Postsynaptic mitochondria are positioned to support functional diversity of dendritic spines

Abstract

Postsynaptic mitochondria are critical to the development, plasticity, and maintenance of synaptic inputs. However, their relationship to synaptic structure and functional activity is unknown. We examined a correlative dataset from ferret visual cortex with in vivo two-photon calcium imaging of dendritic spines during visual stimulation and electron microscopy (EM) reconstructions of spine ultrastructure, investigating mitochondrial abundance near functionally- and structurally-characterized spines. Surprisingly, we found no correlation to structural measures of synaptic strength. Instead, we found that mitochondria are positioned near spines with orientation preferences that are dissimilar to the somatic preference. Additionally, we found that mitochondria are positioned near groups of spines with heterogeneous orientation preferences. For a subset of spines with a mitochondrion in the head or neck, synapses were larger and exhibited greater selectivity to visual stimuli than those without a mitochondrion. Our data suggest mitochondria are not necessarily positioned to support the energy needs of strong spines, but rather support the structurally and functionally diverse inputs innervating the basal dendrites of cortical neurons.

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

“…Information on animals, survival viral injections, cranial window implantation are described in depth in our previous studies (Scholl et al, 2017(Scholl et al, , 2019(Scholl et al, , 2021Thomas et al, 2023). Briefly, layer 2/3 neurons of the primary visual cortex of female ferrets (n = 3, Marshall Farms) were driven to express the Ca 2+ indicator GCaMP6s via a Cre-dependent AAV expression system.…”

“…Although a great number of spines are co-tuned with the somatic output (Scholl et al, 2021), there is considerable diversity in orientation preference across the population of spines on a neuron (Scholl and Fitzpatrick, 2020). We previously found that dendritic mitochondria tend to be located near spines that are more diverse in their preferences, suggesting enhanced energetic support (Thomas et al, 2023). This inspired us to consider whether differentially-tuned spines require more astrocytic support.…”