Transient sensorimotor projections in the developmental song learning period
Matthew I.M. Louder,
Masafumi Kuroda,
Daisuke Taniguchi,
Joanna Agnieszka Komorowska-Müller,
Yuichi Morohashi,
Megumu Takahashi,
Miguel Sánchez-Valpuesta,
Kazuhiro Wada,
Yasushi Okada,
Hiroyuki Hioki,
Yoko Yazaki-Sugiyama
Affiliations
Matthew I.M. Louder
International Research Center for Neurointelligence (WPI-IRCN), The University of Tokyo, Bunkyo-ku, Tokyo 113-0033, Japan
Masafumi Kuroda
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
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
Neuronal Mechanism of Critical Period Unit, OIST Graduate University, Kunigami, Okinawa 904-0495, Japan
Yuichi Morohashi
Neuronal Mechanism of Critical Period Unit, OIST Graduate University, Kunigami, Okinawa 904-0495, Japan
Megumu Takahashi
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
Graduate School of Life Science, Hokkaido University, Sapporo, Hokkaido 060-0810, Japan
Kazuhiro Wada
Graduate School of Life Science, Hokkaido University, Sapporo, Hokkaido 060-0810, Japan; Faculty of Science, Hokkaido University, Sapporo, Hokkaido 060-0810, Japan
Yasushi Okada
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
Department of Neuroanatomy, Juntendo University Graduate School of Medicine, Bunkyo-ku, Tokyo 113-8421, Japan
Yoko Yazaki-Sugiyama
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; Corresponding author
Summary: 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.
