Tuning dissimilarity explains short distance decline of spontaneous spike correlation in macaque V1

Fast spike correlation is a signature of neural ensemble activity thought to underlie perception, cognition, and action. To relate spike correlation to tuning and other factors, we focused on spontaneous activity because it is the common 'baseline' across studies that test different stimuli, and because variations in correlation strength are much larger across cell pairs than across stimuli. Is the probability of spike correlation between two neurons a graded function of lateral cortical separation, independent of functional tuning (e.g. orientation preferences)? Although previous studies found a steep decline in fast spike correlation with horizontal cortical distance, we hypothesized that, at short distances, this decline is better explained by a decline in receptive field tuning similarity. Here we measured macaque V1 tuning via parametric stimuli and spike-triggered analysis, and we developed a generalized linear model (GLM) to examine how different combinations of factors predict spontaneous spike correlation. Spike correlation was predicted by multiple factors including color, spatiotemporal receptive field, spatial frequency, phase and orientation but not ocular dominance beyond layer 4. Including these factors in the model mostly eliminated the contribution of cortical distance to fast spike correlation (up to our recording limit of 1.4mm), in terms of both 'correlation probability' (the incidence of pairs that have significant fast spike correlation) and 'correlation strength' (each pair's likelihood of fast spike correlation). We suggest that, at short distances and non-input layers, V1 fast spike correlation is determined more by tuning similarity than by cortical distance or ocular dominance.