Multimodal encoding of novelty, reward, and learning in the primate nucleus basalis of meynert

Clarissa Martinez-Rubio, Angelique C. Paulk, Eric J. McDonald, Alik S. Widge, Emad N. Eskandar

Research output: Contribution to journalArticlepeer-review

5 Scopus citations

Abstract

Associative learning is crucial for daily function, involving a complex network of brain regions. One region, the nucleus basalis of Meynert (NBM), is a highly interconnected, largely cholinergic structure implicated in multiple aspects of learning. We show that single neurons in the NBM of nonhuman primates (NHPs; n=2 males; Macaca mulatta) encode learning a new association through spike rate modulation. However, the power of low-frequency local field potential (LFP) oscillations decreases in response to novel, not-yet-learned stimuli but then increase as learning progresses. Both NBM and the dorsolateral prefrontal cortex encode confidence in novel associations by increasing low-and high-frequency LFP power in anticipation of expected rewards. Finally, NBM high-frequency power dynamics are anticorrelated with spike rate modulations. Therefore, novelty, learning, and reward anticipation are separately encoded through differentiable NBM signals. By signaling both the need to learn and confidence in newly acquired associations, NBM may play a key role in coordinating cortical activity throughout the learning process.

Original languageEnglish (US)
Pages (from-to)1942-1958
Number of pages17
JournalJournal of Neuroscience
Volume38
Issue number8
DOIs
StatePublished - Feb 21 2018
Externally publishedYes

Bibliographical note

Funding Information:
This work was supported by the National Institutes of Health (Grant EY017658 to C.M.-R. and postdoctoral fellowship NS083208 and grants MH086400, DA026297, and EY017658 to E.N.E.), the Epilepsy Foundation (E.N.E.). Analysis of the data was supported in part by the Defense Advanced Research Projects Agency (DARPA) under Cooperative Agreement Number W911NF-14-2-0045 issued by ARO contracting office in support of DARPA’s SUBNETS Program. The views, opinions, and/or findings expressed are those of the author and should not be interpreted as representing the official views or policies of the Department of Defense or the U.S. Government.

Funding Information:
This work was supported by the National Institutes of Health (Grant EY017658 to C.M.-R. and postdoctoral fellowshipNS083208andgrantsMH086400,DA026297,andEY017658toE.N.E.),theEpilepsyFoundation(E.N.E.). Analysis of the data was supported in part by the Defense Advanced Research Projects Agency (DARPA) under Cooperative Agreement Number W911NF-14-2-0045 issued by ARO contracting office in support of DARPA’s SUBNETS Program. The views, opinions, and/or findings expressed are those of the author and should not be interpreted as representing the official views or policies of the Department of Defense or the U.S. Government. The authors declare no competing financial interests. *C.M.-R. and A.C.P. contributed equally to this work. †A.S.W. and E.N.E. are cosenior authors.

Publisher Copyright:
© 2018 the authors.

Keywords

  • Encoding cognitive state
  • Learning
  • Local field potential
  • Nucleus basalis of Meynert
  • Single neuron activity

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