Transient sensorimotor projections in the developmental song learning period.

CP: Neuroscience auditory axon retraction critical period development memory ensembles neuronal circuit rewiring sensorimotor learning songbird vocal whole-brain connectome

Journal

Cell reports
ISSN: 2211-1247
Titre abrégé: Cell Rep
Pays: United States
ID NLM: 101573691

Informations de publication

Date de publication:
07 May 2024
Historique:
received: 18 04 2023
revised: 15 01 2024
accepted: 19 04 2024
medline: 8 5 2024
pubmed: 8 5 2024
entrez: 8 5 2024
Statut: aheadofprint

Résumé

Memory recall and guidance are essential for motor skill acquisition. Like humans learning to speak, male zebra finches learn to sing by first memorizing and then matching their vocalization to the tutor's song (TS) during specific developmental periods. Yet, the neuroanatomical substrate supporting auditory-memory-guided sensorimotor learning has remained elusive. Here, using a whole-brain connectome analysis with activity-dependent viral expression, we identified a transient projection into the motor region, HVC, from neuronal ensembles responding to TS in the auditory forebrain, the caudomedial nidopallium (NCM), in juveniles. Virally induced cell death of the juvenile, but not adult, TS-responsive NCM neurons impaired song learning. Moreover, isolation, which delays closure of the sensory, but not the motor, learning period, did not affect the decrease of projections into the HVC from the NCM TS-responsive neurons after the song learning period. Taken together, our results suggest that dynamic axonal pruning may regulate timely auditory-memory-guided vocal learning during development.

Identifiants

pubmed: 38717902
pii: S2211-1247(24)00524-2
doi: 10.1016/j.celrep.2024.114196
pii:
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

114196

Informations de copyright

Copyright © 2024 The Author(s). Published by Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests The authors declare no competing interests.

Auteurs

Matthew I M Louder (MIM)

International Research Center for Neurointelligence (WPI-IRCN), The University of Tokyo, Bunkyo-ku, Tokyo 113-0033, Japan.

Masafumi Kuroda (M)

International Research Center for Neurointelligence (WPI-IRCN), The University of Tokyo, Bunkyo-ku, Tokyo 113-0033, Japan; RIKEN Center for Biosystems Dynamics Research (BDR), Suita, Osaka 565-0874, Japan.

Daisuke Taniguchi (D)

International Research Center for Neurointelligence (WPI-IRCN), The University of Tokyo, Bunkyo-ku, Tokyo 113-0033, Japan; RIKEN Center for Biosystems Dynamics Research (BDR), Suita, Osaka 565-0874, Japan.

Joanna Agnieszka Komorowska-Müller (JA)

Neuronal Mechanism of Critical Period Unit, OIST Graduate University, Kunigami, Okinawa 904-0495, Japan.

Yuichi Morohashi (Y)

Neuronal Mechanism of Critical Period Unit, OIST Graduate University, Kunigami, Okinawa 904-0495, Japan.

Megumu Takahashi (M)

Department of Neuroanatomy, Juntendo University Graduate School of Medicine, Bunkyo-ku, Tokyo 113-8421, Japan; Center for Genomic and Regenerative Medicine, Juntendo University Graduate School of Medicine, Bunkyo-ku, Tokyo 113-8421, Japan.

Miguel Sánchez-Valpuesta (M)

Graduate School of Life Science, Hokkaido University, Sapporo, Hokkaido 060-0810, Japan.

Kazuhiro Wada (K)

Graduate School of Life Science, Hokkaido University, Sapporo, Hokkaido 060-0810, Japan; Faculty of Science, Hokkaido University, Sapporo, Hokkaido 060-0810, Japan.

Yasushi Okada (Y)

International Research Center for Neurointelligence (WPI-IRCN), The University of Tokyo, Bunkyo-ku, Tokyo 113-0033, Japan; RIKEN Center for Biosystems Dynamics Research (BDR), Suita, Osaka 565-0874, Japan; Department of Cell Biology, Department of Physics, and Universal Biology Institute (UBI), The University of Tokyo, Bunkyo-ku, Tokyo 113-0033, Japan.

Hiroyuki Hioki (H)

Department of Neuroanatomy, Juntendo University Graduate School of Medicine, Bunkyo-ku, Tokyo 113-8421, Japan.

Yoko Yazaki-Sugiyama (Y)

International Research Center for Neurointelligence (WPI-IRCN), The University of Tokyo, Bunkyo-ku, Tokyo 113-0033, Japan; Neuronal Mechanism of Critical Period Unit, OIST Graduate University, Kunigami, Okinawa 904-0495, Japan. Electronic address: yazaki-sugiyama@oist.jp.

Classifications MeSH