Architecture and intrinsic connections of the prefrontal cortex in the rhesus monkey

Authors

  • H. Barbas,

    1. Department of Health Sciences, Boston University, Boston, Massachusetts 02215
    2. Department of Anatomy, Boston University School of Medicine, Bedford, Massachusetts 01730
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  • D. N. Pandya

    1. Department of Anatomy, Boston University School of Medicine, Bedford, Massachusetts 01730
    2. Edith Nourse Rogers Veterans Administration Hospital, Bedford, Massachusetts 01730
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Abstract

An investigation of the architectonic organization and intrinsic connections of the prefrontal cortex was conducted in rhesus monkeys. Cytoarchitectonic analysis indicates that in the prefrontal cortex there are two trends of gradual change in laminar characteristics that can be traced from limbic periallocortex towards isocortical areas. The stepwise change in laminar features is characterized by the emergence and gradual increase in the width of granular layer IV, by an increase in the size of pyramidal cells in layers III and V, and by a higher cell-packing density in the supragranular layers. Myeloarchitectonic analysis reveals that the limbic areas are poorly myelinated, adjacent areas have a diffuse myelin content confined to the deep layers, and in isocortices the myelinated fibers are distributed in organized horizontal bands (of Baillarger) and a vertical plexus. Using the above architectonic criteria, we observed that one of the architectonic trends takes a radial basoventral course from the periallocortex in the caudal orbitofrontal region to the adjacent proisocortex and then to area 13. The next stage of architectonic regions includes orbital areas 12, 11, and 14, which is followed by area 10, lateral area 12, and the rostral part of ventral area 46. The last group includes the caudal part of ventral area 46 and ventral area 8. The other trend takes a mediodorsal course from the periallocortex around the rostral portion of the corpus callosum to the adjacent proisocortical areas 24, 25, and 32 and then to the medially situated isocortical areas 9, 10, and 14. The next stage includes lateral areas 10 and 9 and the rostral part of dorsal area 46. The last group includes the caudal part of dorsal area 46 and dorsal area 8.

The interconnections of subdivisions of the basoventral and mediodorsal cortices were studied with the aid of anterograde and retrograde tracers. Within each trend a given area projects in two directions: to adjoining regions belonging to succeeding architectonic stages on the one hand, and to nearby regions from the preceding architectonic stage on the other. In each direction there is more than one region involved in this projection system, paralleling the radial nature of architectonic change. Periallo- and proisocortices have widespread intrinsic connections, whereas isocortices situated at a distance from limbic areas, such as area 8, have restricted connections. Most interconnections are limited to areas within the same architectonic trend. However, there are links between cortices from the two trends, and these seem to occur between areas that are at a similar stage of architectonic differentiation.

The results suggest that there are two architectonically, and perhaps functionally, distinct axes within the prefrontal cortex. The earliest stages within each axis, which have widespread connections, may have a global role in neural processing. On the other hand, the latest stages, which have restricted connections, may have a more specific role in processes associated with the frontal lobe.

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