The Statistical Structure of the Hippocampal Code for Space as a Function of Time, Context, and Value

Cell. 2020 Oct 29;183(3):620-635.e22. doi: 10.1016/j.cell.2020.09.024. Epub 2020 Oct 8.

Abstract

Hippocampal activity represents many behaviorally important variables, including context, an animal's location within a given environmental context, time, and reward. Using longitudinal calcium imaging in mice, multiple large virtual environments, and differing reward contingencies, we derived a unified probabilistic model of CA1 representations centered on a single feature-the field propensity. Each cell's propensity governs how many place fields it has per unit space, predicts its reward-related activity, and is preserved across distinct environments and over months. Propensity is broadly distributed-with many low, and some very high, propensity cells-and thus strongly shapes hippocampal representations. This results in a range of spatial codes, from sparse to dense. Propensity varied ∼10-fold between adjacent cells in salt-and-pepper fashion, indicating substantial functional differences within a presumed cell type. Intracellular recordings linked propensity to cell excitability. The stability of each cell's propensity across conditions suggests this fundamental property has anatomical, transcriptional, and/or developmental origins.

Keywords: calcium imaging; excitability; gain modulation; hippocampus; intracellular recording; memory; place cell; place field; propensity; sparse coding.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Behavior, Animal / physiology
  • Biophysical Phenomena
  • Calcium / metabolism
  • Hippocampus / anatomy & histology*
  • Hippocampus / physiology*
  • Male
  • Mice, Inbred C57BL
  • Models, Neurological
  • Pyramidal Cells / physiology
  • Reward
  • Task Performance and Analysis
  • Time Factors

Substances

  • Calcium