Astrocyte coverage of excitatory synapses correlates to measures of synapse structure and function in primary visual cortex

Abstract

Most excitatory synapses in the mammalian brain are contacted by astrocytes, forming the tripartite synapse. This interface is thought to be critical for glutamate turnover and structural or functional dynamics of synapses. While the degree of synaptic contact of astrocytes is known to vary across brain regions and animal species, the implications of this variability remain unknown. Furthermore, precisely how astrocyte coverage of synapses relates to in vivo functional properties of individual dendritic spines has yet to be investigated. Here, we characterized perisynaptic astrocyte processes (PAPs) contacting synapses of pyramidal neurons of the ferret visual cortex and, using correlative light and electron microscopy, examined their relationship to synaptic strength and to sensory-evoked Ca2+ activity. Nearly all synapses were contacted by PAPs, and most were contacted along the axon-spine interface (ASI). Structurally, we found that the degree of PAP coverage scaled with synapse size and complexity. Functionally, we found that PAP coverage scaled with the selectivity of Ca2+ responses of individual synapses to visual stimuli and, at least for the largest synapses, scaled with the reliability of visual stimuli to evoke postsynaptic Ca2+ events. Our study shows astrocyte coverage is highly correlated with structural properties of excitatory synapses in the visual cortex and implicates astrocytes as a contributor to reliable sensory activation.