Organization of cortical afferent input to orbitofrontal areas in the rhesus monkey

Odorant signal processing takes place in a diverse group of primary olfactory areas which receive direct input from the olfactory bulb. Orbitofrontal cortices participate in olfactory functions, but the pathways through which they receive olfactory or other input have not been clearly defined. The retrograde tracers horseradish peroxidase and fluorescent dyes were injected in orbital cortices to study their afferent cortical connections. Labeled neurons in primary olfactory areas (prepiriform cortex, anterior olfactory nucleus and olfactory tubercle) were directed mainly to a posterior orbitofrontal region and to a lesser extent the neighboring caudal part of area 13. There was no evidence of direct projections from primary olfactory areas to the rostral parts of area 13, or to areas 12 or 11. Most labeled neurons in primary olfactory areas were directed to agranular cortices, fewer projected to dysgranular areas, and there was no evidence that any reached granular cortices. The areas which received the most robust olfactory projections showed the lowest degree of laminar organization among prefrontal cortices. Early processing in the olfactory system thus takes place in areas which differ sharply on structural grounds from "early" eulaminate post-Rolandic sensory cortices. In addition to olfactory cortical projections, numerous labeled neurons in transitional (limbic) cortices were directed to orbital areas, and fewer but still substantial numbers of afferent neurons were found in eulaminate cortices. Unlike post-Rolandic unimodal sensory areas, which seems to be committed to the processing of input from one sensory modality via sequential and/or parallel pathways, caudal orbital areas received highly distributed input from primary olfactory areas, and in addition, from gustatory, visual, auditory and somatosensory areas. The structural and connectional features of olfactory recipient orbital cortices thus differ markedly from those observed in other sensory association areas and suggest a mode of processing adapted early in cortical evolution.