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Beta traveling waves in monkey frontal and parietal areas encode recent reward history

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Listed:
  • Erfan Zabeh

    (Columbia University
    Columbia University)

  • Nicholas C. Foley

    (Columbia University)

  • Joshua Jacobs

    (Columbia University
    Columbia University)

  • Jacqueline P. Gottlieb

    (Columbia University
    Columbia University
    Columbia University)

Abstract

Brain function depends on neural communication, but the mechanisms of this communication are not well understood. Recent studies suggest that one form of neural communication is through traveling waves (TWs)—patterns of neural oscillations that propagate within and between brain areas. We show that TWs are robust in microarray recordings in frontal and parietal cortex and encode recent reward history. Two adult male monkeys made saccades to obtain probabilistic rewards and were sensitive to the (statistically irrelevant) reward on the previous trial. TWs in frontal and parietal areas were stronger in trials that followed a prior reward versus a lack of reward and, in the frontal lobe, correlated with the monkeys’ behavioral sensitivity to the prior reward. The findings suggest that neural communication mediated by TWs within the frontal and parietal lobes contribute to maintaining information about recent reward history and mediating the impact of this history on the monkeys’ expectations.

Suggested Citation

  • Erfan Zabeh & Nicholas C. Foley & Joshua Jacobs & Jacqueline P. Gottlieb, 2023. "Beta traveling waves in monkey frontal and parietal areas encode recent reward history," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-41125-9
    DOI: 10.1038/s41467-023-41125-9
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    References listed on IDEAS

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    1. Evgueniy V. Lubenov & Athanassios G. Siapas, 2009. "Hippocampal theta oscillations are travelling waves," Nature, Nature, vol. 459(7246), pages 534-539, May.
    2. Kazutaka Takahashi & Sanggyun Kim & Todd P. Coleman & Kevin A. Brown & Aaron J. Suminski & Matthew D. Best & Nicholas G. Hatsopoulos, 2015. "Large-scale spatiotemporal spike patterning consistent with wave propagation in motor cortex," Nature Communications, Nature, vol. 6(1), pages 1-11, November.
    3. Pieter R. Roelfsema & Andreas K. Engel & Peter König & Wolf Singer, 1997. "Visuomotor integration is associated with zero time-lag synchronization among cortical areas," Nature, Nature, vol. 385(6612), pages 157-161, January.
    4. Jonathan K. Kleen & Jason E. Chung & Kristin K. Sellers & Jenny Zhou & Michael Triplett & Kye Lee & Angela Tooker & Razi Haque & Edward F. Chang, 2021. "Bidirectional propagation of low frequency oscillations over the human hippocampal surface," Nature Communications, Nature, vol. 12(1), pages 1-10, December.
    5. Zachary W. Davis & Lyle Muller & Julio Martinez-Trujillo & Terrence Sejnowski & John H. Reynolds, 2020. "Spontaneous travelling cortical waves gate perception in behaving primates," Nature, Nature, vol. 587(7834), pages 432-436, November.
    6. Charles W. Dickey & Anna Sargsyan & Joseph R. Madsen & Emad N. Eskandar & Sydney S. Cash & Eric Halgren, 2021. "Travelling spindles create necessary conditions for spike-timing-dependent plasticity in humans," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
    7. Daria Osipova & Dora Hermes & Ole Jensen, 2008. "Gamma Power Is Phase-Locked to Posterior Alpha Activity," PLOS ONE, Public Library of Science, vol. 3(12), pages 1-7, December.
    8. Athena Akrami & Charles D. Kopec & Mathew E. Diamond & Carlos D. Brody, 2018. "Posterior parietal cortex represents sensory history and mediates its effects on behaviour," Nature, Nature, vol. 554(7692), pages 368-372, February.
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