Single-neuron representation of learned complex sounds in the auditory cortex

Meng Wang; Xiang Liao; Ruijie Li; Shanshan Liang; Ran Ding; Jingcheng Li; Jianxiong Zhang; Wenjing He; Ke Liu; Junxia Pan; Zhikai Zhao; Tong Li; Kuan Zhang; Xingyi Li; Jing Lyu; Zhenqiao Zhou; Zsuzsanna Varga; Yuanyuan Mi; Yi Zhou; Junan Yan; Shaoqun Zeng; Jian K. Liu; Arthur Konnerth; Israel Nelken; Hongbo Jia; Xiaowei Chen

doi:10.1038/s41467-020-18142-z

Single-neuron representation of learned complex sounds in the auditory cortex

Meng Wang, Xiang Liao^*, Ruijie Li, Shanshan Liang, Ran Ding, Jingcheng Li, Jianxiong Zhang, Wenjing He, Ke Liu, Junxia Pan, Zhikai Zhao, Tong Li, Kuan Zhang, Xingyi Li, Jing Lyu, Zhenqiao Zhou, Zsuzsanna Varga, Yuanyuan Mi, Yi Zhou, Junan YanShaoqun Zeng, Jian K. Liu, Arthur Konnerth, Israel Nelken, Hongbo Jia^*, Xiaowei Chen^*

^*Corresponding author for this work

Department of Neurobiology (Natural Sciences)

Research output: Contribution to journal › Article › peer-review

26 Scopus citations

Abstract

The sensory responses of cortical neuronal populations following training have been extensively studied. However, the spike firing properties of individual cortical neurons following training remain unknown. Here, we have combined two-photon Ca²⁺ imaging and single-cell electrophysiology in awake behaving mice following auditory associative training. We find a sparse set (~5%) of layer 2/3 neurons in the primary auditory cortex, each of which reliably exhibits high-rate prolonged burst firing responses to the trained sound. Such bursts are largely absent in the auditory cortex of untrained mice. Strikingly, in mice trained with different multitone chords, we discover distinct subsets of neurons that exhibit bursting responses specifically to a chord but neither to any constituent tone nor to the other chord. Thus, our results demonstrate an integrated representation of learned complex sounds in a small subset of cortical neurons.

Original language	American English
Article number	4361
Journal	Nature Communications
Volume	11
Issue number	1
DOIs	https://doi.org/10.1038/s41467-020-18142-z
State	Published - 1 Dec 2020

Bibliographical note

Funding Information:
The authors are grateful to Dr. X.-Q. Wang, Dr. S. Song, Dr. S. Jacob, Dr. H. Adelsberger, Dr. S. Remy, Dr. O. Barnstedt, M. Fabiszak, Dr. W. Freiwald, Dr. Q. Wen, Dr. D. Kleinfeld, Dr. K. Svoboda, Dr. S. Wu, Dr. R. Quian Quiroga, Dr. J.-D. Wu and Dr. W. Ku for very helpful discussions and comments; to Ms. Jia Lou for help in composing and layout editing of the figures. This study was supported by grants from the National Natural Science Foundation of China (31925018, 31861143038, 31921003, 81671106, 31700933, 81771175, 61705251), the Ministry of Science and Technology of China (2018YFA0109600), the Key Scientific Research Equipment Development Project of the CAS (Super-resolution Microscopy Systems and Key Components, ZDYZ2013-1), and the “100-Talents Program for Elite Engineers” of the CAS (H.J.). A.K. is a Hertie Senior Professor of Neuroscience at TUM and a CAS President’s Distinguished International Visiting Fellow. X.C. is a fellow of the CAS Center for Excellence in Brain Science and Intelligence Technology, and also a member of the Institute of Brain and Intelligence at the Third Military Medical University.

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@article{c6ecf357029a46b8958f3751cac4e2e2,

title = "Single-neuron representation of learned complex sounds in the auditory cortex",

abstract = "The sensory responses of cortical neuronal populations following training have been extensively studied. However, the spike firing properties of individual cortical neurons following training remain unknown. Here, we have combined two-photon Ca2+ imaging and single-cell electrophysiology in awake behaving mice following auditory associative training. We find a sparse set (~5%) of layer 2/3 neurons in the primary auditory cortex, each of which reliably exhibits high-rate prolonged burst firing responses to the trained sound. Such bursts are largely absent in the auditory cortex of untrained mice. Strikingly, in mice trained with different multitone chords, we discover distinct subsets of neurons that exhibit bursting responses specifically to a chord but neither to any constituent tone nor to the other chord. Thus, our results demonstrate an integrated representation of learned complex sounds in a small subset of cortical neurons.",

author = "Meng Wang and Xiang Liao and Ruijie Li and Shanshan Liang and Ran Ding and Jingcheng Li and Jianxiong Zhang and Wenjing He and Ke Liu and Junxia Pan and Zhikai Zhao and Tong Li and Kuan Zhang and Xingyi Li and Jing Lyu and Zhenqiao Zhou and Zsuzsanna Varga and Yuanyuan Mi and Yi Zhou and Junan Yan and Shaoqun Zeng and Liu, {Jian K.} and Arthur Konnerth and Israel Nelken and Hongbo Jia and Xiaowei Chen",

note = "Funding Information: The authors are grateful to Dr. X.-Q. Wang, Dr. S. Song, Dr. S. Jacob, Dr. H. Adelsberger, Dr. S. Remy, Dr. O. Barnstedt, M. Fabiszak, Dr. W. Freiwald, Dr. Q. Wen, Dr. D. Kleinfeld, Dr. K. Svoboda, Dr. S. Wu, Dr. R. Quian Quiroga, Dr. J.-D. Wu and Dr. W. Ku for very helpful discussions and comments; to Ms. Jia Lou for help in composing and layout editing of the figures. This study was supported by grants from the National Natural Science Foundation of China (31925018, 31861143038, 31921003, 81671106, 31700933, 81771175, 61705251), the Ministry of Science and Technology of China (2018YFA0109600), the Key Scientific Research Equipment Development Project of the CAS (Super-resolution Microscopy Systems and Key Components, ZDYZ2013-1), and the “100-Talents Program for Elite Engineers” of the CAS (H.J.). A.K. is a Hertie Senior Professor of Neuroscience at TUM and a CAS President{\textquoteright}s Distinguished International Visiting Fellow. X.C. is a fellow of the CAS Center for Excellence in Brain Science and Intelligence Technology, and also a member of the Institute of Brain and Intelligence at the Third Military Medical University. Publisher Copyright: {\textcopyright} 2020, The Author(s).",

year = "2020",

month = dec,

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doi = "10.1038/s41467-020-18142-z",

language = "American English",

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Wang, M, Liao, X, Li, R, Liang, S, Ding, R, Li, J, Zhang, J, He, W, Liu, K, Pan, J, Zhao, Z, Li, T, Zhang, K, Li, X, Lyu, J, Zhou, Z, Varga, Z, Mi, Y, Zhou, Y, Yan, J, Zeng, S, Liu, JK, Konnerth, A, Nelken, I, Jia, H & Chen, X 2020, 'Single-neuron representation of learned complex sounds in the auditory cortex', Nature Communications, vol. 11, no. 1, 4361. https://doi.org/10.1038/s41467-020-18142-z

TY - JOUR

T1 - Single-neuron representation of learned complex sounds in the auditory cortex

AU - Wang, Meng

AU - Liao, Xiang

AU - Li, Ruijie

AU - Liang, Shanshan

AU - Ding, Ran

AU - Li, Jingcheng

AU - Zhang, Jianxiong

AU - He, Wenjing

AU - Liu, Ke

AU - Pan, Junxia

AU - Zhao, Zhikai

AU - Li, Tong

AU - Zhang, Kuan

AU - Li, Xingyi

AU - Lyu, Jing

AU - Zhou, Zhenqiao

AU - Varga, Zsuzsanna

AU - Mi, Yuanyuan

AU - Zhou, Yi

AU - Yan, Junan

AU - Zeng, Shaoqun

AU - Liu, Jian K.

AU - Konnerth, Arthur

AU - Nelken, Israel

AU - Jia, Hongbo

AU - Chen, Xiaowei

N1 - Funding Information: The authors are grateful to Dr. X.-Q. Wang, Dr. S. Song, Dr. S. Jacob, Dr. H. Adelsberger, Dr. S. Remy, Dr. O. Barnstedt, M. Fabiszak, Dr. W. Freiwald, Dr. Q. Wen, Dr. D. Kleinfeld, Dr. K. Svoboda, Dr. S. Wu, Dr. R. Quian Quiroga, Dr. J.-D. Wu and Dr. W. Ku for very helpful discussions and comments; to Ms. Jia Lou for help in composing and layout editing of the figures. This study was supported by grants from the National Natural Science Foundation of China (31925018, 31861143038, 31921003, 81671106, 31700933, 81771175, 61705251), the Ministry of Science and Technology of China (2018YFA0109600), the Key Scientific Research Equipment Development Project of the CAS (Super-resolution Microscopy Systems and Key Components, ZDYZ2013-1), and the “100-Talents Program for Elite Engineers” of the CAS (H.J.). A.K. is a Hertie Senior Professor of Neuroscience at TUM and a CAS President’s Distinguished International Visiting Fellow. X.C. is a fellow of the CAS Center for Excellence in Brain Science and Intelligence Technology, and also a member of the Institute of Brain and Intelligence at the Third Military Medical University. Publisher Copyright: © 2020, The Author(s).

PY - 2020/12/1

Y1 - 2020/12/1

N2 - The sensory responses of cortical neuronal populations following training have been extensively studied. However, the spike firing properties of individual cortical neurons following training remain unknown. Here, we have combined two-photon Ca2+ imaging and single-cell electrophysiology in awake behaving mice following auditory associative training. We find a sparse set (~5%) of layer 2/3 neurons in the primary auditory cortex, each of which reliably exhibits high-rate prolonged burst firing responses to the trained sound. Such bursts are largely absent in the auditory cortex of untrained mice. Strikingly, in mice trained with different multitone chords, we discover distinct subsets of neurons that exhibit bursting responses specifically to a chord but neither to any constituent tone nor to the other chord. Thus, our results demonstrate an integrated representation of learned complex sounds in a small subset of cortical neurons.

AB - The sensory responses of cortical neuronal populations following training have been extensively studied. However, the spike firing properties of individual cortical neurons following training remain unknown. Here, we have combined two-photon Ca2+ imaging and single-cell electrophysiology in awake behaving mice following auditory associative training. We find a sparse set (~5%) of layer 2/3 neurons in the primary auditory cortex, each of which reliably exhibits high-rate prolonged burst firing responses to the trained sound. Such bursts are largely absent in the auditory cortex of untrained mice. Strikingly, in mice trained with different multitone chords, we discover distinct subsets of neurons that exhibit bursting responses specifically to a chord but neither to any constituent tone nor to the other chord. Thus, our results demonstrate an integrated representation of learned complex sounds in a small subset of cortical neurons.

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DO - 10.1038/s41467-020-18142-z

M3 - Article

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AN - SCOPUS:85089998104

SN - 2041-1723

VL - 11

JO - Nature Communications

JF - Nature Communications

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ER -

Single-neuron representation of learned complex sounds in the auditory cortex

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