the ventrome-

to the medial portion immediately adjacent to the lateral ventricle (Fig. 2, sections 1-6).*

" I" " dial region a't more rostral levels and a tral region caudally. The label continued in the rostra1 half of the body of the caudate nucleus and was confined strictly

*In the descriptions of the results, the caudate nucleus is subdivided into dorsal, central, and ventral sectors in the dorsoventral dimension, and into medial, intermediate, and lateral znnes in the mediolateral dimension.

PREFRONTOSTRIATAL CONNECTIONS 47

1 7 2

4

7 6 5 4

Fig. 3. Diagrammatic representation of the medial surface of the cerebral hemisphere showing the injection site in case 2 and the distribution of terminal label in seven representative coronal sections of the caudate nucleus and the putamen.

In cases 2 and 3, isotope injections were placed in area 32 on the medial surface. In both cases the isotope also spread into area 10 rostrally. Additionally the injections in case 2 (Fig. 3) extended more ventrally, whereas those in case 3 (not illustrated) also involved area 24 caudally. The distribution of terminal label in the head and body of the caudate

nucleus in case 2 resembled that of case 1 (Fig. 3, lower right). Grains were observed in the ventromedial and central sectors of the head and body of the caudate nucleus, with a similar rostral-caudal distribution. The main differences between cases 1 and 2 were that in case 2 label was found in the rostralmost portion of the head of the caudate


nucleus, as well as medially in the rostral portion of the tail. The other difference between cases 1 and 2 was that whereas the grains in the caudate nucleus in case 1 occupied the extreme medial portion, those in case 2 were somewhat less medial in location (Fig. 3, sections 1-7). In case 3, the rostral-caudal extent of label in the head and body of the caudate nucleus resembled that of case 2, but the distribution of grains differed in the medial-lateral dimension. In the head of the caudate nucleus, grains were observed in the intermediate as well as the medial portion. No evidence of terminal label was noted over the tail of the caudate nucleus. In both cases 2 and 3, some label was observed in the rostral and medial sectors of the putamen (not shown).

In case 4, the isotope injections were placed in the dorsal portion of area 10 (Fig. 4). The rostral-caudal extent of terminal label in the head and body of the caudate nucleus in this case resembled that of cases 2 and 3. However, the distribution of grains was relatively less ventral, occupying mainly a dorsomedial location. Like case 2, some label was noted also in the tail of the caudate nucleus, and in the rostromedial portion of the putamen (Fig. 4, sections 1-7).

In case 5, the isotope injections were placed in the dorsolateral prefrontal region and involved the middorsal portions of areas 46 and 9 (Fig. 5). The extent and distribution of terminal label in this case differed sharply from the previous cases. The label extended throughout all three subdivisions of the caudate nucleus. Within the head of the caudate nucleus, grains occupied primarily a dorsal location (see Fig. 14B), and remained in the intermediate portion between the internal capsule and the medial border of the nucleus. The label in the body of the caudate nucleus was distributed ventrally as well as dorsally. In the tail of the caudate nucleus, grains were found in intermediate as well as medial locations. The label in the putamen was observed to have a greater rostral-caudal extent than in the previous cases. The main bulk of grains was observed in the rostral part of the putamen, and was located more centrally than in the preceding cases. Caudally within the putamen, grains were ventromedial in location (Fig. 5, sections 1-8).

In cases 6 and 7 isotope injections were placed in area 46. The injection in case 6 extended into the upper bank of the principal sulcus (Fig. 6). The injection in case 7 (not illustrated) extended into area 9 dorsally and area 8 caudally. The basic pattern of terminal label in the striatum was similar in these cases. In case 6, grains were relatively less dorsal in location throughout the rostral-caudal extent of the head and the body of the caudate nucleus than in case 5. The strongest accumulations of label were in the intermediate portion of the nucleus. Label extended caudally in the body of the caudate nucleus, also in a dorsal location. A restricted amount of label was noted in the rostral part of the tail of the caudate nucleus. Label was also observed in the rostral part of the putamen, mainly in a dorsal location adjacent to the internal capsule (Fig. 6, sections 1-6).

In cases 8 and 9, isotope injections were placed in dorsal area 8 within the concavity of the arcuate sulcus. In case 8 (not illustrated), the injection extended into caudal area 46, whereas in case 9, the injection was confined strictly to area 8 (Fig. 7). In both cases the terminal label in the head (see Fig. 14C) and the body of the caudate nucleus was found mainly in the intermediate sector and in the central and lateral portion adjacent to the internal capsule. In the putamen, grains were located dorsomedially, in contrast to the preceding dorsolateral prefrontal cases. The distribu-

tion of label in case 9 was more restricted in the caudate nucleus and the putamen as compared to the preceding cases (Fig. 7, sections 1-6).

To summarize, the distribution of terminal label from medial prefrontal regions is mainly central and dorsal in the medial portion of the head and body of the caudate nucleus, whereas that from lateral and caudal prefrontal regions is primarily dorsal and lateral (see Fig. 15A,C). Label was noted in the tail of the caudate nucleus following injections in dorsomedial and dorsolateral prefrontal regions (cases 2, 4, 5, and 6). Label in the putamen as compared to the caudate nucleus is less extensive. Cases with dorsal and medial prefrontal injections have label in more rostral portions of the putamen, whereas those with injections in more lateral and caudal regions have label in more caudal parts of the putamen. Additionally, medial prefrontal injections result in label ventrally in the putamen, and caudal prefrontal injections dorsally in the nucleus.

Isotope injections of orbital and ventrolateral prefrontal regions

In three cases, isotope injections were placed in different sectors of the orbital frontal cortex. In case 10, the injection involved orbital proisocortex and rostrally adjoining area 13 (Fig. 81, whereas in case 11 (not illustrated) the injection involved area 12 as well as the proisocortex. The injection in case 12 was medial and rostral in location and involved areas 14, 11, and 10 (Fig. 9). The overall distribution of label in these three cases was similar, that is, label was found mainly in the medial and ventral portions of the head and body of the caudate nucleus and of the putamen. In case 10, label occurred throughout the rostral-caudal extent of the head and body of the caudate nucleus, occupying a medial and intermediate location, and was also seen medially in the tail of the caudate nucleus (Fig. 8, sections 1-7). The label in the putamen occupied a ventromedial location throughout most of the rostral-caudal extent of the nucleus. The distribution of label in case ll was somewhat less medial in the head and body of the caudate nucleus than in case 10. The label in the tail of the caudate nucleus and in the putamen was less extensive caudally. In case 12, the label in the head and the body of the caudate nucleus was located mainly in medial and intermediate sectors, and also extended laterally to the internal capsule (Fig. 9, sections 1-6; see Fig. 14D). No label was noted in the tail of the caudate oucleus, or in the caudal portion of the putamen.

In another two cases isotope injections were placed in the ventrolateral prefrontal cortex, involving areas 12 and 46. In case 13 the injection involved the lateral portion of area 12 (Fig. lo), whereas the injection in case 14 (not illustrated) involved area 12 as well as the adjacent part of area 46. The distribution of terminal label in the striatum was similar in these two cases. In case 13, label was observed mainly in the ventral and central sector of the head and body of the caudate nucleus, in intermediate and lateral locations extending to the internal capsule. Label was noted in the medial portion of the putamen, at rostral, middle, and caudal levels of the nucleus (Fig. 10, sections 1-6). Compared to the orbital frontal cases, the label in this case did not extend as far ventrally or medially in the head of the caudate nucleus.

In cases 15 (Fig. 11) and 16 (not illustrated), injections were placed in the frontal polar region, and involved area 10


CASE 4

3

-2

Fig. 4. Diagrammatic representation of the medial surface of the cerebral hemisphere showing the injection site in case 4 and the distribution of terminal label in seven representative coronal sections of the caudate nucleus and the putamen.

as well as the adjoining portion of ventral area 46. The distribution of terminal label was similar in these cases. In both cases, the main bulk of grains was observed in the head and body of the caudate nucleus. Label occurred mainly in medial and intermediate locations, and tended to avoid the dorsalmost and ventralmost regions (Fig. 11, sections 1-7; see Fig. 14F). A restricted amount of terminal

label was noted medially in the tail of the caudate nucleus. Additionally, label was seen in a rostra1 and ventral location in the putamen.

In cases 17 and 18, the injections were placed in area 46. In case 17, the injection extended more ventrally (Fig. 121, whereas in case 18 (not illustrated) the injection extended into the depth of the lower bank of the principal sulcus. In


k

CASE 5

4

....... d' ,:!:;$ 9 .. .:... 2

1

Y 5

2

8

Fig. 5. Diagrammatic representation of the lateral surface of the cerebral hemisphere showing the injection site in case 5 and the distribution of terminal label in eight representative coronal sections of the caudate nucleus and the putamen.

6

the latter case, there was additional involvement of dorsal area 46 in the upper bank of the principal sulcus. In both cases, terminal label in the head of the caudate nucleus was observed in an intermediate and lateral location, extending to the central portion of the internal capsule (Fig. 12, sections 1-7; see Fig. 14E). In case 18, however, a smaller

zone of terminal label was also noted in the dorsomedial part of the head of the caudate nucleus, distinct from the primary projection zone located more ventrally. This could be due to the involvement of dorsal area 46 in the injection site (see case 6, Fig. 6). In addition, grains were noted in the body of the caudate nucleus, mainly in a ventral location.


CASE 6

I

3

1 L

4

4 5 6

Fig. 6. Diagrammatic representation of the lateral surface of the cerebral hemisphere showing the injection site in case 6 and the distribution of terminal label in six representative coronal sections of the caudate nucleus and the putamen.

Label was observed medially in the putamen in cases 17 and 18, although the rostral-caudal extent was greater in the latter case.

In case 19, the isotope injections were placed in the ventral part of area 8 in the concavity of the arcuate sulcus (Fig. 13). Like the dorsal area 8 case (case 91, the terminal label in this case was relatively restricted, and was intermediate and lateral in location within the caudal portion of the

head as well as in the body of the caudate nucleus (Fig. 13, sections 1-6). Label avoided the dorsalmost and ventralmost portions of the caudate nucleus. Minor label occurred in the caudal part of the putamen in a dorsal location.

In summary, the distribution of grains within the head and body of the caudate nucleus from orbital prefrontd regions is primarily medial and ventral in location, whereas that of lateral and caudal prefrontal regions tends to be


CASE 9

.:. .._ . ....

Pu

cd?



CASE 10

3 4

6 7

Fig. 8. Diagrammatic representation of the orbital surface of the cerebral hemisphere showing the injection site in case 10 and the distribution of terminal label in seven representative coronal sections of the caudate nucleus and the putamen.

lateral and central (Fig. 15B,D). Label appears in the tail of the caudate nucleus only in cases involving the orbital and frontal polar regions. In the putamen, the orbital cases have label mainly in rostral and ventral locations, whereas the lateral and caudal prefrontal regions tend to have label in more caudal and dorsal portions.

In all cases, as has been reported previously (e.g., Gold- man and Nauta, '771, the grains were distributed in the form of distinct patches. These occurred either as discrete

clusters against an unlabeled background, or as relatively dense patches on a background of lighter labeling (see Fig. 14).

DISCUSSION Organization of prefrontostriatal connections

Prefrontostriatal connections have been examined by a number of investigators (DeVito and Smith, '64; Johnson et


CASE 12

3

....: ... . ;:,.,..;. p .. -.: .:...... ..'

b-- 1 ..

L

6 5 4

Fig. 9. Diagrammatic representation of the orbital surface of the cerebral hemisphere showing the injection site in case 12 and the distribution of terminal label in six representative coronal sections of the caudate nucleus and the putamen.


-

CASE 13

, .:. .: . . 0 .:.... ,. . . .. .. . . .. ' b

6 5 4

W 2

5


al., '68; Kemp and Powell, '70; Goldman and Nauta, '77; Kunzle and Akert, '77; Jacobson et al., '78; Kunzle, '78; Yeterian and Van Hoesen, '78; Selemon and Goldman- Rakic, '85; Huerta et al., '86; Stanton et al., '88). The organization of these connections has been viewed from different perspectives (Kemp and Powell, '70; Yeterian and Van Hoesen, '78; Selemon and Goldman-Rakic, '85; Alex-

ander et al., '86; Goldman-Rakic and Selemon, '86). In view of the differences in neuroanatomical techniques and in the specific cortical areas examined by various investigators, it is difficult to make direct comparisons between the present cases and those of previous studies. Nevertheless, there is an overall consistency in the topography of prefrontostriatal connections as described by other investigators and in

56


CASE 15

3

1 2

Q Cd . . .,. __.. :. . ... 4 .... .::__

4

4 5 6 7

Fig. 11. Diagrammatic representation of the lateral surface of the cerebral hemisphere showing the injection site in case 15 and the distribution of terminal label in seven representative coronal sections of the caudate nucleus and the putamen.

the present study. Thus, Kemp and Powell ( '70) have shown that the medial prefrontal region is related mainly to the dorsal part of the head of the caudate nucleus. The dorsolateral prefrontal cortex has been found to project to the dorsal-intermediate and lateral sectors of the head of

the caudate nucleus (Kemp and Powell, '70; Goldman and Nauta, '77; Kiinzle, '78; Yeterian and Van Hoesen, '78; Selemon and Goldman-Rakic, '85). In contrast, the ventrolateral prefrontal region is related primarily to the interrne- diate and lateral sectors of the ventral portion of the head of


3

(cd3 b 1

2

4


the caudate nucleus (Kiinzle, '78; Yeterian and Van Hoe- sen, '78; Selemon and Goldman-bkic, '85). Finally, the orbital frontal cortex projects ventrally and medially in the head of the caudate nucleus (Kiinzle, '78; Yeterian and Van Hoesen, '78; Selemon and Goldman-Rakic, '85). Our observations are essentially in agreement with those of other investigators. Moreover, the present study provides a com- prehensive view of corticostriatal connections in relation to

the architectonic features of different subregions of the prefrontal cortex.

Several investigators have subdivided the prefrontal cortex on the basis of architectonic features (Brodmann, '09; Vogt and Vogt, '19; Walker, '40; von Bonin and Bailey, '47). More recently, it has been suggested that the subregions of the prefrontal cortex can be organized according to two progressive architectonic trends (Sanides, '69; Barbas and

58

CASE 19

3

cda Of-

/:? (- gQ

E.H.

%

YETERIAN AND D.N. PANDYA

I 5

1 2 3 4 S 6 (a . . . ..._. _.: l/lJ-Ll-J .:.. . . .._:... .:;. . . :. . ..... .

_....


Pandya, '89). The dorsal, or archicortical, prefrontal trend contains a series of areas with progressive architectonic differentiation from the medial proisocortices toward the dorsolateral prefrontal region (dorsal area 8). Likewise, the ventral, or paleocortical, trend stems from the orbital proisocortex and progresses toward the ventrolateral prefrontal region (ventral area 8) (Barbas and Pandya, '89). The proisocortical areas of the archicortical and paleocortical trends are characterized by a predominance of infragran-

ular neurons and a lack of fourth layer neurons. Within each trend, from the proisocortices toward more lateral isocortical regions, there is a progressive increase in third and fourth layer neurons.

The corticostriatal projections of prefrontal regions appear to correlate with the architectonic progressions as described above. Thus medial and orbital prefrontal regions, with less differentiated architectonic features, project predominantly to the medial and intermediate portion of


Fig. 14. Photomicrographs showing the distribution of terminal label in the head of the caudate nucleus following isotope injections in various regions of the prefrontal cortex. A, case 1; €3, case 5; C, case 8; D, case 12; E, case 18; F, case 16. Bar in F = 2 rnm.

59


Fig. 15. Summary diagrams showing the connectional relationships between the dorsal and ventral architectonic trends of the prefrontal cortex and the caudate nucleus in the coronal plane.


\ -

Fig. 16. Summary diagrams showing the connectional relationships between the dorsal and ventral architectonic trends of the prefrontal cortex and the caudate nucleus in the sagittal plane.

the head and body of the caudate nucleus. In contrast, the highly differentiated caudal prefrontal region (area 8) projects mainly to the lateral and intermediate portion. The lateral prefrontal region, which has intermediate architectonic features, is related preferentially to the intermediate portion of the head and body of the caudate nucleus (Fig. 15). Moreover, the dorsal prefrontal areas belonging to the archicortical trend are related mainly to the dorsal portion of the head and body of the caudate nucleus, whereas the ventral areas of the paleocortical trend are connected preferentially with the ventral portion (Fig. 16). Neverthe- less, our data indicate that there is a certain degree of intermingling of projections from areas within the dorsal and ventral trends in the central sector of the head of the caudate nucleus. It should be pointed out that the topography of prefrontal projections to the tail of the caudate nucleus is less distinct. The medial portion of the tail receives projections from the dorsal and ventral proisocortical areas as well as from the dorsomedial (dorsal area 10) and dorsolateral (dorsal areas 9 and 46) portions of the prefrontal cortices.

In comparison to prefrontocaudate connections, the projections of the prefrontal cortex to the putamen are less extensive, and in most instances appear to be continuous with those to the caudate nucleus. The projections also appear to have a dorsal-ventral topography. Thus dorsal trend regions (areas 10, 9, 46, and 8) project mainly to dorsal and central parts of the putamen. In contrast, ventral trend regions (areas Pro, 13, 12, 14, 10, and 46) project to ventral and central portions of the putamen, with the exception of ventral area 8, which projects to the dorsal

part of the putamen. In addition, within each trend, projections to the putamen from more differentiated regions of the prefrontal cortex tend to be more dorsal.

The distribution of prefrontal projections to the striatum, when viewed in a sagittal orientation, appears to be longitudinal in nature, although the projections tend to occur in discrete patches. These observations are in agreement with those of previous investigations (e.g., Selemon and Goldman-Rakic, '85). Moreover, not all prefrontal regions have the same rostral-caudal extent of projections within the caudate nucleus. For example, within the dorsal or archicortical trend, the longitudinal extent of projections within the caudate nucleus from the dorsal arcuate region is less than that of dorsal areas 9 and 46 (Figs. 5, 7). Similarly, within the ventral or paleocortical trend, the projections from the ventral arcuate region are less extensive than those from the orbital cortex (Figs. 8, 13).

The proposed concept of corticostriatal organization, based on the dual nature of prefrontal architecture, is consistent with other afferent and efferent connectivity of this region. The relationship between the progressive architectonic features and the distribution of corticostriatal projections of the prefrontal cortex is paralleled by prefron- tothalamic connections, which also are organized in a medial-lateral and a dorsal-ventral manner (Giguere and Goldman-Rakic, '88; Siwek and Pandya, in press). Accord- ingly, medial and orbital prefrontal regions are connected with the medial portion of the mediodorsal (MD) nucleus (magnocellular division, MDmc), whereas the caudal prefrontal region (area 8) is connected with the lateral portion (multiform division, MDmf). The lateral prefrontal cortex


is related to the intermediate portion of the MD nucleus (parvicellular division, MDpc). Like the prefrontostriatal connections, dorsal trend prefrontal regions are connected preferentially with the dorsal part of the MD nucleus, whereas ventral trend areas are related mainly to the ventral portion of the nucleus. Thus both striatal and thalamic connections of the prefrontal cortex have similar patterns of topographic organization.

The long association connections to the prefrontal cortex also seem to be organized according to the concept of dual architectonic trends. For example, the proisocortical area of the superior temporal gyrus (area Pro) and adjacent area Tsl are connected preferentially with the orbital and medial prefrontal cortices, whereas the highly differentiated areas of the superior temporal gyrus (areas Tpt and paAlt) are related to the caudal prefrontal cortex (area 8). The intermediate portion of the superior temporal gyrus is related to the lateral prefrontal cortex (Pandya and Yete- rian, '85; Petrides and Pandya, '88). Thus the architectonic areas of the auditory association cortices within the superior temporal gyrus are related to those areas of the prefrontal cortex that have similar architectonic features. Prefrontal connections of the parietal association cortex are also consistent with the concept of two architectonic trends within the frontal lobe. The superior parietal regions comprising the archicortical trend are connected preferentially with the dorsal and medial prefrontal cortices, whereas the inferior parietal areas belonging to the paleocortical trend are related mainly to the ventrolateral and orbital prefrontal cortices (Pandya and Yeterian, '85). A similar dichotomous organization has been described for the visual system (Rosene and Pandya, '83; Barbas, '88). The visual association areas of the ventral and dorsomedial occipitotemporal cortices relating to the peripheral visual field (archicortical trend) project mainly to the dorsal prefrontal region. In contrast, the areas of the inferotemporal region involved in central vision (paleocortical trend) are related preferentially to the ventral prefrontal region (Pandya and Yeterian, '85).

It seems, therefore, that the architectonic organization of the prefrontal cortex may be a major substrate for connectional relationships at the subcortical and cortical level. Our data suggest that there may be several anatomically distinct corticostriatal circuits originating from the prefrontal cortex. These circuits can be viewed as components of larger integrated systems involving cortical as well as other subcortical connections of specific prefrontal regions. Thus, for example, the connections from the medial prefrontal region to the dorsomedial portion of the head and body of the caudate nucleus, along with related thalamic (dorsal MDmc) and cortical (medial parietal region, medial preoccip- ital area, and rostral superior temporal gyrus) connectivity may act in concert to subserve common functions. Like- wise, the ventrolateral prefrontal cortex, which projects to the ventral-intermediate portion of the head of the caudate nucleus and to the medial putamen, along with related thalamic (ventral MDpc) and cortical (middle levels of the inferior parietal and the inferior temporal cortices, and of the superior temporal gyrus) regions, may have a role in similar functions. This notion is in agreement with the concepts of parallel distributed circuitry proposed by Alex- ander et al. ('86) and by Selemon and Goldman-Rakic ('88), but with cortical architecture as the specific anatomical underpinning.

As mentioned above, there appears to be a partial intermingling of the corticostriatal connections arising in dorsal

and ventral prefrontal areas, as well as of those originating from adjacent regions within each prefrontal architectonic trend. These observations are of interest in view of the intrinsic connections of the prefrontal cortices. It has been shown that there are sequential connections that parallel the architectonic differentiation within the dorsal and the ventral trend, from the proisocortices toward the caudal prefrontal region. Despite the segregation of connectivity within each trend, it has been shown that the dorsal and ventral prefrontal regions are interconnected at several levels (Barbas and Pandya, '89), including connections between proisocortical areas of the orbital and medial surfaces, between areas 9 and 12, and between the dorsal and ventral sectors of the arcuate region. The intermingling of corticostriatal projections from prefrontal areas within and between architectonic trends may reflect the interrelat- edness of these areas at the cortical level.

Functional considerations The precise functional significance of differential prefron-

tostriatal connectivity remains to be determined. One way to address this issue is to examine the specific functions of prefrontal areas and of connectionally related striatal regions. Both classic and more recent studies suggest that prefrontal areas are engaged in several different functions that can be viewed in light of the dual architectonic and connectional organization of the prefrontal cortex. Several investigators have demonstrated differential functions for dorsal vs. ventral prefrontal regions. For example, Mishkin and colleagues have pointed out that the deficits in monkeys with lateral vs. orbital frontal lesions appear to be of different types (Brutkowski et al., '63; Mishkin, '64; Mishkin et al., '69; Iversen and Mishkin, '70). Thus the inferior prefrontal and the orbital areas are thought to be more closely related to the reversal aspects of testing (as evi- denced by perseverative deficits), whereas the lateral region is tied to spatial factors. Subsequent behavioral studies have yielded essentially similar findings with regard to dichotomous functions of dorsal vs. ventral prefrontal regions, emphasizing spatial functions for the former and a role in responsle inhibition for the latter (Lawicka et al., '75; Deuel and Mishkin, '77; Mishkin and Manning, '78; Oscar- Berman, '78; Rosenkilde et al., '81). More recently, Bachev- alier and Mishkin ('86) have shown that animals with ventromedial prefrontal (VM) lesions, which included the anterior portion of the cingulate gyrus as well as the medial prefrontal and the orbital cortices, had deficits in visual object recognition. In contrast, animals with dorsolateral (DL) lesions, which included peri-principalis cortex and the dorsolateral prefrontal cortex extending to midline, were impaired on a spatial delayed response task. Bachevalier and Mishkin iconcluded that whereas the VM region is involved in cognitive memory processes, the DL region subserves spatial functions. In another study involving more discrete prefrontal lesions, Mishkin and Bachevalier ('86) found that the orbital cortex was involved in object memory, and that the medial prefrontal (anterior cingulate) cortex is involved in spatial memory. Physiological studies also have implied that there is a dichotomy in the functions of dorsal vs. ventral prefrontal regions. Fuster and colleagues (Fuster et al., '82; Fuster, '841, usinga series of short-term memory tasks, have shown that peri- principalis and dorsolateral prefrontal neurons are more involved in delay or memory functions, whereas neurons in ventral and orbital prefrontal regions are more responsive to stimuli or cues.


In addition to the differential functional roles observed for dorsal vs. ventral prefrontal regions, there is evidence for functionally distinct subsectors within each architectonic trend. With regard to the dorsal trend, there is a relative paucity of behavioral studies involving discretely either the medial prefrontal cortex or the superior prefrontal convexity. Nevertheless, the medial prefrontal region (anterior cingulate area) appears to be involved in spatial memory (Mishkin and Bachevalier, '861, whereas the superior prefrontal convexity has been implicated in kinesthetic function (Goldman et al., '71; Mishkin et al., '77; Manning, '78; Rosenkilde, '79). The peri-principalis region, in contrast, is generally thought to play a role in tasks that depend upon memory for spatial information, that is, working or representational memory (French and Harlow, '62; Goldman and Rosvold, '70; Abplanalp and Mirsky, '73; Pohl, '73; Niki, '74a,b; Passingham, '75, '85; Bauer and Fuster, '76; Niki and Watanabe, '76; Goldberg et al., '80; Kojima and Goldman-Rakic, '82, '84; Kojima et al., '82; Batuev et al., '85; Goldman-Rakic, '87; Quintana et al., '88; Funahashi et al., '89, '90; Carlson et al., '90). Other studies have suggested different functional roles for the peri- principalis region and the adjacent dorsolateral prefrontal cortex, including the integration of spatial and visual information (Gaffan and Harrison, '89), the motivational evaluation of sensory stimuli (Yajeya et al., '891, and effecting strategy in self-ordered tasks (Traverse and Latto, '86; Petrides, '89).

In contrast to the dorsal prefrontal trend, which is related to kinesthetic, motivational, and spatial factors, the ventral prefrontal trend appears to be involved in autonomic and emotional, response inhibition, and stimulus significance functions. The orbital region has been shown to have a role in social and emotional behavior (Butter et al., '68; Butter and Snyder, '72; Raleigh and Steklis, '81), in response inhibition (Butter et al., '63; Passingham, '72a,b; Passingham and Ettlinger, '72; Stamm, '73) and in the formation of new memories (Voytko, '85; Kowalska et al., '84, '86). Physiological studies have also shown a role for the orbital cortex in autonomic and visceral functions (see Rosenkilde, '79 for review; also Nakano et al., '84), in olfactory and gustatory processing (Tanabe et al., '75; Rolls et al., '89, 'go), and in response to reward in learning paradigms (Rosenkilde et al., '81). In contrast, the cortex of the inferior convexity is involved in response inhibition (Iversen and Mishkin, '70, '73), but not in autonomic or emotional functions (Rosenkilde, '79). The inferior prefrontal convexity also has been shown to play a role in processes relating to the behavioral significance of stimuli (Suzuki and Azuma, '77; Kojima, '80; Watanabe, '86, '90) as well as in reward (Rosenkilde et al., '81). Moreover, it has been suggested that the cortex of the inferior convexity is involved in immediate visual memory (Pizlo et al., '90).

Compared to the dorsal and ventral prefrontal regions above and below the principal sulcus, the cortex in and around the arcuate sulcus seems to have a different functional role. I t is well established that this region is involved in processes important for attention and orientation, partic- ularly in the visual sphere (Kennard and Ectors, '38; Kennard, '39; Welch and Stuteville, '58; Latto, '78, '86; Pigarev et al., '79; Crowne et al., '81, '89; Goldberg and Bushnell, '81; Rizzolatti et al., '81b; Collin et al., '82; Crowne, '83; Suzuki and Azuma, '83; Bruce and Goldberg, '84, '85; Azuma, '85; Bruce et al., '85; Goldberg and Bruce, '85; Suzuki, '85; Goldberg et al., '86; Vaadia et al., '86; van der Steen et al., '86; Goldberg and Segraves, '87, '90;

63

Lawler and Cowey, '87; Lynch, '87; Pragay et al., '87; Azuma et al., '88; Keating and Gooley, '88; Barone and Joseph, '89; Boch and Goldberg, '89) and in the auditory and somatosensory modalities as well (Welch and Stuteville, '58; Rizzolatti et al., '81a; Crowne, '83; Azuma and Suzuki, '84; Suzuki, '85; Vaadia et al., '86). In addition, the arcuate region has been implicated in integrative functions such as crossmodal matching and intermodal association (Petrides and Iversen, '76; Van Hoesen et al., '80) and conditional associative learning (Stamm, '73; Podbros et al., '80; Pet- rides, '82, '85, '86, '87).

The functions of striatal regions that receive connections from the prefrontal cortex reflect, in part, those of the areas with which they are heavily interconnected. In general, it has been shown that lesions, or electrical stimulation, of the head of the caudate nucleus result in cognitive deficits (in delayed alternation, delayed response, and go, no-go tasks), perceptuomotor alterations, and visceral-autonomic changes that resemble those observed after frontal lobe lesions (Rosvold and Delgado, '56; Rosvold et al., '58; Dean and Davis, '59; Battig et al., '60; Battig et al., '62; Teuber and Proctor, '64; Cianci, '65; Rosvold, '68; Bossom, '65, '72; Stamm, '69; Woodburne, '71). Moreover, functional specificity for striatal subregions related to either the dorsal or ventral prefrontal sector has been demonstrated in a number of studies. Thus damage to the anterodorsal portion of the head of the caudate nucleus results in deficits in delayed alternation performance, whereas ablation of the ventrolat- era1 sector produces deficits in an object-reversal paradigm (Divac et al., '67). These results are complemented by those of other investigators. Bowen ('69) observed visuomotor deficits (misreaching and poor manual tracking) following lesions that involved primarily the dorsal portion of the head of the caudate nucleus. Cohen ('72) found that electrical stimulation of the anterodorsal portion of the head of the caudate nucleus produced deficits in delayed alternation performance. In contrast to the dorsal portion of the head of the caudate nucleus, lesions of the ventral sector produce deficits of a different nature. Butters and Rosvold ('68) observed that lesions of the ventral portion of the head of the caudate nucleus resulted in increased resistance to extinction in a conditioning paradigm, and in increased perseverative errors in delayed alternation, imply- ing a role in the regulation of response tendencies. Rubin- stein and Delgado ('63), using brain stimulation techniques, found that the ventral sector of the head of the caudate nucleus was more closely related to visceral functions than either the rostral or central sectors.

Thus, lesion-behavior and stimulation studies suggest that the dorsal sector of the head of the caudate nucleus, like the dorsolateral prefrontal cortex, may be related to spatial functions, whereas the ventral sector, like the ventral prefrontal cortex, is involved in visceral-autonomic functions and in the regulation of response tendencies (Divac, '72; Rosvold, '72; Iversen, '79; Rosenkilde, '79). Our connectional data imply that there may be additional functional specialization, from medial to lateral, within the dorsal and ventral sectors of the head of the caudate nucleus, reflecting differential functions of related prefrontal cortical regions. Behavioral studies of the striatum have not specifically addressed this issue. Several physiological investigations of the striatum have been carried out in an attempt to relate unit activity to behavior (Kitsikis et al., '71; Buser et al., '74; Anderson et al., '79; Aldridge et al., '80a,b; Rolls et al., '83; Rolls, '84; Nishino et al., '81, '84; Hikosaka and Sakamoto, '86a,b; Hikosaka et al., '89a,b,c;


Schultz and Romo, '88; Johnstone and Rolls, '90). However, few of these have dealt explicitly with the functions of distinct subsectors within major subdivisions of the striatum, e.g., within the head of the caudate nucleus. Neverthe- less, the results of certain studies imply that such medial to lateral specialization may exist. For example, Hikosaka et al. ('89a) have shown that neurons involved in the initiation of saccadic eye movements are located centrally and laterally in the head of the caudate nucleus. In contrast, Nishino et al. ('84) found that neurons related to ingestion during an operant task tended to be located medially within the head of the caudate nucleus, Hikosaka et al. ( '89~) have observed that neurons activated during cognitive tasks (e.g., expectancy of cue or target) are located centrally in the head of the caudate nucleus.

Although there is a paucity of behavioral studies that specifically address subsectors of the caudate nucleus, on the basis of prefrontostriatal connectivity and the known functions of prefrontal areas, functionally distinct corticostriatal circuitry has been suggested. Thus, Alexander et al. ('86) have proposed that connections from the dorsolateral prefrontal cortex to the dorsolateral portion of the head of the caudate nucleus are involved in spatial memory. Connec- tions from the lateral orbital frontal regions to the ventromedial sector of the head of the caudate nucleus are presumed to be involved in response inhibition. Connec- tions from the arcuate region (area 8) to the central portion of the body of the caudate nucleus are thought to be engaged in oculomotor function.

Based on a consideration of prefrontostriatal connectivity, and of functional aspects of the prefrontal cortex and the striatum as described above, we suggest the existence of additional functional corticostriatal circuits. The connections from the medial prefrontal region to the dorsomedial portion of the head and to the medial sector of the body of the caudate nucleus may have a role in motivational processes. In contrast, the connectivity from the superior prefrontal convexity to the dorsal-intermediate portion of the head of the caudate nucleus may subserve kinesthetic- spatial as well as mnemonic (working or representational memory) functions. Connections from the medial as well as the lateral orbital frontal cortex to the ventromedial sector of the head of the caudate nucleus and to the adjoining portion of the body can be viewed as having a role in the visceral-autonomic and emotional spheres. The connectivity from the inferior convexity to the ventral-intermediate sector of the head of the caudate nucleus may be involved in the regulation of response tendencies and also in immediate visual memory. Finally, the pathway between the arcuate region and the intermediate and lateral portion of the head and the body of the caudate nucleus may contribute to attentional, orientational and integrative processes as well as to oculomotor function.

In summary, the present observations reveal systematic connectional relationships between various architectonic regions of the prefrontal cortex and specific subsectors of the striatum. Although the frontal lobe classically was thought to have a unitary function, there is substantial evidence that specific prefrontal regions subserve differential processes (see, e.g., Rosenkilde, '79 for review). Despite relatively few behavioral studies, there is a suggestion of functional specificity within specific subdivisions of the striatum as well. The differential corticostriatal connectivity observed by other investigators as well as the architectonic-connectional relationships described in the present

study may provide a basis for further understanding of the functions of the prefrontal cortex and related subcortical areas.

ACKNOWLEDGMENTS We are very grateful to Michael Schorr, David Moser, and

David Randall for excellent technicd assistance. This study is supported by the Veterans Administration, Edith Nourse Rogers Memorial Veterans Hospital (Bedford, MA), by NIH grant 16841, and by Colby College Social Science grants A22132,012248, and 01 2265.

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