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A primate temporal cortex–zona incerta pathway for novelty seeking

Nature Neuroscience volume 25, pages 50–60 (2022)Cite this article

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Abstract

Primates interact with the world by exploring visual objects; they seek opportunities to view novel objects even when these have no extrinsic reward value. How the brain controls this novelty seeking is unknown. Here we show that novelty seeking in monkeys is regulated by the zona incerta (ZI). As monkeys made eye movements to familiar objects to trigger an opportunity to view novel objects, many ZI neurons were preferentially activated by predictions of novel objects before the gaze shift. Low-intensity ZI stimulation facilitated gaze shifts, whereas ZI inactivation reduced novelty seeking. ZI-dependent novelty seeking was not regulated by neurons in the lateral habenula or by many dopamine neurons in the substantia nigra, traditionally associated with reward seeking. But the anterior ventral medial temporal cortex, an area important for object vision and memory, was a prominent source of novelty predictions. These data uncover a functional pathway in the primate brain that regulates novelty seeking.

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Fig. 1: Behavior and single neurons’ activities during novelty seeking.
Fig. 2: Novelty-seeking signals in the ZI.
Fig. 3: ZI is causally related to novelty seeking.
Fig. 4: The AVMTC is a prominent cortical source of novelty-prediction signals.

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Data availability

All data are available upon reasonable request from the corresponding author.

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All code is available upon request.

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Acknowledgements

This work is supported by the National Institute of Mental Health under award numbers R01MH110594 and R01MH116937 to IEM, and by the McKnight Foundation award to IEM. The optimization of array technology was supported by the Defense Advanced Research Projects Agency (DARPA) Biological Technologies Office (BTO) ElectRx program under the auspices of D. Weber through the CMO grant/contract no. HR0011-16-2-0022. We are grateful to K. Kocher for great animal care and animal training, and to A. Kepecs, E. S. Bromberg-Martin and C. Padoa-Schioppa for giving us valuable suggestions to improve this manuscript. We are also grateful to B. Goodell and C. M. Gray for technical and scientific assistance with high channel-count recording arrays, to D. W. Moran for assistance with perfusion, and to FD Neuro Technologies for assistance with tissue processing.

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  1. These authors contributed equally: F. Sogukpinar and K. Zhang.

Authors and Affiliations

  1. Department of Neuroscience, Washington University School of Medicine, St. Louis, MO, USA

    Takaya Ogasawara, Julia Pai, Ahmad Jezzini & Ilya E. Monosov

  2. Department of Electrical Engineering, Washington University, St. Louis, MO, USA

    Fatih Sogukpinar & Ilya E. Monosov

  3. Department of Biomedical Engineering, Washington University, St. Louis, MO, USA

    Kaining Zhang, Yang-Yang Feng & Ilya E. Monosov

  4. Department of Neurosurgery School of Medicine, Washington University, St. Louis, MO, USA

    Ilya E. Monosov

  5. Pain Center, Washington University School of Medicine, St. Louis, MO, USA

    Ilya E. Monosov

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Contributions

T.O., I.E.M. and Y.F. performed the neuronal recordings. T.O., F.S., K.Z. and J.P. analyzed the data. I.E.M. wrote the manuscript. T.O., J.P., Y.F. and I.E.M. discussed and revised the manuscript. A.J. analyzed the anatomical data. I.E.M. guided and conceptualized the research.

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Correspondence to Takaya Ogasawara or Ilya E. Monosov.

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Ogasawara, T., Sogukpinar, F., Zhang, K. et al. A primate temporal cortex–zona incerta pathway for novelty seeking. Nat Neurosci 25, 50–60 (2022). https://doi.org/10.1038/s41593-021-00950-1

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