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Abstract

Understanding the structure of multi-neuronal firing patterns in ensembles of cortical neurons is a major challenge for systems neuroscience. The dependence of network properties on the statistics of the sensory input can provide important insights into the computations performed by neural ensembles. Here, we study the functional properties of neural populations in the primary visual cortex of awake, behaving macaques by varying visual input statistics in a controlled way. Using arrays of chronically implanted tetrodes, we record simultaneously from up to thirty well-isolated neurons while presenting sets of images with three different correlation structures: spatially uncorrelated white noise (whn), images matching the second-order correlations of natural images (phs) and natural images including higher-order correlations (nat).
We find that groups of six nearby cortical neurons show little redundancy in their firing patterns (represented as binary vectors, 10ms bins) but rather act almost independently (mean multi-information 0.85 bits/s, range 0.16 - 1.90 bits/s, mean fraction of marginal entropy 0.34 , N=46). Although network correlations are weak, they are statistically significant. While relatively few groups showed significant redundancies under stimulation with white noise (67.4 ± 3.2; mean fraction of groups ± S.E.M.), many more did so in the other two conditions (phs: 95.7 ± 0.6; nat: 89.1 ± 1.4). Additional higher-order correlations in natural images compared to phase scrambled images did not increase but rather decrease the redundancy in the cortical representation: Network correlations are significantly higher in phs than in nat, as is the number of significantly correlated groups.
Multi-information measures the reduction in entropy due to any form of correlation. By using second order maximum entropy modeling, we find that a large fraction of multi-information is accounted for by pairwise correlations (whn: 75.0 ± 3.3; phs: 82.8 ± 2.1; nat: 80.8 ± 2.4; groups with significant redundancy). Importantly, stimulation with natural images containing higher-order correlations only lead to a slight increase in the fraction of redundancy due to higher-order correlations in the cortical representation (mean difference 2.26 , p=0.054, Sign test).
While our results suggest that population activity in V1 may be modeled well using pairwise correlations only, they leave roughly 20-25 of the multi-information unexplained. Therefore, choosing a particular form of higher-order interactions may improve model quality. Thus, in addition to the independent model, we evaluated the quality of three different models: (a) The second-order maximum entropy model, which minimizes higher-order correlations, (b) a model which assumes that correlations are a product of common inputs (Dichotomized Gaussian) and (c) a mixture model in which correlations are induced by a discrete number of latent states. We find that an independent model is sufficient for the white noise condition but neither for phs or nat. In contrast, all of the correlation models (a-c) perform similarly well for the conditions with correlated stimuli.
Our results suggest that under natural stimulation redundancies in cortical neurons are relatively weak. Higher-order correlations in natural images do not increase but rather decrease the redundancies in the cortical representation.