Abstract

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.

Highlights

  • Astrocytes, the most abundant class of glial cells in the brain, exhibit complex dynamics in intracellular calcium concentration [1]

  • To control for potential reactivity of astrocytes, we stained against the glial fibrillary acidic protein (GFAP) sections of fixed tissue from animals implanted with the chronic hippocampal window (S1 Fig)

  • We found similar GFAP immunoreactivity in the stratum Pyramidale and Radiatum in implanted hemispheres compared to controls (S1E and S1F Fig)

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Summary

Introduction

Astrocytes, the most abundant class of glial cells in the brain, exhibit complex dynamics in intracellular calcium concentration [1]. Previous reports suggest that astrocytic calcium signals triggered by external sensory stimuli largely mirror the activity of local neuronal cells [10,11] Such findings have led current models of sensory information coding in the brain to overlook the contribution of astrocytes, under the implicit or explicit assumption that astrocytic cells only provide information already encoded in neurons [13,14]. We challenged this assumption and tested the hypothesis that astrocytes encode information in their intracellular calcium dynamics that is not present in the activity of nearby neurons.

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