Connectivity of somatosensory cortical area 1 forms an anatomical substrate for the emergence of multifinger receptive fields and complex feature selectivity in the squirrel monkey (Saimiri sciureus)

ABSTRACT Converging evidence shows that interaction of digit‐specific input, which is required to form global tactile percepts, begins as early as area 3b in the primary somatosensory cortex with the involvement of intrinsic lateral connections. How tactile processing is further elaborated in area 1, the next stage of the somatosensory cortical hierarchy, is less understood. This question was investigated by studying the tangential distribution of intrinsic and interareal connections of finger representations of area 1. Retrogradely labeled cell densities and anterogradely labeled fibers and terminal patches were plotted and quantified with respect to the hand representation by combining tract tracing with electrophysiological mapping and intrinsic signal optical imaging in somatosensory areas. Intrinsic connections of distal finger pad representations of area 1 spanned the representation of multiple digits indicating strong cross‐digit connectivity. Area 1 distal finger pad regions also established high‐density connections with homotopic regions of areas 3b and 2. Although similar to area 3b, connections of area 1 distributed more widely and covered a larger somatotopic representation including more proximal parts of the finger representations. The lateral connectivity pattern of area 1 is a suitable anatomical substrate of the emergence of multifinger receptive fields, complex feature selectivity, and invariant stimulus properties of the neurons. J. Comp. Neurol. 522:1769–1785, 2014. © 2013 Wiley Periodicals, Inc. Based on anatomical, optical imaging, and electrophysiological methods, the authors show that intrinsic connections of area 1 connect neighboring distal finger pad representations, whereas their interareal connections create strong connections with homotopic regions. Connections of area 1 distal pad regions spread into more proximal representation of the fingers.