Dissociation Between Neuronal and Astrocytic Calcium Activity in Response to Locomotion in Mice

Locomotion triggers a coordinated response of both neurons and astrocytes in the brain. Here we performed calcium (Ca²⁺) imaging of these two cell types in the somatosensory cortex in head-fixed mice moving on the airlifted platform. Ca²⁺ activity in astrocytes significantly increased during locomotion from a low quiescence level. Ca²⁺ signals first appeared in the distal processes and then propagated to astrocytic somata, where it became significantly larger and exhibited oscillatory behaviour. Thus, astrocytic soma operates as both integrator and amplifier of Ca²⁺ signal. In neurons, Ca²⁺ activity was pronounced in quiescent periods and further increased during locomotion. Neuronal Ca²⁺ concentration ([Ca²⁺]_i) rose almost immediately following the onset of locomotion, whereas astrocytic Ca²⁺ signals lagged by several seconds. Such a long lag suggests that astrocytic [Ca²⁺]_i elevations are unlikely to be triggered by the activity of synapses among local neurons. Ca²⁺ responses to pairs of consecutive episodes of locomotion did not significantly differ in neurons, while were significantly diminished in response to the second locomotion in astrocytes. Such astrocytic refractoriness may arise from distinct mechanisms underlying Ca²⁺ signal generation. In neurons, the bulk of Ca²⁺ enters through the Ca²⁺ channels in the plasma membrane allowing for steady-level Ca²⁺ elevations in repetitive runs. Astrocytic Ca²⁺ responses originate from the intracellular stores, the depletion of which affects subsequent Ca²⁺ signals. Functionally, neuronal Ca²⁺ response reflects sensory input processed by neurons. Astrocytic Ca²⁺ dynamics is likely to provide metabolic and homeostatic support within the brain active milieu.