FY2019 Annual Report

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


Songbirds learn to sing their courtship song from their tutor song experience intensively 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. Recent years we have focused more on how song learning is regulated by juveniles attention and/or motivation; Juvenile birds learn songs intensively from social vocal communications with tutor birds (normally their fathers), while they learn little from passive auditory experiences. We have focused on neuromodulatory functions which regulates attention and elucidated the neuronal activities of the noradrenergic nucleus, Locus Cereleous (LC), during song learning. We further investigated how LC neurons regulate activities of neurons in the NCM which has been suggested to store tutor auditory memories. We found that subsets of NCM neurons decreased their auditory response to tutor song by inhibiting of LC neuronal activities at NCM using optogenetical tools. Inactivaton of LC axon activities at NCM during juveniles listening tutors’ songs prevented them to learn from tutors’ song. Taken together we suggest that attention changes by social interaction with tutors leads to altering auditory activities of higher auditory cortex through activities of LC, that would result in intensive memory formation with social vocal communications.

1. Staff

  • Dr. Makoto Araki, Postdoctoral scholar
  • Dr. Jelena Katic, Postdoctoral scholar
  • Dr. Sarah Morson, Postdoctoral scholar (from December 2019)
  • Dr. Yuichi Morohashi, Technician
  • Anna Kuneji, Technician
  • Zhehao Cheng, OIST student
  • Yung-Chieh Liu, OIST Student
  • Chie Edwards, Research Unit Administrator

2. Collaborations

2.1 GABA inhibitory control of auditory activity in zebra finch higher auditory cortical neurons (Supported by NIH RO1 grant)

  • Researcher:
    • Dr. Luke Ramegy-Healry (U Mass)

2.2 Innate restriction in bird song learning

  • Researchers:
    • Dr. Jon Sakata and Dr. Sarah Woolley (McGill Univ)

2.3 Regulation of the timing critical period by neuronal inhibitory function development (Supported by OIST KICKS grant)

  • Researcher:
    • Dr. Takao Hensch (WPI-IRCN, University of Tokyo)

3. Activities and Findings

3.1 Social interaction modulating auditory neuronal activities

Songbirds are learning to sing from auditory experiences of singing of tutor birds during development. Juvenile birds intensively learn from the auditory experience through social interactions with tutors, while they learn little from passive auditory experiences, such as playback from a speaker. However, underlaying neuronal mechanism for social interaction dependent song learning has yet to be elucidated. In previous years we showed that a subset of neurons in the higher auditory cortex of juvenile zebra finches 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). We also found that the neurons in LC, the noradrenergic nucleus which control attention, showed auditory responses to song playback as well as greater responses to tutor song singing. LC neurons, which were activated by hearing of tutor singing, project to the higher auditory cortex. We further investigated how LC neuronal activities regulate higher auditory cortex by manipulating the LC neuronal activities by using optogenetical tools. Inactivation of LC neuronal activities during juvenile birds hearing of tutor singing caused decrease in auditory responses of auditory cortical neurons to tutors’ song and less song learning (Figure 1). Taken together these suggests neuronal activity changes of LC neurons by attentional level alteration by social interaction with tutors regulate auditory neuronal activities in the higher auditory cortex neurons of juvenile zebra finches, that may result in forming a memory of tutor songs.

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

Continuing from the previous years we anatomically identified the two categories of neurons in the brain area, called Field L, which is homologous to mammalian primary auditory cortex. Previously we found two types of neurons in the Field L which encode complemental temporal and acoustical features of songs, respectively (Araki et al., 2016). By combining the tissue clearing technique, X-Clarity, and virus vector mediated fluorescent protein expressions, we randomly visualize the anatomical structures of hundreds of neurons in the primary auditory cortex. We then categorized them into group with their anatomical character, such as cell body shape and axon projection patterns etc. We further identified the song responsive neurons anatomically after intracellular recording of their auditory physiological properties and match to the categorized group in volume data. Taken together we elucidated the anatomical characterizations of neurons in the zebra finch primary auditory cortex, Field L and identified the neurons which convey temporal and morphological information of songs.

4. Publications

4.1 Journals

Nothing to report

4.2 Books and other one-time publications

Book Chapter: ‘Neural Circuits Underlying Vocal Learning in Songbirds’ in "The Neuroethology of Birdsong", SHAR volume 71 ed. by Sakata S.T., Woolley S.C., Springer, Fay R.R., Popper A.N. (2020), Springer

4.3 Oral and Poster Presentations

  1. Jelena Katic & Yoko Yazaki-Sugiyama, How attention shapes song perception in juvenile zebra finches during song learning, The 42nd Japanese Neuroscience Meeting, Niigata, July 2019
  2. Makoto Araki & Yoko Yazaki-Sugiyama, Morphological identification of zebra finch primary auditory neurons for parallel encoding of individually unique and species-specific song features, Annual meeting of Society for Neuroscience, Oct 2019
  3. Jelena Katic & Yoko Yazaki-Sugiyama, How social interactions affect attention and song perception in juvenile zebra finches during song learning, Annual meeting of Society for Neuroscience, Oct 2019
  4. ‘Meet-the-Expert’ at Society for Neuroscience, Chicago, USA, Oct 2019
  5. Teaching Lecture at 42nd Annual Meeting of Japanese Neuroscience Society, ‘What we can learn from how birds learn to vocalize’, Niigata Japan, July 2019
  6. Invited lecture at Kumamoto University, HIGO leading program, Kumamoto Japan, Dec 2019

5. Intellectual Property Rights and Other Specific Achievements

Nothing to report

6. Meetings and Events

6.1 OIST Workshop: Developmental Neurobiology Course (DNC)

  • Co-organizers: David Van Vactor, Ichiro Masai

6.2 OIST mini-workshop: Neuromodulators: its’ development and functions

  • Co-organizers: Hisashi Umemori (Harvard Univ)

7. Other

Nothing to report.