A Distributed Neural Code in the Dentate Gyrus and in CA1

Neuron. 2020 Jun 4;S0896-6273(20)30391-3. doi: 10.1016/j.neuron.2020.05.022. Online ahead of print.

Abstract

Neurons are often considered specialized functional units that encode a single variable. However, many neurons are observed to respond to a mix of disparate sensory, cognitive, and behavioral variables. For such representations, information is distributed across multiple neurons. Here we find this distributed code in the dentate gyrus and CA1 subregions of the hippocampus. Using calcium imaging in freely moving mice, we decoded an animal's position, direction of motion, and speed from the activity of hundreds of cells. The response properties of individual neurons were only partially predictive of their importance for encoding position. Non-place cells encoded position and contributed to position encoding when combined with other cells. Indeed, disrupting the correlations between neural activities decreased decoding performance, mostly in CA1. Our analysis indicates that population methods rather than classical analyses based on single-cell response properties may more accurately characterize the neural code in the hippocampus.

Keywords: calcium imaging; correlated activity; decoding; dentate gyrus; distributed representations; hippocampus; mixed selectivity; place cells; population coding.