Conservation of neuron-astrocyte coordinated activity among sensory processing centers of the developing brain

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Abstract

Afferent neurons in developing sensory organs exhibit a prolonged period of burst firing prior to the onset of sensory experience. This intrinsically generated activity propagates from the periphery through central processing centers to promote the survival and physiological maturation of neurons and refine their synaptic connectivity. Recent studies in the auditory system indicate that these bursts of action potentials also trigger metabotropic glutamate receptor-mediated calcium increases within astrocytes that are spatially and temporally correlated with neuronal events; however, it is not known if this phenomenon occurs in other sensory modalities. Here we show using in vivo simultaneous imaging of neuronal and astrocyte calcium activity in awake mouse pups that waves of retinal ganglion cell activity induce spatially and temporally correlated waves of astrocyte activity in the superior colliculus that depend on metabotropic glutamate receptors mGluR5 and mGluR3. Astrocyte calcium transients reliably occurred with each neuronal wave, but peaked more than one second after neuronal events. Despite differences in the temporal features of spontaneous activity in auditory and visual processing regions, individual astrocytes exhibited similar overall calcium activity patterns, providing a conserved mechanism to synchronize neuronal and astrocyte maturation within discrete sensory domains.

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  1. the amplitudes of neuronal and astrocyte calcium changes were highly correlated

    It looks like other waves features were correlated between neurons and astrocytes beyond amplitude, including duration. Was that indeed the case? May be other features to explore below as you look at correlations across brain regions.

  2. Astrocyte calcium waves from mice of this age exhibited similar properties, consisting of a continuous line of co-active astrocytes that propagated primarily in one direction, visible as diagonals in raster plots of cellular activity (Figure 1D; Movie S2).

    This is a great way to visualize the waves. I'm wondering how much gap junctions contribute mechanistically to wave propagation within the developing astrocyte networks.

  3. To determine whether coordinated activation of neurons and astrocytes is conserved in other sensory systems, we used in vivo widefield and two-photon imaging of genetically encoded calcium indicators selectively expressed in astrocytes and neurons to define activity patterns in the SC, a visual processing region of the midbrain that receives direct retinal input.

    Congrats on a beautiful, technologically impressive piece of work!