FY2014 Annual Report

Neuronal Mechanism for Critical Period Unit

Assistant Professor Yoko Yazaki-Sugiyama

1.Abstract

Like humans learning to speak, songbirds learn to sing by hearing what other birds are singing, preferentially other conspecific birds, during a developmental critical period. In zebra finches, the best-studied model of songbird vocalization, males sing and females do not. Baby male zebra finches listen and memorize tutor songs, normally their fathers’ songs, during an early, sensory learning period. Then in a subsequent sensory-motor learning period, they vocalize by themselves and shape their own songs, by matching their songs to the memorized tutor songs. We are especially interested in how auditory experience during sensory learning period shapes the brain circuitry to form a memory of auditory experiences. In addition, we are learning how auditory information is processed to distinguish conspecific songs for referentially learning from them.

2. Staff

Yoko Yazaki-Sugiyama, Assistant Professor
Makoto Araki, Postdoctral scholar
Christian Flecke, Postdoctral scholar
Shin Yanagihara, Staff scientist
Yuichi Morohashi Technician
Mohamed Haytham Mohamed Aly, Graduate Student
Sachiko Blanck, Administrative Assistant

3. Collaborations

Application of viral vector system to the zebra finches.

Collaboration with Prof.. Michael Lazarus, Tsukuba Universityc

4. Activities and Findings

1. Forming memory of early auditory experience in zebra finch brain

During early development, juvenile songbirds listen to and form an auditory memory of the adult tutor song. Thereafter, they use this memory to shape their vocalizations in later sensorimotor learning. The auditory association cortex, called the NCM, is a potential storage site for tutor song memory, but no direct evidence has been found for a neuronal representation of this memory in juvenile songbirds. We explored the neuronal substrate for tutor song memory by recording single-neuron activity in the NCM of behaving juvenile zebra finches. We found there are two types of neurons in NCM, different in spike shape and firing rate. Both of the neurons were responsive to many of behaviorally relevant auditory stimulation, including their own song, father’s song or other zebra finch songs, before having adult song experience. In contrast, after being tutored, a subset of one neuron type began to exhibit highly selective auditory responses to the experienced tutor song. Moreover, blockade of GABAergic inhibition, as well as a sleep state, decreased the auditory selectivity to a specific song. Taken together, these results suggest that experience-dependent recruitment of GABA-mediated inhibition shapes auditory cortical circuits, and the tutor song memory is therefore sparsely represented in a subset of auditory cortical neurons.

Figure 2: Two distinct neurons in zebra finch auditory forebrain (L3) encode different song information.

Sound spectrograph of song stimulation (top), zebra finch song (CON), contentious white noise (WHN), artificial song with white noise syllables (White noise song (WNS)), with phase-scrambled syllable (Phase scrambled song (PSS)), and a raster plot of LF and HF (bottom) to those songs.

2. Auditory information processing in zebra finch auditory pathway for conspecific voice detection.

Male zebra finches learn songs from their auditory experience during the juvenile period. Among varieties of song they hear, interestingly they preferentially learn from conspecific songs. Songs of zebra finches generally consist of a few acoustical elements, called syllables, which emerge in a stereotyped sequence separated by small silent gaps (~30 ms). However, it is largely unknown how zebra finches detect their species song and proceed to learn from it. We investigated how song auditory information is processed and cognized in the auditory circuit, especially in the primary auditory area, field L (homologous to the mammalian primary auditory cortex) where neurons detect natural sound such as birdsongs out of noise.

In subregion L2a (homologous to layer 4 in the mammalian auditory cortex), where neurons receive thalamic inputs, neurons showed auditory responses to continuous white noise (WHN) as well as to conspecific songs (CON), while neurons in the downstream layer, L3, did not respond to WHN. In L3 we identified two distinct neurons, lower firing neuron (LF) and higher firing neuron (HF). Interestingly, HF responded to WHN when it was presented with the same durations and intervals as syllable elements of CON (white noise song: WNS), while LF did not. In contrast, both LF and HF responded to the CON, even when the frequency phase was scrambled within each syllable. Moreover, when HF was stimulated with same CON syllables repeatedly, they did not response when the silent gaps in between were too short (<5ms), and showed synchronized response to the repeat with decreasing of firing along with repeats when the durations of silent gap were relevant with those in zebra finch songs. These results suggest that within the auditory information processing for song cognition, temporal cues of syllable onset and offset are proceeded independent of the morphology information of songs.

Figure 2: Two distinct neurons in zebra finch auditory forebrain (L3) encode different song information.

5. Intellectual Property Rights and Other Specific Achievements

5.1 Journals

Yazaki-Sugiyama, Y., Yanagihara, S, Fuller, P.M. and Lazarus M. (2014) Acute inhibition of a cortical motor area impairs vocal control in singing zebra finches. Eur J Neurosci. 2015 Jan;41(1):97-108

5.2 Books and other one-time publications,

None

5.3 Oral and Poster Presentations

Invited oral talk at conference

‘Neuronal representations of tutor song experience.’

Symposium ‘Learned vocal communication in songbirds: Recent developments' at 11th International Congress of Neuroethology (2014), Sapporo, Japan

Poster presentation

Flecke, C. & Yazaki-Sugiyama, Y. Sensory memory forms in the caudomedial nidopallium during song learning. International Congress of Neuroethology, July 2014, Sapporo
Yanagihara, S. & Yazaki-Sugiyama, Y., Auditory experience shapes neural selectivity to a tutor’s song in the songbird auditory cortex. International Congress of Neuroethology, July 2014, Sapporo
Yanagihara, S. & Yazaki-Sugiyama, Y., Emergence of neural selectivity for learned songs in the songbird auditory cortex. Neuro2014, Sept 2014, Yokohama
Araki, M., Bandi, M.M., Connaughton C.P. & Yazaki-Sugiyama, Y., Temporal cue cognition of song information processing in the auditory forebrain of the zebra finch. The 44th Annual Meeting of Society for Neuroscience, Nov 2014, Washington DC, USA
Yanagihara, S. & Yazaki-Sugiyama, Y., Emergence of neural selectivity for memorized birdsongs in the higher-level auditory cortex of juvenile songbird. The 44th Annual Meeting of Society for Neuroscience, Nov 2014, Washington DC, USA

6 Intellectual Property Rights and Other Specific Achievements

6.1 Patent

None

6.2 Grant

‘Neuronal mechanism song learning critical period’

JSPS KAKENHI Grants-in-Aid for Scientific Research (C)

PI: Yoko Yazaki-Sugiyama

‘Behavioral state control of auditory memory formation in zebra finch song learning.’

MEXT KAKENHI, Grant-in-Aid for Scientific Research on Innovative Areas, ‘Memory Dynamism’