PLoS Biology (Mar 2022)

Complementary encoding of spatial information in hippocampal astrocytes

  • Sebastiano Curreli,
  • Jacopo Bonato,
  • Sara Romanzi,
  • Stefano Panzeri,
  • Tommaso Fellin

Journal volume & issue
Vol. 20, no. 3

Abstract

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Calcium dynamics into astrocytes influence the activity of nearby neuronal structures. However, because previous reports show that astrocytic calcium signals largely mirror neighboring neuronal activity, current information coding models neglect astrocytes. Using simultaneous two-photon calcium imaging of astrocytes and neurons in the hippocampus of mice navigating a virtual environment, we demonstrate that astrocytic calcium signals encode (i.e., statistically reflect) spatial information that could not be explained by visual cue information. Calcium events carrying spatial information occurred in topographically organized astrocytic subregions. Importantly, astrocytes encoded spatial information that was complementary and synergistic to that carried by neurons, improving spatial position decoding when astrocytic signals were considered alongside neuronal ones. These results suggest that the complementary place dependence of localized astrocytic calcium signals may regulate clusters of nearby synapses, enabling dynamic, context-dependent variations in population coding within brain circuits. A combination of functional imaging of astrocytes and neurons in the mouse hippocampus with information theory analysis shows that calcium dynamics in topographically-organized subcellular regions of astrocytes encode information about an animal’s position that is complementary and synergistic to that encoded in the spike output of surrounding neurons.