Encoding of spatial information in the calcium signals of hippocampal astrocytes during virtual navigation
Abstract: In the hippocampal formation, navigational information is encoded by neural place cells which modulate their
firing rate as a function of the animal’s location in the environment. Increasing evidence indicates that glial
networks are active elements in sensory information processing, but whether spatial information is encoded in
glial networks or exclusively encoded in neural circuits is currently unknown. Here we determined whether
astrocytes, the major class of non-neural cells in the brain, encode navigational information in their intracellular
calcium signals. To this aim, we trained head restrained mice to navigate in a virtual linear track and we
combined astrocyte-specific expression of genetically encoded calcium indicators with two-photon functional
imaging to capture subcellular calcium dynamics of hippocampal CA1 astrocytes during spatial navigation. We
observed that astrocytic calcium signals were significantly modulated by the animal’s spatial position in the
virtual track. Calcium events occurred in topologically restricted regions of the astrocyte, including the cell body
and the proximal processes, and these calcium signals clustered at preferred spatial locations within the virtual
track. Importantly, using a support vector machine decoder we found that astrocytic calcium signals could be
efficiently used to decode spatial information and to infer the animal’s spatial location. Altogether, these findings
indicate that astroglial networks encode navigational information, suggesting for the first time that the cellular
substrate of spatial cognition is composed of neuronal and glial circuital elements.
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