Slow-wave activity in the S1HL cortex Is contributed by different layer-specific field potential sources during development

Spontaneous correlated activity in cortical columns is critical for postnatal circuit refinement. We used spatial discrimination techniques to explore the late maturation of synaptic pathways through the laminar distribution of the field potential (FP) generators underlying spontaneous and evoked ac...

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Autores: Ortuño, Tania, López-Madrona, Víctor J., Makarova, Julia, Tapia-González, Silvia, Muñoz, Alberto, DeFelipe, Javier, Herreras, Óscar
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2019
País:España
Institución:Consejo Superior de Investigaciones Científicas (CSIC)
Repositorio:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:digital.csic.es:10261/206414
Acceso en línea:http://hdl.handle.net/10261/206414
Access Level:acceso abierto
Palabra clave:Cortex
Development
Field potential
Laminar activity
Somatosensory hindlimb cortex
Spatial discrimination
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repository_id_str
dc.title.none.fl_str_mv Slow-wave activity in the S1HL cortex Is contributed by different layer-specific field potential sources during development
title Slow-wave activity in the S1HL cortex Is contributed by different layer-specific field potential sources during development
spellingShingle Slow-wave activity in the S1HL cortex Is contributed by different layer-specific field potential sources during development
Ortuño, Tania
Cortex
Development
Field potential
Laminar activity
Somatosensory hindlimb cortex
Spatial discrimination
title_short Slow-wave activity in the S1HL cortex Is contributed by different layer-specific field potential sources during development
title_full Slow-wave activity in the S1HL cortex Is contributed by different layer-specific field potential sources during development
title_fullStr Slow-wave activity in the S1HL cortex Is contributed by different layer-specific field potential sources during development
title_full_unstemmed Slow-wave activity in the S1HL cortex Is contributed by different layer-specific field potential sources during development
title_sort Slow-wave activity in the S1HL cortex Is contributed by different layer-specific field potential sources during development
dc.creator.none.fl_str_mv Ortuño, Tania
López-Madrona, Víctor J.
Makarova, Julia
Tapia-González, Silvia
Muñoz, Alberto
DeFelipe, Javier
Herreras, Óscar
author Ortuño, Tania
author_facet Ortuño, Tania
López-Madrona, Víctor J.
Makarova, Julia
Tapia-González, Silvia
Muñoz, Alberto
DeFelipe, Javier
Herreras, Óscar
author_role author
author2 López-Madrona, Víctor J.
Makarova, Julia
Tapia-González, Silvia
Muñoz, Alberto
DeFelipe, Javier
Herreras, Óscar
author2_role author
author
author
author
author
author
dc.contributor.none.fl_str_mv Ministerio de Economía y Competitividad (España)
Ministerio de Ciencia, Innovación y Universidades (España)
Cajal Blue Brain
European Commission
Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]
dc.subject.none.fl_str_mv Cortex
Development
Field potential
Laminar activity
Somatosensory hindlimb cortex
Spatial discrimination
topic Cortex
Development
Field potential
Laminar activity
Somatosensory hindlimb cortex
Spatial discrimination
description Spontaneous correlated activity in cortical columns is critical for postnatal circuit refinement. We used spatial discrimination techniques to explore the late maturation of synaptic pathways through the laminar distribution of the field potential (FP) generators underlying spontaneous and evoked activities of the S1HL cortex in juvenile (P14-P16) and adult anesthetized rats. Juveniles exhibit an intermittent FP pattern resembling Up/Down states in adults, but with much reduced power and different laminar distribution. Whereas FPs in active periods are dominated by a layer VI generator in juveniles, in adults a developing multipart generator takes over, displaying current sinks in middle layers (III-V). The blockade of excitatory transmission in upper and middle layers of adults recovered the juvenile-like FP profiles. In addition to the layer VI generator, a gamma-specific generator in supragranular layers was the same in both age groups. While searching for dynamical coupling among generators in juveniles we found significant cross-correlation in ∼one-half of the tested pairs, whereas excessive coherence hindered their efficient separation in adults. Also, potentials evoked by tactile and electrical stimuli showed different short-latency dipoles between the two age groups, and the juveniles lacked the characteristic long latency UP state currents in middle layers. In addition, the mean firing rate of neurons was lower in juveniles. Thus, cortical FPs originate from different intra-columnar segments as they become active postnatally. We suggest that although some cortical segments are active early postnatally, a functional sensory-motor control relies on a delayed maturation and network integration of synaptic connections in middle layers.SIGNIFICANCE STATEMENT Early postnatal activity in the rodent cortex is mostly endogenous, whereas it becomes driven by peripheral input at later stages. The precise schedule for the maturation of synaptic pathways is largely unknown. We explored this in the somatosensory hindlimb cortex at an age when animals begin to use their limbs by uncovering the laminar distribution of the field potential generators underlying the dominant delta waves in juveniles and adults. Our results suggest that field potentials are mostly generated by a pathway in deep layers, whereas other pathways mature later in middle layers and take over in adults. We suggest that a functional sensory-motor control relies on a delayed maturation and network integration of synaptic connections in middle layers.
publishDate 2019
dc.date.none.fl_str_mv 2019
2020
2020
2020
dc.type.none.fl_str_mv info:eu-repo/semantics/article
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dc.identifier.none.fl_str_mv http://hdl.handle.net/10261/206414
url http://hdl.handle.net/10261/206414
dc.language.none.fl_str_mv Inglés
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dc.publisher.none.fl_str_mv Society for Neuroscience
publisher.none.fl_str_mv Society for Neuroscience
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spelling Slow-wave activity in the S1HL cortex Is contributed by different layer-specific field potential sources during developmentOrtuño, TaniaLópez-Madrona, Víctor J.Makarova, JuliaTapia-González, SilviaMuñoz, AlbertoDeFelipe, JavierHerreras, ÓscarCortexDevelopmentField potentialLaminar activitySomatosensory hindlimb cortexSpatial discriminationSpontaneous correlated activity in cortical columns is critical for postnatal circuit refinement. We used spatial discrimination techniques to explore the late maturation of synaptic pathways through the laminar distribution of the field potential (FP) generators underlying spontaneous and evoked activities of the S1HL cortex in juvenile (P14-P16) and adult anesthetized rats. Juveniles exhibit an intermittent FP pattern resembling Up/Down states in adults, but with much reduced power and different laminar distribution. Whereas FPs in active periods are dominated by a layer VI generator in juveniles, in adults a developing multipart generator takes over, displaying current sinks in middle layers (III-V). The blockade of excitatory transmission in upper and middle layers of adults recovered the juvenile-like FP profiles. In addition to the layer VI generator, a gamma-specific generator in supragranular layers was the same in both age groups. While searching for dynamical coupling among generators in juveniles we found significant cross-correlation in ∼one-half of the tested pairs, whereas excessive coherence hindered their efficient separation in adults. Also, potentials evoked by tactile and electrical stimuli showed different short-latency dipoles between the two age groups, and the juveniles lacked the characteristic long latency UP state currents in middle layers. In addition, the mean firing rate of neurons was lower in juveniles. Thus, cortical FPs originate from different intra-columnar segments as they become active postnatally. We suggest that although some cortical segments are active early postnatally, a functional sensory-motor control relies on a delayed maturation and network integration of synaptic connections in middle layers.SIGNIFICANCE STATEMENT Early postnatal activity in the rodent cortex is mostly endogenous, whereas it becomes driven by peripheral input at later stages. The precise schedule for the maturation of synaptic pathways is largely unknown. We explored this in the somatosensory hindlimb cortex at an age when animals begin to use their limbs by uncovering the laminar distribution of the field potential generators underlying the dominant delta waves in juveniles and adults. Our results suggest that field potentials are mostly generated by a pathway in deep layers, whereas other pathways mature later in middle layers and take over in adults. We suggest that a functional sensory-motor control relies on a delayed maturation and network integration of synaptic connections in middle layers.This work was supported by the Spanish Ministries of (1) Economy and Competitiveness (Grants BFU2013-41533R and SAF2016-80100-R to O.H.); (2) Science, Innovation, and Universities (Grant SAF 2015-66603-P and the Cajal Blue Brain Project (C080020-09; the Spanish partner of the Blue Brain Project initiative from EPFL, Switzerland)], and the European Union's Horizon 2020 Research and Innovation Program under Grant 785907 (Human Brain Project, SGA2) to J.D.F.Society for NeuroscienceMinisterio de Economía y Competitividad (España)Ministerio de Ciencia, Innovación y Universidades (España)Cajal Blue BrainEuropean CommissionConsejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]2020202020192020info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Publisher's versioninfo:eu-repo/semantics/publishedVersionhttp://hdl.handle.net/10261/206414reponame:DIGITAL.CSIC. Repositorio Institucional del CSICinstname:Consejo Superior de Investigaciones Científicas (CSIC)Inglés#PLACEHOLDER_PARENT_METADATA_VALUE##PLACEHOLDER_PARENT_METADATA_VALUE##PLACEHOLDER_PARENT_METADATA_VALUE##PLACEHOLDER_PARENT_METADATA_VALUE#info:eu-repo/grantAgreement/MINECO/Plan Estatal de Investigación Científica y Técnica y de Innovación 2013-2016/BFU2013-41533-Rinfo:eu-repo/grantAgreement/MINECO/Plan Estatal de Investigación Científica y Técnica y de Innovación 2013-2016/SAF2016-80100-Rinfo:eu-repo/grantAgreement/EC/H2020/785907info:eu-repo/grantAgreement/MINECO/Plan Estatal de Investigación Científica y Técnica y de Innovación 2013-2016/SAF2015-66603-Phttp://dx.doi.org/10.1523/JNEUROSCI.1212-19.2019Síinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/2064142026-05-22T06:33:51Z
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