Chapter 6 - Interareal Connections of the Macaque Cortex: How Neocortex Talks to Itself

Abstract

The neocortex forms a single sheet that is subdivided into 100 or more different functional areas in primates. One unifying concept is that the local circuits in the neocortex share the same basic organization and that the functional differences between cortical areas arise from differences in their afferent input—both from subcortical regions like the thalamus and other regions of neocortex. While investigations in the macaque monkey have provided us with the most complete and quantitative map of the interareal connections for any species, our knowledge of the organization of synaptic connections of these interareal pathways is still quite incomplete. We have investigated the macaque visual cortex in search of the design principles of the synaptic relationships formed by long-distance interareal projections. The pyramidal cells, which form the interareal projections, contribute only a tiny fraction of all the extrinsic excitatory synapses in a given target area. One lamina is the principal target, but frequently the axons form synapses in a secondary lamina. Most interareal synapses are formed with the spines of pyramidal cells. The GABAergic smooth cell dendrites constitute 0–20% of the target population. To explain why the tiny numbers of excitatory synapses that connect two areas are so effective, we suggest that the local recurrent circuit amplifies spatio-temporal patterns of excitation generated by long-distance connections—both thalamic and interareal. The specific computations within an area are a consequence of specific patterns of excitatory input from the long-distance projections that are shaped by excitatory and inhibitory activity evoked in the local circuit.