Coordinated acetylcholine release in prefrontal cortex and hippocampus is associated with arousal and reward on distinct timescales

Leonor M Teles Grilo Ruivo, Keeley Baker, Matthew Conway, Peter Kinsley, Gary Gilmour, Keith Phillips, John T R Isaac, John Lowry, Jack Mellor

Research output: Contribution to journalArticle (Academic Journal)

40 Citations (Scopus)
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Abstract

Cholinergic neurotransmission throughout the neocortex and hippocampus regulates arousal, learning and attention. However, owing to the poorly characterized timing and location of acetylcholine release, its detailed behavioral functions remain unclear. Using electrochemical biosensors chronically implanted in mice we made continuous measurements of the spatiotemporal dynamics of acetylcholine release across multiple behavioral states. We found tonic levels of acetylcholine release were coordinated between the prefrontal cortex and hippocampus and maximal during training on a rewarded working memory task. Tonic release also increased during REM sleep but was contingent on subsequent wakefulness. In contrast, coordinated phasic acetylcholine release occurred only during the memory task and was strongly localized to reward delivery areas without being contingent on trial outcome. These results show that coordinated acetylcholine release between the prefrontal cortex and hippocampus is associated with reward and arousal on distinct timescales, providing dual mechanisms to support learned behavior acquisition during cognitive task performance.
Original languageEnglish
Pages (from-to)905–917
Number of pages13
JournalCell Reports
Volume18
Issue number4
Early online date24 Jan 2017
DOIs
Publication statusPublished - 24 Jan 2017

Bibliographical note

26 December 2016

Keywords

  • acetylcholine
  • hippocampus
  • prefrontal cortex
  • biosensor

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    Teles Grilo Ruivo, L. M., Baker, K., Conway, M., Kinsley, P., Gilmour, G., Phillips, K., Isaac, J. T. R., Lowry, J., & Mellor, J. (2017). Coordinated acetylcholine release in prefrontal cortex and hippocampus is associated with arousal and reward on distinct timescales. Cell Reports, 18(4), 905–917. https://doi.org/10.1016/j.celrep.2016.12.085