Postsynaptic mitochondria are positioned to support functional diversity of dendritic spines

Postsynaptic mitochondria are critical for 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 den...

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Main Authors: Connon I Thomas, Melissa A Ryan, Naomi Kamasawa, Benjamin Scholl
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2023-12-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/89682
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author Connon I Thomas
Melissa A Ryan
Naomi Kamasawa
Benjamin Scholl
author_facet Connon I Thomas
Melissa A Ryan
Naomi Kamasawa
Benjamin Scholl
author_sort Connon I Thomas
collection DOAJ
description Postsynaptic mitochondria are critical for 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 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.
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spelling doaj.art-5e51dd1cd47c477a9e36e813ebb9743f2023-12-07T14:03:19ZengeLife Sciences Publications LtdeLife2050-084X2023-12-011210.7554/eLife.89682Postsynaptic mitochondria are positioned to support functional diversity of dendritic spinesConnon I Thomas0https://orcid.org/0000-0003-0995-9667Melissa A Ryan1https://orcid.org/0000-0002-0468-9525Naomi Kamasawa2https://orcid.org/0000-0002-8926-5309Benjamin Scholl3https://orcid.org/0000-0002-9578-7234Electron Microscopy Core Facility, Max Planck Florida Institute for Neuroscience, Max Planck Way, Jupiter, United StatesElectron Microscopy Core Facility, Max Planck Florida Institute for Neuroscience, Max Planck Way, Jupiter, United StatesElectron Microscopy Core Facility, Max Planck Florida Institute for Neuroscience, Max Planck Way, Jupiter, United StatesDepartment of Neuroscience, Perelman School of Medicine at the University of Pennsylvania, Philadelphia, United StatesPostsynaptic mitochondria are critical for 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 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.https://elifesciences.org/articles/89682Mustela furoelectron microscopytwo-photon calcium imagingdendrite spinemitochondria
spellingShingle Connon I Thomas
Melissa A Ryan
Naomi Kamasawa
Benjamin Scholl
Postsynaptic mitochondria are positioned to support functional diversity of dendritic spines
eLife
Mustela furo
electron microscopy
two-photon calcium imaging
dendrite spine
mitochondria
title Postsynaptic mitochondria are positioned to support functional diversity of dendritic spines
title_full Postsynaptic mitochondria are positioned to support functional diversity of dendritic spines
title_fullStr Postsynaptic mitochondria are positioned to support functional diversity of dendritic spines
title_full_unstemmed Postsynaptic mitochondria are positioned to support functional diversity of dendritic spines
title_short Postsynaptic mitochondria are positioned to support functional diversity of dendritic spines
title_sort postsynaptic mitochondria are positioned to support functional diversity of dendritic spines
topic Mustela furo
electron microscopy
two-photon calcium imaging
dendrite spine
mitochondria
url https://elifesciences.org/articles/89682
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AT naomikamasawa postsynapticmitochondriaarepositionedtosupportfunctionaldiversityofdendriticspines
AT benjaminscholl postsynapticmitochondriaarepositionedtosupportfunctionaldiversityofdendriticspines