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Hierarchical emergence of sequence sensitivity in the songbird auditory forebrain

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Abstract

Bengalese finches (Lonchura striata var. domestica) generate more complex sequences in their songs than zebra finches. Because of this, we chose this species to explore the signal processing of sound sequence in the primary auditory forebrain area, field L, and in a secondary area, the caudomedial nidopallium (NCM). We simultaneously recorded activity from multiple single units in urethane-anesthetized birds. We successfully replicated the results of a previous study in awake zebra finches examining stimulus-specific habituation of NCM neurons to conspecific songs. Then, we used an oddball paradigm and compared the neural response to deviant sounds that were presented infrequently, with the response to standard sounds, which were presented frequently. In a single sound oddball task, two different song elements were assigned for the deviant and standard sounds. The response bias to deviant elements was larger in NCM than in field L. In a triplet sequence oddball task, two triplet sequences containing elements ABC and ACB were assigned as the deviant and standard. Only neurons in NCM that displayed broad-shaped spike waveforms had sensitivity to the difference in element order. Our results suggest the hierarchical processing of complex sound sequences in the songbird auditory forebrain.

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Abbreviations

BOS:

Bird’s own song

CLM:

Caudolateral mesopallium

CMM:

Caudomedial mesopallium

Dv:

Deviant stimulus

IOI:

Inter-onset interval

ISI:

Inter-spike interval

NCM:

Caudomedial nidopallium

RMS:

Root-mean-square

St:

Standard stimulus

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Acknowledgments

We thank Dr. Jun Nishikawa for his instruction in the surgical techniques and the use of the data acquisition software. We also thank Dr. Ryosuke Tachibana for his helpful comments in the data analysis and discussion. This work was supported by Grant in Aids from MEXT #23240033, #25590202 and #26240019 to Kazuo Okanoya, and JST ERATO Okanoya Emotional Information Project. The experimental procedures and housing conditions were approved by the Institutional Animal Care and Use Committee at the University of Tokyo.

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Correspondence to Yoshimasa Seki.

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Ono, S., Okanoya, K. & Seki, Y. Hierarchical emergence of sequence sensitivity in the songbird auditory forebrain. J Comp Physiol A 202, 163–183 (2016). https://doi.org/10.1007/s00359-016-1070-7

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  • DOI: https://doi.org/10.1007/s00359-016-1070-7

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