Astrocytes modulate place cells properties in the mouse hippocampus during virtual navigation

Spatial navigation is fundamental for animal survival. Seminal work in the hippocampal formation identified key neural correlates of spatial navigation, the place cells. These cells encode information about the animal position through the spatial modulation of their firing rate. However, the involvement of glia in the regulation of place cells has not been investigated so far. Recent evidence demonstrated that, in the CA1 hippocampal regions, astrocytic calcium signals encode information about the animal’s position and that information encoded into astrocytes is complementary to that encoded in the activity of nearby neurons. Since, previous work demonstrated a role of astrocytic calcium signals in the modulation of neuronal activity, I here tested the hypothesis that perturbation of astrocytic calcium signalling in the hippocampus during spatial navigation alters the neuronal representation of spatial information. To this aim, I manipulated astrocytic calcium dynamics via activation of Gq-coupled DREADDs while performing two-photon (2P) functional imaging of GCaMP6f expressing CA1 hippocampal neurons in head-fixed mice traversing a virtual linear track. Using an information theoretical approach, we observed that DREADD activation by CNO significantly decreased mutual information about the animal’s position encoded in neuronal place cells. Moreover, we observed increased width of place fields of CA1 place cells upon CNO injection. The fraction of neuronal place cells and the spatial behaviour of the animals were, instead, not significantly affected by the manipulation of astrocytic calcium signalling. These results show that perturbation of astrocytic calcium dynamics decreases the precision with which spatial information is encoded in neuronal place cells by lowering the amount of encoded spatial information and enlarging the place field width. Complementary spatial information encoded in astrocyte calcium dynamics may promote the emergence of dynamic, context-dependent changes in spatial information population coding of CA1 neurons.