Cortical point-spread function and long-range lateral interactions revealed by real-time optical imaging of macaque monkey primary visual cortex

Abstract

Processing of retinal images is carried out in the myriad dendritic arborizations of cortical neurons. Such processing involves complex dendritic integration of numerous inputs, and the subsequent output is transmitted to multiple targets by extensive axonal arbors. Thus far, details of this intricate processing remained unexaminable. This report describes the usefulness of real-time optical imaging in the study of population activity and the exploration of cortical dendritic processing. In contrast to single- unit recordings, optical signals primarily measure the changes in transmembrane potential of a population of neuronal elements, including the often elusive subthreshold synaptic potentials that impinge on the extensive arborization of cortical cells. By using small visual stimuli with sharp borders and real-time imaging of cortical responses, we found that shortly after its onset, cortical activity spreads from its retinotopic site of initiation, covering an area at least 10 times larger, in upper cortical layers. The activity spreads at velocities from 100 to 250 μm/msec. Near the V1/V2 border the direct activation is anisotropic and we detected also anisotropic spread; the 'space constant' for the spread was ~2.7 mm parallel to the border and ~1.5 mm along the perpendicular axis. In addition, we found cortical interactions between cortical activities evoked by a small 'center stimulus' and by large 'surround stimuli' positioned outside the classical receptive field. All of the surround stimuli used suppressed the cortical response to the center stimulus. Under some stimulus conditions iso- orientation suppression was more pronounced than orthogonal-orientation suppression. The orientation dependence of the suppression and its dependency on the size of some specific stimuli indicate that at least part of the center surround inhibitory interaction was of cortical origin. The findings reported here raise the possibility that distributed processing over a very large cortical area plays a major role in the processing of visual information by the primary visual cortex of the primate.