FY2022 Anual Report

Neuronal Mechanism for Critical Period Unit
Associate Professor Yoko Yazaki-Sugiyama

Abstract

Songbirds learn to sing vocalize intensively through social vocal communications during development as humans learn to speak. Our lab has been investigating the neuronal mechanism underlying how early auditory experiences shape neuronal circuits for song learning and auditory perception and how the time window for this neuronal circuits wiring is regulated by using zebra finch, one of premier model of songbirds. Interestingly, zebra finch juveniles learn efficiently through social interaction with a tutor, while they learn little from passive auditory song experiences. Recent years we also have worked on how social interaction regulate effective song learning and found the neuronal circuit from the attention control nucleus, Locus Cereleous (LC) to the higher auditory cortical area, NCM, authenticate social information for song learning via vocal communication. We have started to elucidate how this neuronal circuit change their activities during development regarding regulating the time window of developmental critical period. As we also found transient neuronal projections from NCM to the song motor control area which subserving song learning, we also have established the new project where we are trying to do genetic profiling of these neuronal subsets.

1. Staff

Jelena Katic, Postdoctoral scholar (until Dec 2022)
Sarah Morson, Postdoctoral scholar
Joanna Komorowska-Mueller, Postdoctoral scholar (joined April 2022)
Yuichi Morohashi, Technician
Anna Kuneji, Technician
Zhehao Cheng, OIST student
Yung-Chieh Liu, OIST student
Khelil Bensalah, OIST student
Chie Edwards, Research Unit Administrator

2. Collaborations

Luke Ramegy-Healry (U Mass) for GABA inhibitory control of auditory activity in zebra finch higher auditory cortical neurons (Supported by NIH RO1 grant)
Jon Sakata and Sarah Woolley (McGill Univ) for innate restriction in bird song learning (Supported by CIHR grant)
Takao K Hensch (WPI-IRCN, the University of Tokyo) for regulation of the timing critical period by neuronal inhibitory function development (Supported by OIST KICKS grant)
Masafumi Kuroda and Daisuke Taniguchi (WPI-IRCN, the University of Tokyo) for the development of whole brain axonal tracing and annotations

3. Activities and Findings

3.1 Neuronal circuit for authenticating social information in zebra finch so g learning through vocal communications

Social interactions are essential when learning to communicate. In human speech and bird song, infants must acquire accurate vocalization patterns and learn to associate them with live tutors and not mimetic sources. However, the neural mechanism of social reality during vocal learning remains unknown. Here, we characterize a neural circuit for social authentication in support of accurate song learning in the zebra finch. We recorded neural activity in the noradrenergic command center, the locus coeruleus (LC), of juvenile birds during song learning from a live adult tutor. LC activity increased with real, not artificial, social information during learning that enhanced the precision and robustness of the learned song. During live social song learning, LC firing reconfigured long-term song-selective neural responsiveness in an auditory memory region, the caudomedial nidopallium (NCM). In accord, optogenetic inhibition of LC presynaptic signaling in the NCM disordered NCM neuronal responsiveness to live tutor singing and impaired song learning. These results demonstrate that the LC-NCM neural circuit integrates sensory evidence of real social interactions, distinct from song prosody, to authenticate song learning. The findings suggest a general mechanism for validating social information in brain development (Katic et al, 2022).

3.2 Transient auditory-motor neuronal projections subserving developmental zebra finch song learning

Memory recall and guidance is essential for motor skill acquisition. Like humans learning to speak, male zebra finches learn to sing by memorizing a tutor’s song then vocally matching it in sequentially well-orchestrated auditory then sensorimotor developmental learning periods. Yet, the neuroanatomical substrate supporting auditory memory-guided sensorimotor learning has remained elusive. Here, we identified a transient neuronal projection into the motor control region, HVC, from distinct neuronal memory ensembles of the tutor’s song in the auditory forebrain area, caudomedial nidopallium (NCM). Novel whole-brain connectome analysis during the developmental song learning period was made possible by an activity-dependent viral expression system in zebra finches. In turn, virally-induced cell death of neurons activated earlier by hearing their tutor’s songs in the juvenile NCM impaired song learning, while the same deletion in adulthood had no such effect on faithful song production. Moreover, sequential song learning from two tutors of different species yielded distinct neuronal ensembles for two song memories, both of which retained connectivity to HVC into adulthood. Dynamic pruning of long-range axonal projections thus regulates auditory memory-guided vocal learning during a specific juvenile period in zebra finches. Persistence of exuberant connections with enriched experience in the same period may increase the capacity of song circuits in adulthood, implicating similar underlying mechanisms in human bilingualism (Louder Submitted).

3.3 Effect of social interaction on brain functions sensing through wireless biosensing devices.

Social interaction, especially during development, have an impact either positively or negatively, to establishing healthy mental condition and social life, suggesting affecting of brain functions. However, monitoring brain functions during animals/humans have natural social behaviors is almost impossible due to the needs of wired and/or heavy/big equipment sitting on the head which restrict interaction with other individuals. On the other hand social interaction with others cause changes in biophysical conditions, blood pressure, body temperature etc. through alterations in internal conditions, such as stress, attention or motivation. We have started a new project where we develop methods to sense the effect of social behavior on brain functions by measuring of fluctuations of biological condition with small wireless devices. This is a collation project with Seiko Instruments Ltd. and the Univ of Tokyo.

4. Publications

4.1 Journals

Katic K., Morohashi Y. and Yazaki-Sugiyama Y. Neural Circuit for Social Authentication in Song Learning. Nat. Commun (2022) 13(1):4442. doi: 10.1038/s41467-022-32207-1
Scarpa G.B., Starrett J..R, Li G..L, Brooks C., Morohashi Y., Yazaki-Sugiyama Y., Remage-Healey L. (2022) Estrogens rapidly shape synaptic and intrinsic properties to regulate the temporal precision of songbird auditory neurons. Cereb Cortex bhac280. doi: 10.1093/cercor/bhac280.

4.2 Books and other one-time publications

Nothing to report

4.3 Oral and Poster Presentations

Sarah Morson, Yuichi Morohashi and Yoko Yazaki-Sugiyama, Investigating Functions of Parallel Connections in the Zebra Finch Higher Auditory Cortex For Memory Processing During Song Learning NEURO 2022, The 45th annual meeting of the Japan Neuroscience Society, 2022 July, Okinawa, Japan
Yung-Chieh Liu, Yuichi Morohashi & Yoko Yazaki-Sugiyama, Neural bases for song preference to familiar songs in female zebra finches NEURO 2022, The 45th annual meeting of the Japan Neuroscience Society, 2022 July, Okinawa, Japan
Zhehao Cheng , Yoko Yazaki-Sugiyama, Neural mechanisms underlying song recognition in the zebra finch higher auditory cortex, the 45th Annual Meeting of the Japan Neuroscience Society, 2022 July, Naha
Sarah Morson, Yuichi Morohashi and Yoko Yazaki-Sugiyama, Investigating parallel song memory connections in the zebra finch higher auditory cortex International Congress Neuroethology 2022, July, Lisbon, Portugal
Sarah Morson, Yuichi Morohashi and Yoko Yazaki-Sugiyama, Investigating Parallel Song Memory Connections in the Zebra Finch Higher Auditory Cortex, Neuroscience 2022, The annual meeting of Society for Neuroscience, 2022 November, San Diego, USA
Yung-Chieh Liu, Yuichi Morohashi & Yoko Yazaki-Sugiyama, Neural bases for song preference behavior to father’s song in female zebra finches Neuroscience 2022, The annual meeting of Society for Neuroscience, 2022 November, San Diego, USA

4.4 Invited lectures at conferences

IRCN-iPlasticity International Symposium, “Social information regulates zebra finch song learning during developmental critical period”, the University of Tokyo, Tokyo, Japan, Jan 2023
Gordon Conference, ‘Auditory System’, “Social Interactions Regulate Auditory Experience-Dependent Song Learning in Zebra Finches” Bryant University, MA, USA, July 2022
THE DAVID BODIAN SEMINAR, “Transient auditory-motor projections subserving developmental song learning”, The Zanvyl Krieger Mind/Brain Institute, Johns Hopkins University, March 2023