Neuronal correlates of locomotion speed in the dorsal CA1 of the rat hippocampus: new insights on the speed cells

Detalhes bibliográficos
Autor(a) principal: Góis, José Henrique Targino Dias
Data de Publicação: 2019
Tipo de documento: Tese
Idioma: por
Título da fonte: Repositório Institucional da UFRN
Texto Completo: https://repositorio.ufrn.br/jspui/handle/123456789/28788
Resumo: Edward Tolman postulated the existence of cognitive maps in the brain to explain the animal capability of spatial navigation. Since then, neuroscience seeks to describe brain components underlying this capability. In the present work, we describe advancements in the characterization of a neural sub-population engaged in coding the scalar velocity of rat locomotion. Upon analyzing an open database, we re-discovered the existence of a velocity correlation present in the rate of emission of action potentials of neurons in the dorsal hippocampus. we found that this correlation is independent of theta oscillation frequency (4- 12 Hz) and stable over space and time; moreover, it also persists in different arenas. We then classified the neurons as excitatory and inhibitory by the action potential waveform shapes, the rate of emission of action potentials, and the temporal inter-dependency of action potential emission between pairs of neurons. This classification revealed that, by using Pearson’s r coefficient (speed score) as a correlation metric, in the square open-field arena, only inhibitory neurons high-correlated with locomotion speed (henceforth, speed), even though there was a modulation of the average of the excitatory neurons. Intriguingly, when checking speed correlates in the linear arena, speed score made indistinguishable the correlation among neuronal classes. We then formulated the hypothesis that the apparent locomotion speed correlation of pyramidal neurons in the linear arena is spurious, due to a by-product of their spatial code. To prove this, we simulated artificial neurons that emitted action potentials influenced by the actual animal behavior; the simulated neurons coded either speed or space. The simulation replicated real data Pearson’s r coefficient classifications – true positives in the square arena and false positives in the linear arena for those cells encoding speed. To solve this ethological interdependency, we adopted a new metric of speed correlation – the ratio of the difference of linear-non-linear models prediction accuracy based on speed and position over the prediction accuracy of the two-variable model. This analysis disentangled the ethological issue, satisfactorily classifying the simulated neurons and confirming the spurious hypothesis correlates, and the prevalence of speed correlates in interneurons. The results of the present work demonstrated that a genuine speed correlation is present in the dorsal CA1 of the hippocampus of rats in inhibitory neurons.
id UFRN_06a7316a13a86883b81beb66f6611fe6
oai_identifier_str oai:https://repositorio.ufrn.br:123456789/28788
network_acronym_str UFRN
network_name_str Repositório Institucional da UFRN
repository_id_str
spelling Góis, José Henrique Targino DiasTakahashi, Daniel YasumasaPereira, Rodrigo Neves RomcyTreptow, WernerFiguerola, Wilfredo BlancoTort, Adriano Bretanha Lopes2020-04-15T18:45:30Z2020-04-15T18:45:30Z2019-12-06GÓIS, José Henrique Targino Dias. Neuronal correlates of locomotion speed in the dorsal CA1 of the rat hippocampus: new insights on the speed cells. 2019. 70f. Tese (Doutorado em Neurociências) - Instituto do Cérebro, Universidade Federal do Rio Grande do Norte, Natal, 2019.https://repositorio.ufrn.br/jspui/handle/123456789/28788Edward Tolman postulated the existence of cognitive maps in the brain to explain the animal capability of spatial navigation. Since then, neuroscience seeks to describe brain components underlying this capability. In the present work, we describe advancements in the characterization of a neural sub-population engaged in coding the scalar velocity of rat locomotion. Upon analyzing an open database, we re-discovered the existence of a velocity correlation present in the rate of emission of action potentials of neurons in the dorsal hippocampus. we found that this correlation is independent of theta oscillation frequency (4- 12 Hz) and stable over space and time; moreover, it also persists in different arenas. We then classified the neurons as excitatory and inhibitory by the action potential waveform shapes, the rate of emission of action potentials, and the temporal inter-dependency of action potential emission between pairs of neurons. This classification revealed that, by using Pearson’s r coefficient (speed score) as a correlation metric, in the square open-field arena, only inhibitory neurons high-correlated with locomotion speed (henceforth, speed), even though there was a modulation of the average of the excitatory neurons. Intriguingly, when checking speed correlates in the linear arena, speed score made indistinguishable the correlation among neuronal classes. We then formulated the hypothesis that the apparent locomotion speed correlation of pyramidal neurons in the linear arena is spurious, due to a by-product of their spatial code. To prove this, we simulated artificial neurons that emitted action potentials influenced by the actual animal behavior; the simulated neurons coded either speed or space. The simulation replicated real data Pearson’s r coefficient classifications – true positives in the square arena and false positives in the linear arena for those cells encoding speed. To solve this ethological interdependency, we adopted a new metric of speed correlation – the ratio of the difference of linear-non-linear models prediction accuracy based on speed and position over the prediction accuracy of the two-variable model. This analysis disentangled the ethological issue, satisfactorily classifying the simulated neurons and confirming the spurious hypothesis correlates, and the prevalence of speed correlates in interneurons. The results of the present work demonstrated that a genuine speed correlation is present in the dorsal CA1 of the hippocampus of rats in inhibitory neurons.Edward Tolman postulou a existência de mapas cognitivos no cérebro para explicar a capacidade animal de navegar pelo espaço. Desde então, neurocientistas buscam descrever componentes cerebrais que suportam essa capacidade. No presente trabalho, descrevemos avanços na caracterização de uma sub-população neural que participa na representação da velocidade escalar na locomoção de ratos. Através da análise de um banco de dados aberto, nós re-descobrimos a existência do correlato de velocidade na taxa de emissão de potenciais de ação de neurônios da região CA1 do hipocampo dorsal de ratos. Essa correlação é independente da frequência da oscilação de theta (4-12 Hz) e é estável através do espaço e tempo; além disso, essa correlação persiste em diferentes arenas. A classificação de neurônios entre prováveis excitatórios ou inibitórios revelou que, ao utilizar o coeficiente r de Pearson (índice de velocidade) como métrica de representação de velocidade nos neurônios, somente neurônios inibitórios apresentaram-se como altamente correlacionados com a velocidade na arena quadrada, embora os neurônios excitatórios apresentem uma modulação na média da taxa de emissão de potenciais de ação. Intrigantemente, na arena linear a mesma métrica tornou indistinguiveis as classificações neurais pela correlação com a velocidade. Então, formulamos a hipótese que a aparente correlação com a velocidade dos neurônios excitatórios na arena linear é espúria – um subproduto da correlação de velocidade com o espaço. Para testar essa hipótese, simulei neurônios artificiais que emitem potenciais de ação influenciados pelo comportamento locomotor do animal; essas simulações codificam velocidade ou espaço. As simulações replicaram a classificação pelo índice de velocidade encontrados nos dados reais – ou seja, código de posição não correlaciona com velocidade na arena quadrada mas sim na arena linear. Para solucionar essa interdependência etológica, nós adotamos uma nova métrica de correlação com a velocidade: a razão da diferença da acurácia de predição dos modelos linear-não-linear baseados em velocidade e posição sobre a acurácia de predição do modelo das duas variáveis. Essa análise resolveu o problema etológico, classificou satisfatoriamente as simulações e confirmou a hipótese da correlação espúria na arena linear e a prevalencia da correlação nos neurônios inibitórios. Os resultados deste trabalho demonstra uma correlação genuina da velocidade de locomoção nos neurônios inibitórios na área CA1 do hipocampo dorsal de ratos.Conselho Nacional de Desenvolvimento Científico e Tecnológico - CNPqCoordenação de Aperfeiçoamento de Pessoal de Nível Superior - CAPESCNPQ::OUTROS::CIENCIASSpatial navigationLocomotion speedRatsHippocampusNeuronsElectrophysiologyNeuronal correlates of locomotion speed in the dorsal CA1 of the rat hippocampus: new insights on the speed cellsCorrelatos neuronais da velocidade de locomoção em CA1 dorsal do hipocampo de ratos: novas analises nas células de velocidadeinfo:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/doctoralThesisPROGRAMA DE PÓS-GRADUAÇÃO EM NEUROCIÊNCIASUFRNBrasilinfo:eu-repo/semantics/openAccessporreponame:Repositório Institucional da UFRNinstname:Universidade Federal do Rio Grande do Norte (UFRN)instacron:UFRNTEXTNeuronalcorrelateslocomotion_Gois_2019.pdf.txtNeuronalcorrelateslocomotion_Gois_2019.pdf.txtExtracted texttext/plain141491https://repositorio.ufrn.br/bitstream/123456789/28788/2/Neuronalcorrelateslocomotion_Gois_2019.pdf.txtfbd892c1c8eb9ef7db461ab896aceb7eMD52THUMBNAILNeuronalcorrelateslocomotion_Gois_2019.pdf.jpgNeuronalcorrelateslocomotion_Gois_2019.pdf.jpgGenerated Thumbnailimage/jpeg1456https://repositorio.ufrn.br/bitstream/123456789/28788/3/Neuronalcorrelateslocomotion_Gois_2019.pdf.jpgb8958b3a5492f7f838eabbbe4c58994aMD53ORIGINALNeuronalcorrelateslocomotion_Gois_2019.pdfapplication/pdf8298155https://repositorio.ufrn.br/bitstream/123456789/28788/1/Neuronalcorrelateslocomotion_Gois_2019.pdfb4de91c822561731c16d3a9b0acfa53aMD51123456789/287882020-04-19 04:47:07.241oai:https://repositorio.ufrn.br:123456789/28788Repositório de PublicaçõesPUBhttp://repositorio.ufrn.br/oai/opendoar:2020-04-19T07:47:07Repositório Institucional da UFRN - Universidade Federal do Rio Grande do Norte (UFRN)false
dc.title.pt_BR.fl_str_mv Neuronal correlates of locomotion speed in the dorsal CA1 of the rat hippocampus: new insights on the speed cells
dc.title.alternative.pt_BR.fl_str_mv Correlatos neuronais da velocidade de locomoção em CA1 dorsal do hipocampo de ratos: novas analises nas células de velocidade
title Neuronal correlates of locomotion speed in the dorsal CA1 of the rat hippocampus: new insights on the speed cells
spellingShingle Neuronal correlates of locomotion speed in the dorsal CA1 of the rat hippocampus: new insights on the speed cells
Góis, José Henrique Targino Dias
CNPQ::OUTROS::CIENCIAS
Spatial navigation
Locomotion speed
Rats
Hippocampus
Neurons
Electrophysiology
title_short Neuronal correlates of locomotion speed in the dorsal CA1 of the rat hippocampus: new insights on the speed cells
title_full Neuronal correlates of locomotion speed in the dorsal CA1 of the rat hippocampus: new insights on the speed cells
title_fullStr Neuronal correlates of locomotion speed in the dorsal CA1 of the rat hippocampus: new insights on the speed cells
title_full_unstemmed Neuronal correlates of locomotion speed in the dorsal CA1 of the rat hippocampus: new insights on the speed cells
title_sort Neuronal correlates of locomotion speed in the dorsal CA1 of the rat hippocampus: new insights on the speed cells
author Góis, José Henrique Targino Dias
author_facet Góis, José Henrique Targino Dias
author_role author
dc.contributor.authorID.pt_BR.fl_str_mv
dc.contributor.advisorID.pt_BR.fl_str_mv
dc.contributor.referees1.none.fl_str_mv Takahashi, Daniel Yasumasa
dc.contributor.referees1ID.pt_BR.fl_str_mv
dc.contributor.referees2.none.fl_str_mv Pereira, Rodrigo Neves Romcy
dc.contributor.referees2ID.pt_BR.fl_str_mv
dc.contributor.referees3.none.fl_str_mv Treptow, Werner
dc.contributor.referees3ID.pt_BR.fl_str_mv
dc.contributor.referees4.none.fl_str_mv Figuerola, Wilfredo Blanco
dc.contributor.referees4ID.pt_BR.fl_str_mv
dc.contributor.author.fl_str_mv Góis, José Henrique Targino Dias
dc.contributor.advisor1.fl_str_mv Tort, Adriano Bretanha Lopes
contributor_str_mv Tort, Adriano Bretanha Lopes
dc.subject.cnpq.fl_str_mv CNPQ::OUTROS::CIENCIAS
topic CNPQ::OUTROS::CIENCIAS
Spatial navigation
Locomotion speed
Rats
Hippocampus
Neurons
Electrophysiology
dc.subject.por.fl_str_mv Spatial navigation
Locomotion speed
Rats
Hippocampus
Neurons
Electrophysiology
description Edward Tolman postulated the existence of cognitive maps in the brain to explain the animal capability of spatial navigation. Since then, neuroscience seeks to describe brain components underlying this capability. In the present work, we describe advancements in the characterization of a neural sub-population engaged in coding the scalar velocity of rat locomotion. Upon analyzing an open database, we re-discovered the existence of a velocity correlation present in the rate of emission of action potentials of neurons in the dorsal hippocampus. we found that this correlation is independent of theta oscillation frequency (4- 12 Hz) and stable over space and time; moreover, it also persists in different arenas. We then classified the neurons as excitatory and inhibitory by the action potential waveform shapes, the rate of emission of action potentials, and the temporal inter-dependency of action potential emission between pairs of neurons. This classification revealed that, by using Pearson’s r coefficient (speed score) as a correlation metric, in the square open-field arena, only inhibitory neurons high-correlated with locomotion speed (henceforth, speed), even though there was a modulation of the average of the excitatory neurons. Intriguingly, when checking speed correlates in the linear arena, speed score made indistinguishable the correlation among neuronal classes. We then formulated the hypothesis that the apparent locomotion speed correlation of pyramidal neurons in the linear arena is spurious, due to a by-product of their spatial code. To prove this, we simulated artificial neurons that emitted action potentials influenced by the actual animal behavior; the simulated neurons coded either speed or space. The simulation replicated real data Pearson’s r coefficient classifications – true positives in the square arena and false positives in the linear arena for those cells encoding speed. To solve this ethological interdependency, we adopted a new metric of speed correlation – the ratio of the difference of linear-non-linear models prediction accuracy based on speed and position over the prediction accuracy of the two-variable model. This analysis disentangled the ethological issue, satisfactorily classifying the simulated neurons and confirming the spurious hypothesis correlates, and the prevalence of speed correlates in interneurons. The results of the present work demonstrated that a genuine speed correlation is present in the dorsal CA1 of the hippocampus of rats in inhibitory neurons.
publishDate 2019
dc.date.issued.fl_str_mv 2019-12-06
dc.date.accessioned.fl_str_mv 2020-04-15T18:45:30Z
dc.date.available.fl_str_mv 2020-04-15T18:45:30Z
dc.type.status.fl_str_mv info:eu-repo/semantics/publishedVersion
dc.type.driver.fl_str_mv info:eu-repo/semantics/doctoralThesis
format doctoralThesis
status_str publishedVersion
dc.identifier.citation.fl_str_mv GÓIS, José Henrique Targino Dias. Neuronal correlates of locomotion speed in the dorsal CA1 of the rat hippocampus: new insights on the speed cells. 2019. 70f. Tese (Doutorado em Neurociências) - Instituto do Cérebro, Universidade Federal do Rio Grande do Norte, Natal, 2019.
dc.identifier.uri.fl_str_mv https://repositorio.ufrn.br/jspui/handle/123456789/28788
identifier_str_mv GÓIS, José Henrique Targino Dias. Neuronal correlates of locomotion speed in the dorsal CA1 of the rat hippocampus: new insights on the speed cells. 2019. 70f. Tese (Doutorado em Neurociências) - Instituto do Cérebro, Universidade Federal do Rio Grande do Norte, Natal, 2019.
url https://repositorio.ufrn.br/jspui/handle/123456789/28788
dc.language.iso.fl_str_mv por
language por
dc.rights.driver.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.publisher.program.fl_str_mv PROGRAMA DE PÓS-GRADUAÇÃO EM NEUROCIÊNCIAS
dc.publisher.initials.fl_str_mv UFRN
dc.publisher.country.fl_str_mv Brasil
dc.source.none.fl_str_mv reponame:Repositório Institucional da UFRN
instname:Universidade Federal do Rio Grande do Norte (UFRN)
instacron:UFRN
instname_str Universidade Federal do Rio Grande do Norte (UFRN)
instacron_str UFRN
institution UFRN
reponame_str Repositório Institucional da UFRN
collection Repositório Institucional da UFRN
bitstream.url.fl_str_mv https://repositorio.ufrn.br/bitstream/123456789/28788/2/Neuronalcorrelateslocomotion_Gois_2019.pdf.txt
https://repositorio.ufrn.br/bitstream/123456789/28788/3/Neuronalcorrelateslocomotion_Gois_2019.pdf.jpg
https://repositorio.ufrn.br/bitstream/123456789/28788/1/Neuronalcorrelateslocomotion_Gois_2019.pdf
bitstream.checksum.fl_str_mv fbd892c1c8eb9ef7db461ab896aceb7e
b8958b3a5492f7f838eabbbe4c58994a
b4de91c822561731c16d3a9b0acfa53a
bitstream.checksumAlgorithm.fl_str_mv MD5
MD5
MD5
repository.name.fl_str_mv Repositório Institucional da UFRN - Universidade Federal do Rio Grande do Norte (UFRN)
repository.mail.fl_str_mv
_version_ 1802117877213429760