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Research ArticleNew 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, 5 (2) ENEURO.0078-18.2018; 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, 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, 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
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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, 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, Wako, Saitama 351-0198, Japan
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Noritaka Ichinohe
2Department of Ultrastructural Research, National Institute of Neuroscience, National Center of Neurology and Psychiatry, Kodaira, Tokyo 187-8502, Japan
1Ichinohe Neural System Group, Laboratory for Molecular Analysis of Higher Brain Functions, RIKEN Brain Science Institute, Wako, Saitama 351-0198, Japan
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Wataru Suzuki
2Department of Ultrastructural Research, National Institute of Neuroscience, National Center of Neurology and Psychiatry, Kodaira, Tokyo 187-8502, Japan
1Ichinohe Neural System Group, Laboratory for Molecular Analysis of Higher Brain Functions, RIKEN Brain Science Institute, Wako, Saitama 351-0198, Japan
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  • Figure 1.
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    Figure 1.

    Coronal sections from the left hemisphere of a marmoset stained for myelin and the areal demarcation of the auditory cortical areas. Auditory cortical areas are defined by the myelin structure. The white lines indicate the areal borders. The black filled circles represent positions of blood vessels. The filled and open white arrowheads indicate the lateral sulcus and the superior temporal sulcus, respectively.

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    Figure 2.

    Optical responses to sound frequencies in the auditory cortex of the marmoset shown in Figure 1. A single condition map was reconstructed based on the optical signal changes in response to sound frequencies of 0.5, 0.7, 1, 1.4, 2, 2.9, 4, 5.8, 8, 11.6, and 16 kHz. The response magnitude is indicated by the gray scale shown at the left bottom. The black and white regions indicate the highest and lowest response magnitudes, respectively. The white lines represent the histologically defined areal borders of the auditory cortex.

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    Figure 3.

    Response magnitude maps and the mean response magnitude in each auditory area for the three marmosets. A–C, top, Response magnitude maps reconstructed based on maximum evoked optical signals for sound frequencies of 0.5, 0.7, 1, 1.4, 2, 2.9, 4, 5.8, 8, 11.6, and 16 kHz for each marmoset. The color indicates the maximum signal magnitude at each pixel according to scale bar shown in A. Blood vessel images for each map are shown in the inset. Bottom, The mean response magnitude and SD in each auditory area. LS and STS represent the lateral sulcus and superior temporal sulcus, respectively. D, Time course of optical signals in response to each stimulus frequency in the six regions indicated in A. The colors of the lines correspond to the optical signal evoked for each frequency. The vertical black lines and horizontal red lines represent stimulus onset and the stimulus presentation period, respectively.

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    Figure 4.

    Sound frequency preference maps for the three marmosets. A–C, Sound frequency preference maps reconstructed from averaged responses for all sound frequencies for the three marmosets. The color indicates the preferred frequency at each pixel according to the color code. LS and STS represent the lateral sulcus and superior temporal sulcus, respectively.

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    Figure 5.

    Distribution of preferred sound frequencies in each auditory cortical area. A: relative areas with preference for sound frequencies of 0.5–0.7, 0.7–1, 1–1.4, 1.4–2, 2–2.9, 2.9–4, 4–5.8, 5.8–8, 8–11.6, and 11.6–16 kHz. B, Relative areas with preference for different sound frequencies in the core, belt, and parabelt regions. The pale blue, orange, and gray lines represent the three individual marmosets, and the black line represents the mean value for the three marmosets. The number of asterisks represent the number of animals with significantly biased representation in response to the sound frequency.

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    Figure 6.

    Electrical responses to band-pass noise stimuli. A, ECoG responses to sound frequencies of 1.4, 4, 8, and 16 kHz at four contacts. The horizontal red lines represent the stimulus presentation period. B, left, Electrode positions of the ECoG device on the sound frequency preference map made based on OISI in Figure 4C. Green circles represent the contact positions shown in A. The brown circles correspond to the remaining contacts. LS and STS represent the lateral sulcus and superior temporal sulcus, respectively. Right, Sound frequency preference map reconstructed based on the maximum ECoG responses to all sound frequencies. Color indicates the preferred sound frequency at each contact according to the color code.

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    Figure 7.

    Sound frequency preference map for common marmosets. The circles surrounding H and L indicate regions with preference for high and low frequencies, respectively. The arrows indicate the direction of frequency preference change from low to high. The dotted region represents regions requiring further study. LS and STS represent the lateral sulcus and superior temporal sulcus, respectively. The color map in the simplified schematic of the marmoset cortex in the inset represents the sound frequency preference map.

Tables

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    Table 1.

    The magnitude of the optical signals % (mean ± SD) in each auditory area

    SubjectA1RRTCLMLALRTLCPBRPB
    Marmoset 11.1 ± 0.40.9 ± 0.40.5 ± 0.20.5 ± 0.21.1 ± 0.31.2 ± 0.30.6 ± 0.20.6 ± 0.20.6 ± 0.2
    Marmoset 20.5 ± 0.30.5 ± 0.20.5 ± 0.20.3 ± 0.20.7 ± 0.10.4 ± 0.20.6 ± 0.10.2 ± 0.10.2 ± 0.1
    Marmoset 31.0 ± 0.40.6 ± 0.20.5 ± 0.20.5 ± 0.20.9 ± 0.30.6 ± 0.10.5 ± 0.20.5 ± 0.20.3 ± 0.1
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    Table 2.

    The number of pixels for each defined auditory area

    SubjectA1RRTCLMLALRTLCPBRPB
    Marmoset 11416969614539669011398618061531807418897
    Marmoset 29417529020185092907253202247161848828
    Marmoset 31261666603496670911482493551722134222588
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March/April 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, 5 (2) 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, 5 (2) 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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