Response Facilitation From the “Suppressive” Receptive Field Surround of Macaque V1 Neurons

Abstract

In primary visual cortex (V1), neuronal responses to optimally oriented stimuli in the receptive field (RF) center are usually suppressed by iso-oriented stimuli in the RF surround. The mechanisms and pathways giving rise to surround modulation, a possible neural correlate of perceptual figure-ground segregation, are not yet identified. We previously proposed that highly divergent and fast-conducting top-down feedback connections are the substrate for fast modulation arising from the more distant regions of the surround. We have recently implemented this idea into a recurrent network model ( Schwabe et al. 2006 ). The purpose of this study was to test a crucial prediction of this feedback model, namely that the suppressive “far” surround of V1 neurons can be facilitatory under conditions that weakly activate neurons in the RF center. Using single-unit recordings in macaque V1, we found iso-orientation far-surround facilitation when the RF center was driven by a low-contrast stimulus and the far surround by a small annular stimulus. Suppression occurred when the center stimulus contrast or the size of the surround stimulus was increased. This suggests that center-surround interactions result from excitatory and inhibitory mechanisms of similar spatial extent, and that changes in the balance of local excitation and inhibition, induced by surround stimulation, determine whether facilitation or suppression occurs. In layer 4C, the main target of geniculocortical afferents, lacking long-range intra-cortical connections, far-surround facilitation was rare and large surround fields were absent. This strongly suggests that feedforward connections do not contribute to far-surround modulation and that the latter is generated by intra-cortical mechanisms, likely involving top-down feedback.