Differential receptive field organizations give rise to nearly identical neural correlations across three parallel sensory maps in weakly electric fish

Abstract

Understanding how neural populations encode sensory information thereby leading to perception and behavior (i.e., the neural code) remains an important problem in neuroscience. When investigating the neural code, one must take into account the fact that neural activities are not independent but are actually correlated with one another. Such correlations are seen ubiquitously and have a strong impact on neural coding. Here we investigated how differences in the antagonistic center-surround receptive field (RF) organization across three parallel sensory maps influence correlations between the activities of electrosensory pyramidal neurons. Using a model based on known anatomical differences in receptive field center size and overlap, we initially predicted large differences in correlated activity across the maps. However, in vivo electrophysiological recordings showed that, contrary to modeling predictions, electrosensory pyramidal neurons across all three segments displayed nearly identical correlations. To explain this surprising result, we incorporated the effects of RF surround in our model. By systematically varying both the RF surround gain and size relative to that of the RF center, we found that multiple RF structures gave rise to similar levels of correlation. In particular, incorporating known physiological differences in RF structure between the three maps in our model gave rise to similar levels of correlation. Our results show that RF center overlap alone does not determine correlations which has important implications for understanding how RF structure influences correlated neural activity.

Author summary

Growing evidence across nervous systems and species shows that the activities of neighboring neurons are not independent but are correlated with one another, which has important implications for neural coding. Such correlations are generally thought to be due to shared input. However, how this shared input is integrated by neurons in order to give rise to correlated activity is not well understood in general. Here we investigated how receptive field structure determines correlations between the activities of electrosensory pyramidal neurons in weakly electric fish. To do so, we used a combination of mathematical modeling of the known antagonistic center-surround RF structure as well as in vivo electrophysiological recordings. Our results show that the amount of receptive field center overlap alone is not sufficient to explain experimentally observed neural correlations in general. This is because our experimental data shows that pyramidal neurons with very different amounts of receptive field center overlap display almost identical correlations between their activities. Further, our modeling shows that both receptive field center and surround play important roles in determining correlated activity, such that very different combinations of relative RF surround strength and size can generate nearly identical correlations between neural activities. We discuss the implications of our results for sensory processing.