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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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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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.</description><identifier>ISSN: 1422-0067</identifier><identifier>ISSN: 1661-6596</identifier><identifier>EISSN: 1422-0067</identifier><identifier>DOI: 10.3390/ijms21176101</identifier><identifier>PMID: 32847128</identifier><language>eng</language><publisher>BASEL: Mdpi</publisher><subject>Action potential ; Action Potentials - physiology ; Age Factors ; Age groups ; Animals ; axon initial segment (AIS) ; Axon Initial Segment - physiology ; Biochemistry & Molecular Biology ; Cell Differentiation ; Cell growth ; Cell size ; Cells, Cultured ; Chemistry ; Chemistry, Multidisciplinary ; development ; Elongation ; Growth - physiology ; Life Sciences & Biomedicine ; Maturation ; Models, Neurological ; Morphology ; motor cortex ; Motor Cortex - cytology ; Motor Cortex - growth & development ; Motor Cortex - physiology ; motor neurons ; Motor Neurons - physiology ; Neurogenesis - physiology ; Neuronal Plasticity ; Neurons ; patch clamp ; Physical Sciences ; Physiology ; Plastic properties ; Pyramidal cells ; Rats ; Science & Technology ; Somatosensory cortex ; Structure-function relationships</subject><ispartof>International journal of molecular sciences, 2020-08, Vol.21 (17), p.6101, Article 6101</ispartof><rights>2020. This work is licensed under http://creativecommons.org/licenses/by/3.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2020 by the authors. 2020</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>true</woscitedreferencessubscribed><woscitedreferencescount>4</woscitedreferencescount><woscitedreferencesoriginalsourcerecordid>wos000570181300001</woscitedreferencesoriginalsourcerecordid><citedby>FETCH-LOGICAL-c478t-2a0ef3ae449074acf652e7106478315b0a92f89b56ab4821fdec9dee7145ddf03</citedby><cites>FETCH-LOGICAL-c478t-2a0ef3ae449074acf652e7106478315b0a92f89b56ab4821fdec9dee7145ddf03</cites><orcidid>0000-0001-8020-6604 ; 0000-0002-4286-5067 ; 0000-0002-8486-6412</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC7503395/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC7503395/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,315,728,781,785,886,27929,27930,28253,53796,53798</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/32847128$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Benedetti, Bruno</creatorcontrib><creatorcontrib>Dannehl, Dominik</creatorcontrib><creatorcontrib>Janssen, Jan Maximilian</creatorcontrib><creatorcontrib>Corcelli, Corinna</creatorcontrib><creatorcontrib>Couillard-Despres, Sebastien</creatorcontrib><creatorcontrib>Engelhardt, Maren</creatorcontrib><title>Structural and Functional Maturation of Rat Primary Motor Cortex Layer V Neurons</title><title>International journal of molecular sciences</title><addtitle>INT J MOL SCI</addtitle><addtitle>Int J Mol Sci</addtitle><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.</description><subject>Action potential</subject><subject>Action Potentials - physiology</subject><subject>Age Factors</subject><subject>Age groups</subject><subject>Animals</subject><subject>axon initial segment (AIS)</subject><subject>Axon Initial Segment - physiology</subject><subject>Biochemistry & Molecular Biology</subject><subject>Cell Differentiation</subject><subject>Cell growth</subject><subject>Cell size</subject><subject>Cells, Cultured</subject><subject>Chemistry</subject><subject>Chemistry, Multidisciplinary</subject><subject>development</subject><subject>Elongation</subject><subject>Growth - physiology</subject><subject>Life Sciences & Biomedicine</subject><subject>Maturation</subject><subject>Models, Neurological</subject><subject>Morphology</subject><subject>motor cortex</subject><subject>Motor Cortex - cytology</subject><subject>Motor Cortex - growth & development</subject><subject>Motor Cortex - physiology</subject><subject>motor neurons</subject><subject>Motor Neurons - physiology</subject><subject>Neurogenesis - physiology</subject><subject>Neuronal Plasticity</subject><subject>Neurons</subject><subject>patch clamp</subject><subject>Physical Sciences</subject><subject>Physiology</subject><subject>Plastic properties</subject><subject>Pyramidal cells</subject><subject>Rats</subject><subject>Science & Technology</subject><subject>Somatosensory cortex</subject><subject>Structure-function relationships</subject><issn>1422-0067</issn><issn>1661-6596</issn><issn>1422-0067</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>AOWDO</sourceid><sourceid>EIF</sourceid><sourceid>8G5</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>GUQSH</sourceid><sourceid>M2O</sourceid><sourceid>DOA</sourceid><recordid>eNqNkU1v1DAQhiMEoqVw44wicUGChfFX7FyQUESh0hYqvq6W44xLVtm42A7Qf4-zKastJ04ezzzzejxvUTwm8JKxGl71m22khMiKALlTHBNO6QqgkncP4qPiQYwbAMqoqO8XR4wqLglVx8XF5xQmm6ZghtKMXXk6jTb1fszXczOn50vpXfnJpPIi9FsTrstzn3woGx8S_i7X5hpD-a38gFPwY3xY3HNmiPjo5jwpvp6-_dK8X60_vjtr3qxXlkuVVtQAOmaQ8xokN9ZVgqIkUOUqI6IFU1On6lZUpuWKEtehrTvMCBdd54CdFGeLbufNRl8tk2lver1L-HCpTUi9HVAb5TqJrq1oxzkHWwvkTlBA2hEjXJW1Xi9aV1O7xc7imPI-boneroz9d33pf2opIHsgssCzG4Hgf0wYk9720eIwmBH9FDXlTCrBaD2_9fQfdOOnkPe9oxTjkquZerFQNvgYA7r9MAT0bLs-tD3jTw4_sIf_-pwBtQC_sPUu2h5Hi3sMAIQEogjLEZCmTzvbGz-NKbc-__9W9geMJ8mI</recordid><startdate>20200824</startdate><enddate>20200824</enddate><creator>Benedetti, Bruno</creator><creator>Dannehl, Dominik</creator><creator>Janssen, Jan Maximilian</creator><creator>Corcelli, Corinna</creator><creator>Couillard-Despres, Sebastien</creator><creator>Engelhardt, Maren</creator><general>Mdpi</general><general>MDPI AG</general><general>MDPI</general><scope>AOWDO</scope><scope>BLEPL</scope><scope>DTL</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>3V.</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>8G5</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BENPR</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>GUQSH</scope><scope>K9.</scope><scope>M0S</scope><scope>M1P</scope><scope>M2O</scope><scope>MBDVC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>Q9U</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0001-8020-6604</orcidid><orcidid>https://orcid.org/0000-0002-4286-5067</orcidid><orcidid>https://orcid.org/0000-0002-8486-6412</orcidid></search><sort><creationdate>20200824</creationdate><title>Structural and Functional Maturation of Rat Primary Motor Cortex Layer V Neurons</title><author>Benedetti, Bruno ; Dannehl, Dominik ; Janssen, Jan Maximilian ; Corcelli, Corinna ; Couillard-Despres, Sebastien ; Engelhardt, Maren</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c478t-2a0ef3ae449074acf652e7106478315b0a92f89b56ab4821fdec9dee7145ddf03</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Action potential</topic><topic>Action Potentials - physiology</topic><topic>Age Factors</topic><topic>Age groups</topic><topic>Animals</topic><topic>axon initial segment (AIS)</topic><topic>Axon Initial Segment - physiology</topic><topic>Biochemistry & Molecular Biology</topic><topic>Cell Differentiation</topic><topic>Cell growth</topic><topic>Cell size</topic><topic>Cells, Cultured</topic><topic>Chemistry</topic><topic>Chemistry, Multidisciplinary</topic><topic>development</topic><topic>Elongation</topic><topic>Growth - physiology</topic><topic>Life Sciences & Biomedicine</topic><topic>Maturation</topic><topic>Models, Neurological</topic><topic>Morphology</topic><topic>motor cortex</topic><topic>Motor Cortex - cytology</topic><topic>Motor Cortex - growth & development</topic><topic>Motor Cortex - physiology</topic><topic>motor neurons</topic><topic>Motor Neurons - physiology</topic><topic>Neurogenesis - physiology</topic><topic>Neuronal Plasticity</topic><topic>Neurons</topic><topic>patch clamp</topic><topic>Physical Sciences</topic><topic>Physiology</topic><topic>Plastic properties</topic><topic>Pyramidal cells</topic><topic>Rats</topic><topic>Science & Technology</topic><topic>Somatosensory cortex</topic><topic>Structure-function relationships</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Benedetti, Bruno</creatorcontrib><creatorcontrib>Dannehl, Dominik</creatorcontrib><creatorcontrib>Janssen, Jan Maximilian</creatorcontrib><creatorcontrib>Corcelli, Corinna</creatorcontrib><creatorcontrib>Couillard-Despres, Sebastien</creatorcontrib><creatorcontrib>Engelhardt, Maren</creatorcontrib><collection>Web of Science - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>International journal of molecular sciences</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Benedetti, Bruno</au><au>Dannehl, Dominik</au><au>Janssen, Jan Maximilian</au><au>Corcelli, Corinna</au><au>Couillard-Despres, Sebastien</au><au>Engelhardt, Maren</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Structural and Functional Maturation of Rat Primary Motor Cortex Layer V Neurons</atitle><jtitle>International journal of molecular sciences</jtitle><stitle>INT J MOL SCI</stitle><addtitle>Int J Mol Sci</addtitle><date>2020-08-24</date><risdate>2020</risdate><volume>21</volume><issue>17</issue><spage>6101</spage><pages>6101-</pages><artnum>6101</artnum><issn>1422-0067</issn><issn>1661-6596</issn><eissn>1422-0067</eissn><abstract>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.</abstract><cop>BASEL</cop><pub>Mdpi</pub><pmid>32847128</pmid><doi>10.3390/ijms21176101</doi><tpages>15</tpages><orcidid>https://orcid.org/0000-0001-8020-6604</orcidid><orcidid>https://orcid.org/0000-0002-4286-5067</orcidid><orcidid>https://orcid.org/0000-0002-8486-6412</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Action potential Action Potentials - physiology Age Factors Age groups Animals axon initial segment (AIS) Axon Initial Segment - physiology Biochemistry & Molecular Biology Cell Differentiation Cell growth Cell size Cells, Cultured Chemistry Chemistry, Multidisciplinary development Elongation Growth - physiology Life Sciences & Biomedicine Maturation Models, Neurological Morphology motor cortex Motor Cortex - cytology Motor Cortex - growth & development Motor Cortex - physiology motor neurons Motor Neurons - physiology Neurogenesis - physiology Neuronal Plasticity Neurons patch clamp Physical Sciences Physiology Plastic properties Pyramidal cells Rats Science & Technology Somatosensory cortex Structure-function relationships |
title | Structural and Functional Maturation of Rat Primary Motor Cortex Layer V Neurons |
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