Conservation of Neuron-Astrocyte Correlated Activity in Developing Sensory Pathways

Neurons in developing sensory organs exhibit prolonged burst firing before the onset of sensory experience. This activity promotes neuronal survival and maturation in central sensory pathways. Within the auditory system, periodic bursts of synaptic glutamate release activate metabotropic glutamate receptors (mGluRs) on astrocytes, resulting in spatially and temporally correlated calcium transients; however, whether this phenomenon occurs in other sensory modalities is unknown. Using in vivo calcium imaging in the midbrain of awake mouse pups before eyelid opening, we show that retina wave-induced burst firing of visual afferents induces correlated waves of astrocyte activity in the superior colliculus (SC), a visual processing region. Glutamate sensor imaging revealed that each neuronal burst resulted in glutamate transients at astrocyte membranes in both developing sensory regions. Calcium transients in SC astrocytes resulted from activation of astrocytic mGluR5 and mGluR3, similar to astrocyte events in the nearby inferior colliculus (IC), which are induced by neuronal burst firing in the cochlea. Astrocyte calcium increased with each neuronal wave in the SC, but only the largest neuronal events triggered astrocyte responses in the IC. Astrocyte transcriptomic analysis suggested differential expression of mGluR3 and mGluR5 between these sensory regions, in accordance with the greater dependence on mGluR5 in IC astrocytes. Despite differences in receptor contribution and temporal features of activity, astrocytes in these different regions exhibited similar overall calcium activity. Thus, neuronal burst firing in developing sensory organs provides a conserved mechanism to synchronize neuronal and astrocyte activity in the brain at a critical stage of development.