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New Research, Sensory and Motor Systems

Sound Frequency Representation in the Auditory Cortex of the Common Marmoset Visualized Using Optical Intrinsic Signal Imaging

Toshiki Tani, Hiroshi Abe, Taku Hayami, Taku Banno, Naohisa Miyakawa, Naohito Kitamura, Hiromi Mashiko, Noritaka Ichinohe and Wataru Suzuki
eNeuro 25 April 2018, ENEURO.0078-18.2018; DOI: https://doi.org/10.1523/ENEURO.0078-18.2018
Toshiki Tani
1Ichinohe Neural System Group, Laboratory for Molecular Analysis of Higher Brain Functions, RIKEN Brain Science Institute, RIKEN, Wako, Saitama 351-0198, Japan
2Department of Ultrastructural Research, National Institute of Neuroscience, National Center of Neurology and Psychiatry, Kodaira, Tokyo 187-8502, Japan
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Hiroshi Abe
1Ichinohe Neural System Group, Laboratory for Molecular Analysis of Higher Brain Functions, RIKEN Brain Science Institute, RIKEN, Wako, Saitama 351-0198, Japan
2Department of Ultrastructural Research, National Institute of Neuroscience, National Center of Neurology and Psychiatry, Kodaira, Tokyo 187-8502, Japan
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Taku Hayami
2Department of Ultrastructural Research, National Institute of Neuroscience, National Center of Neurology and Psychiatry, Kodaira, Tokyo 187-8502, Japan
3Department of Biotechnology and Life Science, Graduate School of Engineering, Tokyo University of Agriculture and Technology, Koganei, Tokyo 184-8588, Japan
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Taku Banno
2Department of Ultrastructural Research, National Institute of Neuroscience, National Center of Neurology and Psychiatry, Kodaira, Tokyo 187-8502, Japan
4Department of Otorhinolaryngology, University of Pennsylvania, Philadelphia, PA 19104, USA
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Naohisa Miyakawa
2Department of Ultrastructural Research, National Institute of Neuroscience, National Center of Neurology and Psychiatry, Kodaira, Tokyo 187-8502, Japan
5Department of Functional Brain Imaging Research, National Institutes of Quantum and Radiological Science and Technology, Chiba, Chiba 263-8555, Japan
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  • ORCID record for Naohisa Miyakawa
Naohito Kitamura
1Ichinohe Neural System Group, Laboratory for Molecular Analysis of Higher Brain Functions, RIKEN Brain Science Institute, RIKEN, Wako, Saitama 351-0198, Japan
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Hiromi Mashiko
1Ichinohe Neural System Group, Laboratory for Molecular Analysis of Higher Brain Functions, RIKEN Brain Science Institute, RIKEN, Wako, Saitama 351-0198, Japan
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Noritaka Ichinohe
1Ichinohe Neural System Group, Laboratory for Molecular Analysis of Higher Brain Functions, RIKEN Brain Science Institute, RIKEN, Wako, Saitama 351-0198, Japan
2Department of Ultrastructural Research, National Institute of Neuroscience, National Center of Neurology and Psychiatry, Kodaira, Tokyo 187-8502, Japan
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Wataru Suzuki
1Ichinohe Neural System Group, Laboratory for Molecular Analysis of Higher Brain Functions, RIKEN Brain Science Institute, RIKEN, Wako, Saitama 351-0198, Japan
2Department of Ultrastructural Research, National Institute of Neuroscience, National Center of Neurology and Psychiatry, Kodaira, Tokyo 187-8502, Japan
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Abstract

Natural sound is composed of various frequencies. Although the core region of the primate auditory cortex has functionally defined sound frequency preference maps, how the map is organized in the auditory areas of the belt and parabelt regions is not well known. In this study, we investigated the functional organizations of the core, belt, and parabelt regions encompassed by the lateral sulcus and the superior temporal sulcus in the common marmoset (Callithrix jacchus). Using optical imaging of intrinsic signals, we obtained evoked responses to band-pass noise stimuli in a range of sound frequencies (0.5-16 kHz) in anesthetized adult animals and visualized the preferred sound frequency map on the cortical surface. We characterized the functionally defined organization using histologically defined brain areas in the same animals. We found tonotopic representation of a set of sound frequencies (low to high) within the primary (A1), rostral, and rostrotemporal areas of the core region. In the belt region, the tonotopic representation existed only in the mediolateral (ML) area. This representation was symmetric with that found in A1 along the border between areas A1 and ML. The functional structure was not very clear in the anterolateral area. Low frequencies were mainly preferred in the rostrotemplatal area, while high frequencies were preferred in the caudolateral area. There was a portion of the parabelt region that strongly responded to higher sound frequencies (>5.8 kHz) along the border between the rostral and caudal parabelt regions.

Significance Statement In this study, we examined functional organizations for sound frequency representation in the core, belt, and parabelt regions in the marmoset using optical intrinsic signal imaging. In addition to the auditory areas in the core region, the ML in the belt region continuously represented a range of frequencies from low to high, with tonotopic organization, which was symmetric to that in the A1 in the core region about the border between the A1 and ML. The posterior and anterior belt regions represented mainly low and high frequencies, respectively. The parabelt region contained a distinct region with preference for high frequencies. These results suggest that the functional organization unique to each auditory region would process sound information specific to this species.

  • EcoG
  • Histology
  • Marmoset
  • Optical Imaging
  • Sound Frequency
  • Tonotopy

Footnotes

  • Authors report no conflict of interest.

  • This work was supported by Grant-in-Aid for Scientific Research (C) (17K04512, 26430031), and the program for Brain Mapping by Integrated Neurotechnologies for Disease Studies (Brain/MINDS) from Japan Agency for Medical Research and Development (AMED), Japan.

This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

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Sound Frequency Representation in the Auditory Cortex of the Common Marmoset Visualized Using Optical Intrinsic Signal Imaging
Toshiki Tani, Hiroshi Abe, Taku Hayami, Taku Banno, Naohisa Miyakawa, Naohito Kitamura, Hiromi Mashiko, Noritaka Ichinohe, Wataru Suzuki
eNeuro 25 April 2018, ENEURO.0078-18.2018; DOI: 10.1523/ENEURO.0078-18.2018

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Sound Frequency Representation in the Auditory Cortex of the Common Marmoset Visualized Using Optical Intrinsic Signal Imaging
Toshiki Tani, Hiroshi Abe, Taku Hayami, Taku Banno, Naohisa Miyakawa, Naohito Kitamura, Hiromi Mashiko, Noritaka Ichinohe, Wataru Suzuki
eNeuro 25 April 2018, ENEURO.0078-18.2018; DOI: 10.1523/ENEURO.0078-18.2018
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Keywords

  • ECoG
  • histology
  • marmoset
  • optical imaging
  • Sound Frequency
  • Tonotopy

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