EXPERIMENTAL NEUROLOGY46, 402-408 (1975)

The

Projection

of Occipital Rhesus Monkey L. A. BENEVENTO

College

of

Medicine,

Cortex to Orbital (Macaca Mulatta)

in the

l AND JAMES H. FALLON

University Chicago, Illinois

Received

Cortex

September

of Illinois

Medical

Center,

60680 16, 1974

Near total lesions of occipital cortex were made in rhesus monkeys and the subsequent anterograde degeneration was analyzed using the Fink-Heimer technique. In addition to degenerated terminal endings seen in parietal, temporal and frontal cortices, sparse to moderately dense pericellular and terminal degeneration was seen in posterior portions of ventral orbital cortex and the inferior prefrontal convexity (lateral orbital cortex). These results indicate that activity from the visual cortex may directly influence cells of the frontal orbital cortex.

INTRODUCTION The frontal orbital cortex of the cat and monkey has been shown to be an area which receives convergent input from many sensory systems (2, 5, 9, 11). Physiological evidence in the cat (7) indicates a direct projection from the occipital cortex to the orbital cortex. However, in the rhesus monkey anatomical studies (S-10, 14) have indicated that occipital cortex does not project directly to orbital cortex. In these studies it was found that circumstriate cortex projects to portions of the inferior convexity of the temporal lobe which, in turn, has reciprocal connections with caudal parts of orbital cortex. These pathways form the basis of an indirect route whereby visual activity may reach the oribital cortex. Since physiological evidence indicates that a direct occipito-orbital projection may exist in the cat (7)) we were interested in investigating further the possibility that the occipital cortex projects directly to orbital cortex in the rhesus monkey. We

reinvestigated

the cortico-cortical

projections

of the occipital

cortex

of the rhesus monkey to determine if there is a direct route whereby visual 1 This study was supported by NSF Grant GB 35366X. J. H. Fallon was supported by NIMH training grant 83%. The technical assistance of Nodee DuBose in the preparation of the histological materials is greatly acknowledged. 402 Copyright All rights

Q 1975 by Academic Press, Inc. of reproduction in any form reserved.

OCCIPITO-ORBITAL

activity can reach the orbital scribed above.

cortex

403

PROJECTIONS

in addition

to the indirect

one de-

METHODS Three young, adult rhesus monkeys (2.4-4.5 kg) were used in the study. The animals were anesthetized with pentobarbital sodium (30 mg/kg). Cortical lesions were made by subpial aspirations under aseptic conditions. Lesions of the occipital cortex (areas OA, OB, OC) (17) (Fig. 1) were made and the animals were allowed to survive from 10 to 16 days. At the end of the survival period the animals were anesthetized with pentobarbital sodium and perfused intracardially with 0.9% saline, followed by 10% formalin. The brains were blocked transversally in a stereotaxic plane and stored for at least two weeks in 10% formalin. The brains were then placed in a 30% sucrose solution made with 10% formalin until they sank in the solution. Frozen sections were cut in the transverse plane at 30 pm and were subsequently stained at 300 pm intervals with Procedure I of the Fink-Heimer technique (6). Adjacent sections were stained by the cresyl violet technique. The pattern of degenerated fibers and associated “pericellular” and “terminal” degeneration was correlated with the cytoarchitectural features seen in the cresyl violet stained sections. The method of plotting the degeneration, staining techniques and the interpretation of degeneration are described in detail elsewhere (3, 4). RESULTS Figure 1A illustrates a reconstruction of the degeneration seen in the ipsilateral hemisphere after an occipital lobe lesion. The medial surface of the lesion is shown in Fig. 1B. In addition to pericellular and terminal degeneration found in parietal, temporal and frontal lobes, light density terminal and pericellular degeneration was also found in the inferior prefrontal convexity (lateral orbital cortex) as well as the ventral orbital cortex. Degenerated axons could be seen to originate from the lesion and to course rostrally in longitudinal fascicles. Near area 8 these axons gave rise to moderately dense pericellular and terminal degeneration about the arcuate and principal sulci. Othere axons coursed laterally and ventrally to enter the inferior prefrontal convexity as well as ventral orbital cortex to give rise to fields of sparse to moderately dense pericellular and terminal degeneration. The degenerated axons were of fine caliber and the terminal and pericellular degeneration in the inferior prefrontal convexity was found mainly in cortical layers V and VI (Fig. 2A). In some posterior areas of ventral orbital cortex, sparse degeneration could be found in all layers (Fig. 2B). The degeneration found in the inferior prefrontal convexity and ventral orbital cortex was removed from the degeneration seen in area 8 about

404

BENEVENTO

AND

FALLON

EC

FIG. 1. (A) Reconstruction of the lateral surface of the occipital lobe lesion is shown in solid black and pericellular and terminal degeneration in the cortex ipsilateral to the lesion is illustrated as black dots. The lesion extends about the occipital lobe and includes the medial surface of the lobe (Fig. 1B). The three arrows draw attention to degeneration that was seen in the ventral orbital cortex and the inferior prefrontal convexity, including fronto-opercular cortex (most posterior arrow). (B) Reconstruction of medial surface of the occipital lobe lesion illustrated in Fig. 1A. Abbreviations of sulci according to von Bonin and Bailey (17). The cortical damage in areas OC, 03 and OA is shown in solid black.

the arcuate and principal sulci. We verified the location of degeneration in orbital cortex using the histological criteria of von Bonin and Bailey (17) and Roberts and Akert (16). The degenerated occiptal axonal endings were found in an area of lateral orbital cortex that is defined by von Bonin and Bailey (17) as the inferior portion of granular cortical area FD and also includes the anterior portion of a transitional zone of granulated cortical areas FCD and FCOP (frontoopercular cortex) found between the Sylvian sulcus and the lower tip of the arcuate sulcus (Fig. 1A). The degenerated occipital axonal endings found in the ventral orbital cortex included area FF. These cortical areas also receive projections from nucleus medialis dorsalis of the thalamus (1, 16).

OCCIPIT~-~RBITAL

PRoJEcTIoNs

405

FIG. 2. Photomicrographs of sections stained with the Fink-Heimer technique showing predominantly sparse to moderately dense pericellular degeneration after near total lesion of areas OA, OB and OC of occipital lobe. (A) Degeneration in layer V of inferior prefrontal convexity. (B) Degeneration in layer IV of ventral orbital cortex (Approx. X 400).

DISCUSSION The degeneration observed in the present study adds to the findings of others (2, 5, 7-15) by revealing an additional afferent connection of the inferior prefrontal convexity and ventral orbital cortex of the rhesus monkey. The results show a direct connection between occipital cortex and the orbital cortices. The significance of these new findings will be discussed along with results that agree with and expand upon previously reported findings. Previous degeneration studies have reported cortical projections to the orbital cortex from contralateral cortex (e.g., 13), ipsilateral frontal and prefrontal cortices (e.g., 9, 10, 12, 14, 15) and tip of the temporal lobe (8,9,14). With the use of Nauta strains, Kuypers et al. (lo), Pandya and Kuypers (14), and Jones and Powell (9) have demonstrated multisynaptic cortical routes whereby visual activity can reach orbital cortex from occipital cortex. They showed that circumstriate cortex projects to the inferior convexity of the temporal lobe which, in turn, has reciprocal connections with orbital cortex. In contrast, the frontal areas receiving direct projections

406

BENEVENTO

AND

FALLON

from circumstriate cortex are found about the arcuate and principal sulci (9, 10, 14). The present results add to these studies by revealing a direct projection from the occipital cortex to the inferior prefrontal convexity and ventral orbital cortex. However, the present results cannot provide an answer as to which portion(s) of occipital cortex project to the orbital cortex, since the lesions of occipital cortex were extensive. On the other hand, it is possible to determine some general areas of occipital cortex that may project to orbital cortex by comparing the types the lesions made by previous authors and the present study. For example, Jones and Powell (9), Kuypers et al. (lo), and Pandya and Kuypers (14) made lesions of occipital cortex but did not report a direct projection to the orbital cortex. However, the lesions were made on the lateral surface of the occipital cortex and did not extend to the medial or most inferior sectors of the occipital cortex. In the present study the lesions were made in areas OC, OB and OA about the medial, lateral and inferior surfaces of the occipital lobe and a direct projection to the oribital cortex was seen. Therefore, the medial and/or inferior sectors of the occipital cortex may be the source(s) of direct fibers to orbital cortex. We used the histological criteria of von Bonin and Bailey (17) to determine the extent of our cortical lesions. The lesions were found to include all of area OC and a majority of areas OB and OA, but did not include adjacent parietal or temporal cortices. However, it is often difficult to determine the exact boundaries between area OA and adjacent parietal and temporal cortices (17). For this reason, it is necesary to discuss the possibility that small portions of adjacent cortices were damaged in the course of making occipital lobe lesions, and thus, accounted for the anterograde degeneration seen in the oribital cortex. For example, it has been demonstrated that posterior portions of the temporal cortex project to oribital cortex (9, 14). However, the lesions reported in the present study included cortex posterior to the inferior occiptal sulcus (dorsally) or cortex near the banks of the sulcus (ventrally). Thus, we do not believe we have damaged cortex outside of areas OA, OB and OC near the temporal cortex. ’ The lesions made in the present study also approached portions of the posterior parietal cortex. However, Jones and Powell (9) have shown that the inferior parietal lobule projects to prefrontal areas 45 and 46, but not adjacent areas of orbital cortex. In addition, Pandya and Kuypers (14) made lesions of the inferior parietal lobule and found that when they included cortex * In a recent abstract presented at the Society for Neuroscience (Oct. 1974, abs. #475), Moss reported that anterior, but not posterior infero-temporal cortex projects to two sectors of ventral prefrontal cortex. Thus, it is improbable that possible damage to posteriorinferotemporalcortex in the presentstudy led to degenerationseenin the same two sectors of prefrontal cortex, i.e., cortex ventral to the anterior portion of the principal sulcusand posteriororbital cortex.

OCCIPITO-ORBITAL

PROJECTIONS

407

near the lunate sulcus (case 3C), degeneration could be seen in dorsal areas of the inferior prefrontal convexity. When lesions were made in more anterior portions of the inferior parietal lobule that did not approach dorsal parts of the lunate sulcus (case 3D), degeneration in the inferior prefrontal convexity was slight or non-existent. Thus, posterior portions of the inferior parietal lobule and/or anterodorsal portions of occiptal cortex near the lunate sulcus may project to the inferior prefrontal convexity. We do not believe that we damaged portions of the inferior parietal lobule during our occipital lobe lesions, since the cytoarchitectural boundry between area OA of occipital cortex and area PG of the inferior parietal lobule is well demarcated (17). However, the cytoarchitectural boundary between area OA and area PE of the superior parietal lobule is gradual and indistinct (17). Therefore, it is possible that small portions of area PE were damaged in the course of making the occipital lobe lesions as described in the present study. Since area PE does not project to any portions of oribital cortex (9), it is not likely that damage to this area accounted for the degeneration seen in orbital cortex after lesions of the occipital cortex. In summary, the degeneration seen in the orbital cortex after our occipital lobe lesions does not seem to be due to damage to the parietal cortex. 8 The following conclusions can be made. The occipital cortex mediates the flow of visual activity to orbital cortex in at least two ways, an indirect route and a direct route. The indirect route is mediated by a projection from occipital cortex to the inferior convexity of the temporal lobe which, in turn, projects to oribital cortex (9, 14). The direct route, as described in the present study, is mediated by a projection from the occipital cortex to orbital cortex. Physiological studies in the cat (7) indicate a similar monosynaptic relationship between these cortices. 3 Since this manuscript was submitted, Tigges, Nezlrol. 158: 219-236) have shown in the squirrel 18 that there is a direct projection to the cortex focus similar to the one described here in frontal arcuate sulcus.

Spatz and Tigges (1974, J. Camp. monkey with small lesions of area of the inferior arcuate sulcus or a cortex found ventral to the inferior

REFERENCES K. 1964. Comparative anatomy of frontal cortex and thalamofrontal connections, pp. 372-396. In. “The Frontal Granular Cortex and Behavior.” J. M. Warren and K. Akert [Eds.]. McGraw-Hill, New York. 2. BENEVENTO, L. A. 1973. Synaptic mechanisms of orbital, insular, temporal tip cortex of the Rhesus monkey. Anat. Rec. 175: 498. 3. BENEVENTO, L. A., and F. F. EBNER. 1971. The areas and layers of cortico-cortical terminations in the visual cortex of the Virginia opossum. J. Conzp. Nezrrol. 141: 157-190. 1. AKERT,

408

BENEVENTO

AND

FALLON

L. A., and F. F. EBNER. 1971. The contribution of the dorsal lateral geniculate nucleus to the total pattern of thalamic terminations in striate cortex of the Virginia opossum. J. Comp. Neural. 143: 243-260. 5. BIGNALL, K. E., and M. IMBERT. 1969. Polysensory and cortico-cortical projections to frontal lobe of squirrel and rhesus monkey. Electroencephalogr. Cl&. Neurophysiol. 26 : 205-215. 6. FINK, R., and L. HEIMER. 1967. Two methods of selective sliver impregnation of degenerating axons and their synaptic ending in the central nervous system. Bra& Res. 4 : 369-374. 7. IMBERT, M., K. E. BIGNALL, and P. BUSER. 1966. Neocortical interconnections in the cat. J. Neurophysiol. 29: 382-395. 8 JONES, E. G. 1%9. Interrelationships of parieto-temporal and frontal cortex in the rhesus monkey. Bra& Res. 13 : 41-15. 9. JONES, E. G., and T. P. S. POWELL. 1970. An anatomical study of converging sensory pathways within the cerebral cortex of the monkey. Brain 93: 793-820. 10. KUYPERS, H. G. J. M., M. K. SZWARCBART, F. MISIIKIN, and H. E. ROSVOLD. 1965 Occipitotemporal corticocortical connections in the rhesus monkey. Exp. Neural. 11: 245-262. 11. LOE, P. R., and L. A. BENEVENTO. 1969. Auditory-visual interaction in single units in the orbito-insular cortex of the cat. Electroertcephalogr. Clin. Neurophysiol. 26 : 395-398. 12. PANDYA, D. N., P. DYE, and N. BUTTERS. 1971. Efferent cortico-cortical projections of the prefrontal cortex in the rhesus monkey. Brain Res. 31: 35-46. 13. PANDYA, D. N., E. A. KAROL, and D. HEILBRONN. 1971. The topographical distribution of interhemispheric projections in the corpous callosum of the rhesus monkey. Brain Res. 32: 31-43. 14. PANDYA, D. N., and G. J. M. KUYPERS. 1969. Cortico-cortical connections in the rhesus monkey. Brain. Res. 13 : 13-36. 15. PANDYA, D. N., and L. A. VIGNOLO. 1971. Intra-and interhemispheric projections of the precentral, premotor and arcuate areas in the rhesus monkey. Brain Res. 26 : 217-233. 16. ROBERTS, T. S., and K. AKERT. 1963. I. Insular and opercular cortex and its thalamic projection in Macaca mulatta. Schweiz. Arch. Nezlr. Psych. 92: l-43. 17. VON BONIN, G., and P. BAILEY. 1947. The neocortex of Macaca mulatta. University of Illinois Press, Urbana. 4. BENEVENTO,

The projection of occipital cortex to orbital cortex in the rhesus monkey (Macaca mulatta).

EXPERIMENTAL NEUROLOGY46, 402-408 (1975) The Projection of Occipital Rhesus Monkey L. A. BENEVENTO College of Medicine, Cortex to Orbital (Maca...
922KB Sizes 0 Downloads 0 Views