Randomly connected networks generate emergent selectivity and predict decoding properties of large populations of neurons

Abstract

Advances in neural recording methods enable sampling from populations of thousands of neurons during the performance of behavioral tasks, raising the question of how recorded activity relates to the theoretical models of computations underlying performance. In the context of decision making in rodents, patterns of functional connectivity between choice-selective cortical neurons, as well as broadly distributed choice information in both excitatory and inhibitory populations, were recently reported [1]. The straightforward interpretation of these data suggests a mechanism relying on specific patterns of anatomical connectivity to achieve selective pools of inhibitory as well as excitatory neurons. We investigate an alternative mechanism for the emergence of these experimental observations using a computational approach. We find that a randomly connected network of excitatory and inhibitory neurons generates single-cell selectivity, patterns of pairwise correlations, and indistinguishable excitatory and inhibitory readout weight distributions, as observed in recorded neural populations. Further, we make the readily verifiable experimental predictions that, for this type of evidence accumulation task, there are no anatomically defined sub-populations of neurons representing choice, and that choice preference of a particular neuron changes with the details of the task. This work suggests that distributed stimulus selectivity and patterns of functional organization in population codes could be emergent properties of randomly connected networks.\n\nAuthor summaryWhat can we learn about neural circuit organization and function from recordings of large populations of neurons? For example, in population recordings in the posterior parietal cortex of mice performing an evidence integration task, particular patterns of selectivity and correlations between cells were observed. One hypothesis for an underlying mechanism generating these patterns is that they follow from intricate rules of connectivity between specific neurons, but this raises the question of how such intricate patterns arise during learning or development. An alternative hypothesis, which we explore here, is that such patterns emerge from networks with broad spectra of eigenvalues, which is a generic property of certain random networks. We find that a random network model matches many features of experimental recordings, from single cells to populations. We suggest that such emergent selectivity could be an important principle in brain areas, in which a broad distribution of selectivity is observed.