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Neuronal mechanisms of novelty seeking

Takaya Ogasawara, Fatih Sogukpinar, Kaining Zhang, Yang-Yang Feng, Julia Pai, Ahmad Jezzini, Ilya E. Monosov
doi: https://doi.org/10.1101/2021.03.12.435019
Takaya Ogasawara
1Department of Neuroscience, Washington University School of Medicine, St. Louis, MO, 63110, USA
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Fatih Sogukpinar
2Department of Electrical Engineering, Washington University, St. Louis, MO, 63130, USA
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Kaining Zhang
3Department of Biomedical Engineering, Washington University, St. Louis, MO, 63130, USA
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Yang-Yang Feng
3Department of Biomedical Engineering, Washington University, St. Louis, MO, 63130, USA
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Julia Pai
1Department of Neuroscience, Washington University School of Medicine, St. Louis, MO, 63110, USA
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Ahmad Jezzini
1Department of Neuroscience, Washington University School of Medicine, St. Louis, MO, 63110, USA
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Ilya E. Monosov
1Department of Neuroscience, Washington University School of Medicine, St. Louis, MO, 63110, USA
2Department of Electrical Engineering, Washington University, St. Louis, MO, 63130, USA
3Department of Biomedical Engineering, Washington University, St. Louis, MO, 63130, USA
4Department of Neurosurgery School of Medicine, Washington University, St. Louis, MO, 63110, USA
5Pain Center, Washington University School of Medicine, St. Louis, MO, 63110, USA
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  • For correspondence: ilya.monosov@gmail.com
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Abstract

Humans and other primates interact with the world by observing and exploring visual objects. In particular, they often seek out the opportunities to view novel objects that they have never seen before, even when they have no extrinsic primary reward value. However, despite the importance of novel visual objects in our daily life, we currently lack an understanding of how primate brain circuits control the motivation to seek out novelty. We found that novelty-seeking is regulated by a small understudied subcortical region, the zona incerta (ZI). In a task in which monkeys made eye movements to familiar objects to obtain the opportunity to view novel objects, many ZI neurons were preferentially activated by predictions of future novel objects and displayed burst excitations before gaze shifts to gain access to novel objects. Low intensity electrical stimulation of ZI facilitated gaze shifts, while inactivations of ZI reduced novelty-seeking. Surprisingly, additional experiments showed that this ZI-dependent novelty seeking behavior is not regulated by canonical neural circuitry for reward seeking. The habenula-dopamine pathway, known to reflect reward predictions that control reward seeking, was relatively inactive during novelty-seeking behavior in which novelty had no extrinsic reward value. Instead, high channel-count electrophysiological experiments and anatomical tracing identified a prominent source of control signals for novelty seeking in the anterior ventral medial temporal cortex (AVMTC), a brain region known to be crucially involved in visual processing and object memory. In addition to their well-known function in signaling the novelty or familiarity of objects in the current environment, AVMTC neurons reflected the predictions of future novel objects, akin to the way neurons in reward-circuitry predict future rewards in order to control reward-seeking. Our data uncover a network of primate brain areas that regulate novelty-seeking. The behavioral and neural distinctions between novelty-seeking and reward-processing highlight how the brain can accomplish behavioral flexibility, providing a mechanism to explore novel objects.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • ↵† Contact authors: Ilya E. Monosov (ilya.monosov{at}gmail.com) and Takaya Ogasawara (takaya.ogasawara{at}wustl.edu)

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Posted March 13, 2021.
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Neuronal mechanisms of novelty seeking
Takaya Ogasawara, Fatih Sogukpinar, Kaining Zhang, Yang-Yang Feng, Julia Pai, Ahmad Jezzini, Ilya E. Monosov
bioRxiv 2021.03.12.435019; doi: https://doi.org/10.1101/2021.03.12.435019
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Neuronal mechanisms of novelty seeking
Takaya Ogasawara, Fatih Sogukpinar, Kaining Zhang, Yang-Yang Feng, Julia Pai, Ahmad Jezzini, Ilya E. Monosov
bioRxiv 2021.03.12.435019; doi: https://doi.org/10.1101/2021.03.12.435019

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