Hierarchical organization of macaque and cat cortical sensory systems explored with a novel network processor

Neuroanatomists have described a large number of connections between the va rious structures of monkey and cat cortical sensory systems. Because of the complexity of the connection data, analysis is required to unravel what pr inciples of organization they imply. To date, analysis of laminar origin an d termation connection data to reveal hierarchical relationships between th e cortical areas has been the most widely acknowledged approach. We program med a network processor that searches for optimal hierarchical orderings of cortical areas given known hierarchical constraints and rules for their in terpretation. For all cortical systems and all cost functions, the processor found a mult itude of equally low-cost hierarchies. Laminar hierarchical constraints tha t are presently available in the anatomical literature were therefore insuf ficient to constrain a unique ordering for any of the sensory systems we an alysed. Hierarchical orderings of the monkey visual system that have been w idely reported, but which were derived by hand, were not among the optimal orderings. All the cortical systems we studied displayed a significant degr ee of hierarchical organization, and the anatomical constraints from the mo nkey visual and somatomotor systems were satisfied with very few constraint violations in the optimal hierarchies. The visual and somato-motor systems in that animal were therefore surprisingly strictly hierarchical. Most inc onsistencies between the constraints and the hierarchical relationships in the optimal structures for the visual system were related to connections of area FST (fundus of superior temporal sulcus). The found that the hierarch ical solutions could be further improved by assuming that FST consists of t wo areas, which differ in the nature of their projections. Indeed, we found that perfect hierarchical arrangements of the primate visual system, witho ut any violation of anatomical constraints, could be obtained under two rea sonable conditions, namely the subdivision of FST into two distinct areas, whose connectivity we predict, and the abolition of at least one of the les s reliable rule constraints. Our analyses showed that the future collection of the same type of laminar constraints, or the inclusion of new hierarchical constraints from thalamoc ortical connections, Mill not resolve the problem of multiple optimal hiera rchical representations for the primate visual system. Further data, howeve r, may help to specify the relative ordering of some more areas. This indet erminacy of the visual hierarchy is in part due to the reported absence of some connections between cortical areas. These absences are consistent with limited cross-talk between differentiated processing streams in the system . Hence, hierarchical representation of the visual system is affected by, a nd must take into account, other organizational features. such as processin g streams.