Topography of commissural fibers of the prefrontal cortex in the rhesus monkey

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  • Exp Brain Res (1984) 55:187-191 Ex mental Research

    9 Springer-Verlag 1984

    Research Note

    Topography of Commissural Fibers of the Prefrontal Cortex in the Rhesus Monkey

    H. Barbas and D.N. Pandya

    Edith Nourse Rogers Memorial Veterans Hospital, Bedford, MA, and Departments of Anatomy and Neurology, Boston University School of Medicine, and Department of Health Sciences, Boston University, Boston, MA 02215, USA

    Summary. The topography of commissural fibers of the prefrontal cortex was studied in the rhesus monkey using autoradiography. Commissural fibers originating in the medial prefrontal and the caudal orbital regions course through the anterior portion of the genu and the rostrum of the corpus callosum, while those from the arcuate concavity travel at the rostral border of the body of the corpus callosum. Fibers emanating from the peri-principalis region occupy an intermediate position in the genu of the corpus callosum.

    Key words: Prefrontal cortex - Commissural connec- tions - Rhesus monkey

    An understanding of the precise topography of commissural fibers is essential for physiologic investi- gations, as well as in clinical situations where callosal section is indicated to relieve intractable seizures. Previous studies have shown that commissural fibers of the frontal lobe in the rhesus monkey course through the rostral part of the corpus callosum. These fibers are topographically organized (Sunder- land 1940; Pandya et al. 1971). Fibers from the precentral gyrus (motor cortex and supplementary motor area) travel through the posterior portion of the rostral haft of the corpus callosum, while those from the premotor regions course in its dorsal and ventral sectors. Prefrontal fibers occupy a central position in the genu of the corpus callosum. These findings were based on ablation-degeneration experi- ments, in which the patterns of fiber degeneration following complete versus partial callosal section were compared. Therefore, the conclusions regard-

    Offprint requests to: H. Barbas, Ph.D., Boston University, 36 Cummington Street B-11, Boston, MA 02215, USA

    ing the topography of callosal fibers are indirect. The autoradiographic technique, developed subsequent to these studies, however, allows for a more precise delineation of cortical fiber pathways. In the present study we have investigated the topography of pre- frontal fibers within the corpus callosum in the rhesus monkey using autoradiographic procedures.

    Experiments were conducted in 12 rhesus mon- keys. Each received an isotope injection (3H leucine and proline, 0.4-1.0 ~xl; specific activity 40-80 ~tCi/ ~d), in a different sector of the frontal lobe (Fig. 1A). In six monkeys isotope injections were placed on the medial surface, and in dorsolateral regions above the principal sulcus. Six other animals received injections in the frontal cortex below the principal sulcus, and on the orbital surface~ The brains were processed for autoradiography according to the procedure described by Cowan et al. (1972). Labelled fibers were traced from the injection site to the corpus callosum in coronal sections. The location of commis- sural labelled fibers was reconstructed onto a tracing of the mid-sagittal surface of the hemisphere. The architectonic nomenclature of the frontal cortex in this report is based on the parcellation of Walker (1940) and Barbas and Pandya (1982).

    Following isotope injections on the medial sur- face of the frontal lobe below the rostral tip of the cingulate sulcus (areas 25 and 32), labelled fibers were observed in the rostral part of the genu of the corpus callosum (cases 1 and 2). When injections involved area 46 above the principal sulcus on the lateral surface of the hemisphere (cases 3 and 4), labelled fibers were observed in the genu of the corpus callosum, dorsal to the site of fibers originat-

    9 ing in the medial prefrontal regions described above. After injections in dorsal area 8 in the concavity of the arcuate sulcus (cases 5 and 6) labelled fibers were identified in the rostral part of the body of the corpus callosum. These were situated dorsal and caudal to

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    Fig. 2A-F. Darkfield photomicrographs of coronal sections of the cerebral hemisphere showing labelled fibers within the corpus callosum in six cases. Photographs A, B and C are taken from cases 1, 3, and 5 with isotope injections respectively in medial prefrontal, dorsal peri- principalis, and dorsal peri-arcuat 9 regions. Photographs D, E and F are taken from cases 7, 11 and 12 with isotope injections respectively in orbitofrontal, ventral peri-principalis, and ventral peri-arcuate regions

    those fibers arising from dorsal area 46. Figure 1B shows the location of label in three representative cases (cases 1, 3 and 5).

    In four animals with isotope injections in caudal orbital regions, and in areas 13 and 14 (cases %10), labelled fibers were found in the anterior portion of the genu and in the rostrum of the corpus callosum, overlapping the projection zone of the medial pre- frontal regions described above. In addition, some labelled fibers in these cases were also seen in the anterior commissure. When an isotope injection

    involved ventral area 46 and area 12 below the principal sulcus (case 11) label was observed in the genu of the corpus callosum, dorsal to the site of fibers originating from the orbital regions. The position of these fibers overlapped those arising from dorsal area 46. Finally, following isotope injection within ventral area 8 in the concavity of the arcuate sulcus, labelled fibers were found at the border of the genu and the body of the corpus callosum in a region caudal to the site of fibers emanating from the cortex below the principal sulcus. The location of these

    Fig. 1. A Drawings of the medial, lateral and basal surfaces of the cerebral hemisphere of the rhesus monkey showing the location of isotope injections in the prefrontal cortex in 12 animals. B Drawings of inid-sagittal sections of the corpus callosum and anterior commissure in six representative cases, showing the location of labelled callosal fibers (represented by dots). C Summary diagram showing the overlap of fibers within the corpus callosum arising from medial and orbital prefrontal areas, peri-principalis regions, and areas within the concavity of the arcuate snicus. Abbreviations: AC- anterior commissure; AS - arcuate sulcus; CC- corpus callosum; CF- calcarine fissure; CS - central sulcus; CING S - cingulate sulcus; lOS - inferior occipital sulcus; IPS - intraparietal sulcus; LF - lateral fissure; LS - lunate sulcus; OTS - occipitotemporal sulcus; POMS - medial parieto-occipital sulcus; PS - principal snicus; RhF - rhinal fissure; STS - superior temporal sulcus

  • 190

    fibers overlapped with that occupied by fibers originating from dorsal area 8. Figure 1B shows the location of label in three representative cases (cases 7, 11, and 12).

    The results indicate that there is a distinct topo- graphy of commissural fibers originating in the vari- ous sectors of the prefrontal cortex. Thus, fibers from medial and dorsolateral prefrontal regions respec- tively occupy the ventral and dorsal parts of the genu of the corpus callosum, while the dorsal arcuate region sends fibers through the rostral part of the body of the corpus callosum (Figs. 1 and 2A-C). Similarly, fibers from orbitofrontal and ventrolateral prefrontal regions respectively traverse the ventral and dorsal sectors of the genu, while those from the ventral arcuate region course at the border of the genu and the body of the corpus caUosum (Figs. 1 and 2D-F). These observations parallel those con- cerning the topography of commissural fibers originating in the parietal lobe of the monkey (Selt- zer and Pandya 1983), and in the visual cortex of the cat (Innocenti 1980).

    There is also evidence for overlap of the commis- sural fibers originating from the different regions of the prefrontal cortex. Thus, fibers emanating from ~ the medial prefrontal cortex overlap those arising from the orbital areas, Likewise, fibers from the dorsolateral and ventrolateral regions, above and below the principal sulcus, traverse the same callosal region. Commissural fibers originating in the dorsal and ventral arcuate areas also share a common callosal site (Fig. 1C). Finally, the anterior commis- sure carries a limited number of interhemispheric fibers originating exclusively from the caudal orbital region.

    A recent cytoarchitectonic study of the frontal lobe, based in part on the concept of "dual origin" of phylogenetic development of the cerebral cortex (Sanides 1970), showed that it is possible to trace two distinct architectonic trends in the prefrontal cortex (Barbas and Pandya 1982). One of these trends originates in the medial cortex around the rostral tip of the cingulate sulcus. This region, which consists of areas 25 and 32, is characterized by a bilaminar appearance and is considered proisocortical. From this area, regions with successively increasing laminar differentiation can be traced dorsally through areas 9, 10, 46 and 8. Likewise, in the caudal orbital surface another region adjacent to the olfactory tubercle, has a rudimentary laminar organization and is considered proisocortical. From this area a similar progressive laminar differentiation can be followed ventrally towards areas 13, 12, and ventral areas 10, 46 and 8. The present results indicate that commis- sural fibers originating in regions which have similar

    architectonic features in the two trends share a common place within the corpus callosum. This applies for regions which are distantly located within the frontal lobe, as well as for regions which are closely apposed. Thus, fibers from the two proisocor- tical areas, one situated on the medial and the other on the orbital surface, share a common site in the rostral portion of the corpus callosum. Likewise, dorsal and ventral peri-principalis regions have a similar architecture and a common callosal site. Dorsal and ventral arcuate regions are architectonic- ally similar and their callosal fibers also overlap (Fig. lC).

    These results, therefore, suggest that frontal cortical regions which are at a similar architectonic stage course through the same callosal site. It is possible that this is because regions with similar architectonic features may have developed at the same time. In addition, it appears that the relative rostro-caudal position of fibers within the corpus caUosum is determined by the relative architectonic differentiation of their frontal cortical region of origin. Thus, the commissural fibers of proisocortical regions with incipient laminar organization course in the most rostro-ventral sector, while fibers originat- ing from regions with more highly developed laminar differentiation are represented in successively more caudal sectors of the corpus callosum. Although our experiments do not include the entire prefrontal cortex, the present results suggest that neither the relative dorso-ventral, nor the rostro-caudal location of a frontal cortical region, but rather its relative architectonic differentiation determines the site of passage of its fibers through the corpus callosum.

    Acknowledgements. We wish to thank Dr. B. Seltzer for comments on the manuscript, and Mr. B. Butler and Ms. L. Kenton for excellent technical assistance. This study was supported by the Veterans Administration Edith Nourse Rogers Memorial Hospi- tal, Bedford, Massachusetts, NIH grant NS 16841, Seed grant GRS-691 from Boston University, and NSF grant BNS-8315411.

    References

    Barbas H, Pandya DN (1982) Cytoarchitecture and intrinsic connections of the prefrontal cortex of the rhesus monkey. Neurosci Abstr 8:268.3

    Cowan WM, Gottlieb DI, Hendrickson AE, Price JL, Woolsey TA (1972) The autoradiographic demonstration of axonal connections in the central nervous system. Brain Res 37: 21-51

    Innocenti GM (1980) The primary visual pathway through the corpus eallosum in morphological and functional aspects in the cat. Arch Ital Biol 118:124-188

    Pandya DN, Karol EA, Heilbronn D (1971) The topographic distribution of interhemispheric projections in the corpus callosum of the rhesus monkey. Brain Res 32:31-43

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    Sanides F (1970) Functional architecture of motor and sensory cortices in primates in the light of a new concept of neocortex 9 evolution. In: Noback C, Montagna W (eds) Advances in primatology, vol 1. Appleton-Century-Crofts, New York, pp 137-208

    Seltzer B, Pandya DN (1983) The distribution of posterior parietal fibers in the corpus callosum of the rhesus monkey. Exp Brain Res 49:147-150

    Sunderland S (1940) The distribution of commissural fibers in the corpus callosum in the macaque monkey. J Neurol Psychiat 3: 9-18

    Walker AE (1940) A cytoarchitectural study of the prefrontal area of the macaque monkey. J Comp Neurol 73:59-86

    Received December 6, 1983 / Accepted February 6, 1984

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