FY2021 Annual Report

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


Songbirds learn to sing their song intensively from their song auditory experience 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 model. Interestingly zebra finch juveniles learn efficiently through social vocal communication 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. We have investigated how neuronal activities of the attention control nucleus, Locus Cereleous (LC), during social interaction with a tutor and regulate activities of neurons in the NCM which has been suggested to store tutor auditory memories. We found that the LC-NCM circuit regulate auditory responses of specific subset of NCM neurons for song learning from a tutor which has live socially communication with, suggesting altering attention with social vocal communication with tutors leads to altering auditory activities of higher auditory cortex that would result in intensive song learning. We also found the axonal retraction between auditory memory sites and song motor control area in the brain during development with a new whole brain axonal tracing technique. We will further investigate underlying neuronal mechanism in the coming years.

1. Staff

  • Makoto Araki, Postdoctoral scholar (until Sept 2021)
  • Jelena Katic, Postdoctoral scholar 
  • Sarah Morson, Postdoctoral scholar 
  • Yuichi Morohashi, Technician
  • Anna Kuneji, Technician 
  • Zhehao Cheng, OIST student
  • Yung-Chieh Liu, OIST student
  • Khelil Bensalah, OIST student (joined Jan 2022)
  • Chie Edwards, Research Unit Administrator

2. Collaborations

  • 2.1 Luke Ramegy-Healry (U Mass) for GABA inhibitory control of auditory activity in zebra finch higher auditory cortical neurons (Supported by NIH RO1 grant)
  • 2.2 Jon Sakata and Sarah Woolley (McGill Univ) for innate restriction in bird song learning
  • 2.3 Takao Hensch (WPI-IRCN, University of Tokyo) for regulation of the timing critical period by neuronal inhibitory function development (Supported by OIST KICKS grant)
  • 2.4 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 Social interaction modulating auditory neuronal activities

Songbirds are learning to sing by hearing of tutor bird singing during development like human babies learn to speak. Juvenile birds intensively learn through social vocal communications with tutors, while they learn little from passive auditory experiences, such as playback from a speaker. We have investigated the underlaying neuronal mechanism for social interaction dependent song learning. Our lab has showed that a subset of neurons in the higher auditory cortex of juvenile zebra finches, NCM, exhibit highly selective auditory responses to the tutor song after song learning (Yanagihara and Yazaki-Sugiyama, 2016), and that the selective auditory response are enhanced by the presence of tutor birds (Yanagihara and Yazaki-Sugiyama, 2018). Here we found that neurons in the nucleus Locus Cereleous (LC), the noradrenergic nucleus which control attention, showed greater auditory responses to live tutor singing than song playback. We further found that the LC-NCM circuits regulated the development of selective response to tutor song in a subset of NCM neurons by using optogenetical inhibition of LC axonal activities within the NCM. Inactivation of LC-NCM during juvenile birds hearing of tutor singing prevents juveniles from song learning from tutor. Taken together these suggest the neuronal circuit for authenticating social information for developmental vocal learning in zebra finches (Katic et al, in revisions).

3.2 Identifications of two complemental neuronal circuits for individual varieties and species identities

Development of organized canonical neuronal circuits are required for healthy and functional brain activity. The formation of functional neural circuits involves genetically programed neuronal projections followed by the elimination of overproduced ‘exuberant’ projections. While excessive experiences in developmental period form additional projections, whether the retraction of functional circuits is involved in experience-dependent neuronal circuit development that shapes higher cognitive skills remains unknown. Analogous to human speech development, songbird juveniles learn to produce complex vocalizations, in a step-wise learning process; hearing and memorizing adult tutors, and then match their vocalization to memorized song of tutors via sensory-motor feedback during developmental critical period. We characterized brain-wide axonal projections from the neurons which exhibit auditory responses to a memorized father song in an auditory memory region, the caudomedial nidopallium (NCM). Neuronal labelling with activity dependent virus expression and axonal tracing in a cleared whole brain samples revealed novel NCM axonal projections to the brain area associated with song learning such as AIV, Area X and HVC-Shelf (Fig. 1). We further found the NCM neurons which were activated by playback of the father’s songs projected to the sensory-motor coordinating site, HVC in male juveniles in song learning period (~60 days post hatch (DPH)), but not in adults. Inducing cell death in those father song responsive neurons in the NCM in juvenile resulted in impaired song mimicking, while lesions in adults did not have any effects on song production and learning. However, in the adult zebra finches, which were subjected to extensive song learning from two tutors sequentially, the NCM and HVC stayed connected. These results suggest transient neuronal connections between the song auditory memory and motor regions, NCM and HVC, to regulate step-wise vocal learning from sensory experiences and its’ developmental time window. Extensive experiences in juvenile period might increase a capacity of neuronal circuits in the adults. (Louder in preparation)

Figure 1_Sugiyama_FY2021

4. Publications

4.1 Journals

  1. Spool J. A., Macedo-Lima M., Scarpa G., Morohashi Y., Yazaki-Sugiyama Y. and Remage-Healey L. (2021) Genetically-identified neurons in avian auditory pallium mirror core principles of their mammalian counterparts. Curr Biol 31:2831-2843.e6, doi: 10.1016/j.cub.2021.04.039

4.2 Books and other one-time publications

Nothing to report

4.3 Oral and Poster Presentations

  1. Jelena Katic, Yuichi Morohashi & Yoko Yazaki-Sugiyama, Neural mechanisms underlying song recognition in the zebra finch higher auditory cortex, the 44th Annual Meeting of the Japan Neuroscience Society, 2021 July, Kobe
  2. Sarah Morson, Yuichi Morohashi & Yoko Yazaki-Sugiyama, Anatomical Connections Between Two Regions of the Higher Auditory Cortex in Zebra Finch Song Memories, the 44th Annual Meeting of the Japan Neuroscience Society, 2021 July, Kobe
  3. Zhehao Cheng & Yoko Yazaki-Sugiyama, Neural mechanisms underlying song recognition in the zebra finch higher auditory cortex, the 44th Annual Meeting of the Japan Neuroscience Society, 2021 July, Kobe
  4. Jelena Katic, Yuichi Morohashi & Yoko Yazaki-Sugiyama, Social interactions activate locus coeruleus which shapes auditory forebrain circuits to form selective memories in a songbird zebra finch, the Annual Meeting of the Society for Neuroscience, 2021 November, Online
  5. Matthew IM Louder, Masafumi Kuroda, Yuichi Morohashi, Daisuke Taniguchi, Yoko Yazaki-Sugiyama, Axon retraction within a sensory-motor circuit coincides with the closure of a critical period for song learning, the Annual Meeting of the Society for Neuroscience, 2021 November, Online

Invited lectures at conferences

  • “Variable axon connectivity of song memory ensembles in developmental zebra finch song learning”, International Symposium on Development and Plasticity of Neural System, 2022 March, Online

5. Intellectual Property Rights and Other Specific Achievements

Nothing to report

6. Meetings and Events

6.1 Symposium: Re-visiting and expansions of neuroethology

Organizing the symposium “Re-visiting and expansions of neuroethology” in the 44th Annual Meeting of the Japan Neuroscience Society, 2021 July, Kobe

  • Co-organized with Co-organized with Dr. Kazuhiro Wada (Hokkaido Univ)

7. Other

Nothing to report.