Rapid hippocampal plasticity supports motor sequence learning

Recent evidence suggests that gains in performance observed while humans learn a novel motor sequence occur during the quiet rest periods interleaved with practice (micro-offline gains, MOGs). This phenomenon is reminiscent of memory replay observed in the hippocampus during spatial learning in rode...

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Published in:Proceedings of the National Academy of Sciences - PNAS Vol. 117; no. 38; p. 23898
Main Authors: Jacobacci, Florencia, Armony, Jorge L, Yeffal, Abraham, Lerner, Gonzalo, Amaro, Jr, Edson, Jovicich, Jorge, Doyon, Julien, Della-Maggiore, Valeria
Format: Journal Article
Language:English
Published: United States 22.09.2020
Subjects:
Adolescent
Adult
Female
Hippocampus - physiology
Humans
Learning - physiology
Magnetic Resonance Imaging
Male
Memory
Motor Skills - physiology
Young Adult
functional MRI
structural plasticity
reactivation
hippocampus
motor sequence learning
ISSN:1091-6490, 1091-6490
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Abstract Recent evidence suggests that gains in performance observed while humans learn a novel motor sequence occur during the quiet rest periods interleaved with practice (micro-offline gains, MOGs). This phenomenon is reminiscent of memory replay observed in the hippocampus during spatial learning in rodents. Whether the hippocampus is also involved in the production of MOGs remains currently unknown. Using a multimodal approach in humans, here we show that activity in the hippocampus and the precuneus increases during the quiet rest periods and predicts the level of MOGs before asymptotic performance is achieved. These functional changes were followed by rapid alterations in brain microstructure in the order of minutes, suggesting that the same network that reactivates during the quiet periods of training undergoes structural plasticity. Our work points to the involvement of the hippocampal system in the reactivation of procedural memories.
AbstractList Recent evidence suggests that gains in performance observed while humans learn a novel motor sequence occur during the quiet rest periods interleaved with practice (micro-offline gains, MOGs). This phenomenon is reminiscent of memory replay observed in the hippocampus during spatial learning in rodents. Whether the hippocampus is also involved in the production of MOGs remains currently unknown. Using a multimodal approach in humans, here we show that activity in the hippocampus and the precuneus increases during the quiet rest periods and predicts the level of MOGs before asymptotic performance is achieved. These functional changes were followed by rapid alterations in brain microstructure in the order of minutes, suggesting that the same network that reactivates during the quiet periods of training undergoes structural plasticity. Our work points to the involvement of the hippocampal system in the reactivation of procedural memories.
Recent evidence suggests that gains in performance observed while humans learn a novel motor sequence occur during the quiet rest periods interleaved with practice (micro-offline gains, MOGs). This phenomenon is reminiscent of memory replay observed in the hippocampus during spatial learning in rodents. Whether the hippocampus is also involved in the production of MOGs remains currently unknown. Using a multimodal approach in humans, here we show that activity in the hippocampus and the precuneus increases during the quiet rest periods and predicts the level of MOGs before asymptotic performance is achieved. These functional changes were followed by rapid alterations in brain microstructure in the order of minutes, suggesting that the same network that reactivates during the quiet periods of training undergoes structural plasticity. Our work points to the involvement of the hippocampal system in the reactivation of procedural memories.Recent evidence suggests that gains in performance observed while humans learn a novel motor sequence occur during the quiet rest periods interleaved with practice (micro-offline gains, MOGs). This phenomenon is reminiscent of memory replay observed in the hippocampus during spatial learning in rodents. Whether the hippocampus is also involved in the production of MOGs remains currently unknown. Using a multimodal approach in humans, here we show that activity in the hippocampus and the precuneus increases during the quiet rest periods and predicts the level of MOGs before asymptotic performance is achieved. These functional changes were followed by rapid alterations in brain microstructure in the order of minutes, suggesting that the same network that reactivates during the quiet periods of training undergoes structural plasticity. Our work points to the involvement of the hippocampal system in the reactivation of procedural memories.
Author Amaro, Jr, Edson
Doyon, Julien
Della-Maggiore, Valeria
Armony, Jorge L
Jovicich, Jorge
Yeffal, Abraham
Jacobacci, Florencia
Lerner, Gonzalo
Author_xml – sequence: 1
  givenname: Florencia
  orcidid: 0000-0001-5407-4345
  surname: Jacobacci
  fullname: Jacobacci, Florencia
  organization: Instituto de Fisiología y Biofísica (IFIBIO) Houssay, Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Departamento de Fisiología y Biofísica, Universidad de Buenos Aires, Buenos Aires, 1121, Argentina
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  givenname: Jorge L
  surname: Armony
  fullname: Armony, Jorge L
  organization: Douglas Mental Health Research Institute, McGill University, Montreal, QC, H4H 1R3, Canada
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  givenname: Abraham
  orcidid: 0000-0002-9645-6664
  surname: Yeffal
  fullname: Yeffal, Abraham
  organization: Instituto de Fisiología y Biofísica (IFIBIO) Houssay, Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Departamento de Fisiología y Biofísica, Universidad de Buenos Aires, Buenos Aires, 1121, Argentina
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  givenname: Gonzalo
  surname: Lerner
  fullname: Lerner, Gonzalo
  organization: Instituto de Fisiología y Biofísica (IFIBIO) Houssay, Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Departamento de Fisiología y Biofísica, Universidad de Buenos Aires, Buenos Aires, 1121, Argentina
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  givenname: Edson
  orcidid: 0000-0002-5889-1382
  surname: Amaro, Jr
  fullname: Amaro, Jr, Edson
  organization: Plataforma de Imagens na Sala de Autopsia (PISA), Instituto de Radiologia, Facultade de Medicina, Universidade de Sao Paulo, Sao Paulo, 05403-000, Brazil
– sequence: 6
  givenname: Jorge
  orcidid: 0000-0001-9504-7503
  surname: Jovicich
  fullname: Jovicich, Jorge
  organization: Center for Mind/Brain Sciences, University of Trento, Rovereto, 38068, Trento, Italy
– sequence: 7
  givenname: Julien
  surname: Doyon
  fullname: Doyon, Julien
  organization: Department of Neurology and Neurosurgery, McGill University, Montreal, QC, H3A 2B4, Canada
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  givenname: Valeria
  orcidid: 0000-0001-9586-4255
  surname: Della-Maggiore
  fullname: Della-Maggiore, Valeria
  email: vdellamaggiore@fmed.uba.ar
  organization: Instituto de Fisiología y Biofísica (IFIBIO) Houssay, Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Departamento de Fisiología y Biofísica, Universidad de Buenos Aires, Buenos Aires, 1121, Argentina; vdellamaggiore@fmed.uba.ar
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structural plasticity
reactivation
hippocampus
motor sequence learning
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Snippet Recent evidence suggests that gains in performance observed while humans learn a novel motor sequence occur during the quiet rest periods interleaved with...
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SubjectTerms Adolescent
Adult
Female
Hippocampus - physiology
Humans
Learning - physiology
Magnetic Resonance Imaging
Male
Memory
Motor Skills - physiology
Young Adult
Title Rapid hippocampal plasticity supports motor sequence learning
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