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Change detection in the primate auditory cortex through feedback of prediction error signals

Author

Listed:
  • Keitaro Obara

    (The University of Tokyo
    RIKEN Center for Brain Science)

  • Teppei Ebina

    (The University of Tokyo)

  • Shin-Ichiro Terada

    (The University of Tokyo)

  • Takanori Uka

    (University of Yamanashi)

  • Misako Komatsu

    (RIKEN Center for Brain Science)

  • Masafumi Takaji

    (RIKEN Center for Brain Science
    RIKEN Center for Brain Science)

  • Akiya Watakabe

    (RIKEN Center for Brain Science
    RIKEN Center for Brain Science)

  • Kenta Kobayashi

    (Section of Viral Vector Development, National Institute for Physiological Sciences)

  • Yoshito Masamizu

    (RIKEN Center for Brain Science)

  • Hiroaki Mizukami

    (Jichi Medical University)

  • Tetsuo Yamamori

    (RIKEN Center for Brain Science
    RIKEN Center for Brain Science
    Central Institute of Experimental Animals)

  • Kiyoto Kasai

    (The University of Tokyo
    The University of Tokyo Institutes for Advanced Study)

  • Masanori Matsuzaki

    (The University of Tokyo
    RIKEN Center for Brain Science
    The University of Tokyo Institutes for Advanced Study)

Abstract

Although cortical feedback signals are essential for modulating feedforward processing, no feedback error signal across hierarchical cortical areas has been reported. Here, we observed such a signal in the auditory cortex of awake common marmoset during an oddball paradigm to induce auditory duration mismatch negativity. Prediction errors to a deviant tone presentation were generated as offset calcium responses of layer 2/3 neurons in the rostral parabelt (RPB) of higher-order auditory cortex, while responses to non-deviant tones were strongly suppressed. Within several hundred milliseconds, the error signals propagated broadly into layer 1 of the primary auditory cortex (A1) and accumulated locally on top of incoming auditory signals. Blockade of RPB activity prevented deviance detection in A1. Optogenetic activation of RPB following tone presentation nonlinearly enhanced A1 tone response. Thus, the feedback error signal is critical for automatic detection of unpredicted stimuli in physiological auditory processing and may serve as backpropagation-like learning.

Suggested Citation

  • Keitaro Obara & Teppei Ebina & Shin-Ichiro Terada & Takanori Uka & Misako Komatsu & Masafumi Takaji & Akiya Watakabe & Kenta Kobayashi & Yoshito Masamizu & Hiroaki Mizukami & Tetsuo Yamamori & Kiyoto , 2023. "Change detection in the primate auditory cortex through feedback of prediction error signals," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-42553-3
    DOI: 10.1038/s41467-023-42553-3
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    References listed on IDEAS

    as
    1. Gloria G. Parras & Javier Nieto-Diego & Guillermo V. Carbajal & Catalina Valdés-Baizabal & Carles Escera & Manuel S. Malmierca, 2017. "Neurons along the auditory pathway exhibit a hierarchical organization of prediction error," Nature Communications, Nature, vol. 8(1), pages 1-17, December.
    2. Teppei Ebina & Yoshito Masamizu & Yasuhiro R. Tanaka & Akiya Watakabe & Reiko Hirakawa & Yuka Hirayama & Riichiro Hira & Shin-Ichiro Terada & Daisuke Koketsu & Kazuo Hikosaka & Hiroaki Mizukami & Atsu, 2018. "Two-photon imaging of neuronal activity in motor cortex of marmosets during upper-limb movement tasks," Nature Communications, Nature, vol. 9(1), pages 1-16, December.
    3. Debajit Saha & Wensheng Sun & Chao Li & Srinath Nizampatnam & William Padovano & Zhengdao Chen & Alex Chen & Ege Altan & Ray Lo & Dennis L. Barbour & Baranidharan Raman, 2017. "Engaging and disengaging recurrent inhibition coincides with sensing and unsensing of a sensory stimulus," Nature Communications, Nature, vol. 8(1), pages 1-19, August.
    4. Timothy P. Lillicrap & Daniel Cownden & Douglas B. Tweed & Colin J. Akerman, 2016. "Random synaptic feedback weights support error backpropagation for deep learning," Nature Communications, Nature, vol. 7(1), pages 1-10, December.
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    Cited by:

    1. Shinnosuke Nomura & Shin-Ichiro Terada & Teppei Ebina & Masato Uemura & Yoshito Masamizu & Kenichi Ohki & Masanori Matsuzaki, 2024. "ARViS: a bleed-free multi-site automated injection robot for accurate, fast, and dense delivery of virus to mouse and marmoset cerebral cortex," Nature Communications, Nature, vol. 15(1), pages 1-23, December.
    2. Teppei Ebina & Akitaka Sasagawa & Dokyeong Hong & Rieko Setsuie & Keitaro Obara & Yoshito Masamizu & Masashi Kondo & Shin-Ichiro Terada & Katsuya Ozawa & Masato Uemura & Masafumi Takaji & Akiya Wataka, 2024. "Dynamics of directional motor tuning in the primate premotor and primary motor cortices during sensorimotor learning," Nature Communications, Nature, vol. 15(1), pages 1-21, December.

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