The cerebellum acts as the analog to the medial temporal lobe for sensorimotor memory.


Journal

Proceedings of the National Academy of Sciences of the United States of America
ISSN: 1091-6490
Titre abrégé: Proc Natl Acad Sci U S A
Pays: United States
ID NLM: 7505876

Informations de publication

Date de publication:
15 Oct 2024
Historique:
medline: 7 10 2024
pubmed: 7 10 2024
entrez: 7 10 2024
Statut: ppublish

Résumé

The cerebellum is critical for sensorimotor learning. The specific contribution that it makes, however, remains unclear. Inspired by the classic finding that for declarative memories, medial temporal lobe (MTL) structures provide a gateway to the formation of long-term memory but are not required for short-term memory, we hypothesized that for sensorimotor memories, the cerebellum may play an analogous role. Here, we studied the sensorimotor learning of individuals with severe ataxia from cerebellar degeneration. We dissected the memories they formed during sensorimotor learning into a short-term temporally-volatile component, that decays rapidly with a time constant of just 15 to 20 s and thus cannot lead to long-term retention, and a longer-term temporally-persistent component that is stable for 60 s or more and leads to long-term retention. Remarkably, we find that these individuals display dramatically reduced levels of temporally-persistent sensorimotor memory, despite spared and even elevated levels of temporally-volatile sensorimotor memory. In particular, we find both impairment that systematically worsens with memory window duration over shorter memory windows (<12 s) and near-complete impairment of memory maintenance over longer memory windows (>25 s). This dissociation uncovers a unique role for the cerebellum as a gateway for the formation of long-term but not short-term sensorimotor memories, mirroring the role of the MTL for declarative memories. It thus reveals the existence of distinct neural substrates for short-term and long-term sensorimotor memory, and it explains both the trial-to-trial differences identified in this study and long-standing study-to-study differences in the effects of cerebellar damage on sensorimotor learning ability.

Identifiants

pubmed: 39374383
doi: 10.1073/pnas.2411459121
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

e2411459121

Subventions

Organisme : McKnight Foundation (McKnight)
ID : McKnight Scholar Award
Organisme : Alfred P. Sloan Foundation (APSF)
ID : Sloan Research Fellowship
Organisme : NIA NIH HHS
ID : R01 AG041878
Pays : United States

Déclaration de conflit d'intérêts

Competing interests statement:The authors declare no competing interest.

Auteurs

Alkis M Hadjiosif (AM)

John A. Paulson School of Engineering and Applied Sciences, Cambridge, MA 02138.
Center for Neurotechnology and Neurorecovery, Massachusetts General Hospital, Boston, MA 02114.

Tricia L Gibo (TL)

Philips Medical Systems, Best, Noord-Brabant 5684, The Netherlands.
Department of Mechanical Engineering, Johns Hopkins University, Baltimore, MD 21218.

Maurice A Smith (MA)

John A. Paulson School of Engineering and Applied Sciences, Cambridge, MA 02138.
Center for Brain Science, Harvard University, Cambridge, MA 02138.

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