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Structural and Functional Maturation of Rat Primary Motor Cortex Layer V Neurons

Rodent neocortical neurons undergo prominent postnatal development and maturation. The process is associated with structural and functional maturation of the axon initial segment (AIS), the site of action potential initiation. In this regard, cell size and optimal AIS length are interconnected. In s...

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Autores principales: Benedetti, Bruno, Dannehl, Dominik, Janssen, Jan Maximilian, Corcelli, Corinna, Couillard-Després, Sébastien, Engelhardt, Maren
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7503395/
https://www.ncbi.nlm.nih.gov/pubmed/32847128
http://dx.doi.org/10.3390/ijms21176101
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author Benedetti, Bruno
Dannehl, Dominik
Janssen, Jan Maximilian
Corcelli, Corinna
Couillard-Després, Sébastien
Engelhardt, Maren
author_facet Benedetti, Bruno
Dannehl, Dominik
Janssen, Jan Maximilian
Corcelli, Corinna
Couillard-Després, Sébastien
Engelhardt, Maren
author_sort Benedetti, Bruno
collection PubMed
description Rodent neocortical neurons undergo prominent postnatal development and maturation. The process is associated with structural and functional maturation of the axon initial segment (AIS), the site of action potential initiation. In this regard, cell size and optimal AIS length are interconnected. In sensory cortices, developmental onset of sensory input and consequent changes in network activity cause phasic AIS plasticity that can also control functional output. In non-sensory cortices, network input driving phasic events should be less prominent. We, therefore, explored the relationship between postnatal functional maturation and AIS maturation in principal neurons of the primary motor cortex layer V (M1LV), a non-sensory area of the rat brain. We hypothesized that a rather continuous process of AIS maturation and elongation would reflect cell growth, accompanied by progressive refinement of functional output properties. We found that, in the first two postnatal weeks, cell growth prompted substantial decline of neuronal input resistance, such that older neurons needed larger input current to reach rheobase and fire action potentials. In the same period, we observed the most prominent AIS elongation and significant maturation of functional output properties. Alternating phases of AIS plasticity did not occur, and changes in functional output properties were largely justified by AIS elongation. From the third postnatal week up to five months of age, cell growth, AIS elongation, and functional output maturation were marginal. Thus, AIS maturation in M1LV is a continuous process that attunes the functional output of pyramidal neurons and associates with early postnatal development to counterbalance increasing electrical leakage due to cell growth.
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spelling pubmed-75033952020-09-23 Structural and Functional Maturation of Rat Primary Motor Cortex Layer V Neurons Benedetti, Bruno Dannehl, Dominik Janssen, Jan Maximilian Corcelli, Corinna Couillard-Després, Sébastien Engelhardt, Maren Int J Mol Sci Article Rodent neocortical neurons undergo prominent postnatal development and maturation. The process is associated with structural and functional maturation of the axon initial segment (AIS), the site of action potential initiation. In this regard, cell size and optimal AIS length are interconnected. In sensory cortices, developmental onset of sensory input and consequent changes in network activity cause phasic AIS plasticity that can also control functional output. In non-sensory cortices, network input driving phasic events should be less prominent. We, therefore, explored the relationship between postnatal functional maturation and AIS maturation in principal neurons of the primary motor cortex layer V (M1LV), a non-sensory area of the rat brain. We hypothesized that a rather continuous process of AIS maturation and elongation would reflect cell growth, accompanied by progressive refinement of functional output properties. We found that, in the first two postnatal weeks, cell growth prompted substantial decline of neuronal input resistance, such that older neurons needed larger input current to reach rheobase and fire action potentials. In the same period, we observed the most prominent AIS elongation and significant maturation of functional output properties. Alternating phases of AIS plasticity did not occur, and changes in functional output properties were largely justified by AIS elongation. From the third postnatal week up to five months of age, cell growth, AIS elongation, and functional output maturation were marginal. Thus, AIS maturation in M1LV is a continuous process that attunes the functional output of pyramidal neurons and associates with early postnatal development to counterbalance increasing electrical leakage due to cell growth. MDPI 2020-08-24 /pmc/articles/PMC7503395/ /pubmed/32847128 http://dx.doi.org/10.3390/ijms21176101 Text en © 2020 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Benedetti, Bruno
Dannehl, Dominik
Janssen, Jan Maximilian
Corcelli, Corinna
Couillard-Després, Sébastien
Engelhardt, Maren
Structural and Functional Maturation of Rat Primary Motor Cortex Layer V Neurons
title Structural and Functional Maturation of Rat Primary Motor Cortex Layer V Neurons
title_full Structural and Functional Maturation of Rat Primary Motor Cortex Layer V Neurons
title_fullStr Structural and Functional Maturation of Rat Primary Motor Cortex Layer V Neurons
title_full_unstemmed Structural and Functional Maturation of Rat Primary Motor Cortex Layer V Neurons
title_short Structural and Functional Maturation of Rat Primary Motor Cortex Layer V Neurons
title_sort structural and functional maturation of rat primary motor cortex layer v neurons
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7503395/
https://www.ncbi.nlm.nih.gov/pubmed/32847128
http://dx.doi.org/10.3390/ijms21176101
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