A functional topography within the cholinergic basal forebrain for encoding sensory cues and behavioral reinforcement outcomes.

Blaise Robert, Eyal Y. Kimchi, Yurika Watanabe, Tatenda Chakoma, Miao Jing, Yulong Li, Daniel B. Polley*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

22 Scopus citations

Abstract

Basal forebrain cholinergic neurons (BFCNs) project throughout the cortex to regulate arousal, stimulus salience, plasticity, and learning. Although often treated as a monolithic structure, the basal forebrain features distinct connectivity along its rostrocaudal axis that could impart regional differences in BFCN processing. Here, we performed simultaneous bulk calcium imaging from rostral and caudal BFCNs over a one-month period of variable reinforcement learning in mice. BFCNs in both regions showed equivalently weak responses to unconditioned visual stimuli and anticipated rewards. Rostral BFCNs in the horizontal limb of the diagonal band were more responsive to reward omission, more accurately classified behavioral outcomes, and more closely tracked fluctuations in pupil-indexed global brain state. Caudal tail BFCNs in globus pallidus and substantia innominata were more responsive to unconditioned auditory stimuli, orofacial movements, aversive reinforcement, and showed robust associative plasticity for punishment-predicting cues. These results identify a functional topography that diversifies cholinergic modulatory signals broadcast to downstream brain regions.

Original languageEnglish (US)
Article numbere69514
JournaleLife
Volume10
DOIs
StatePublished - Nov 2021

Funding

These studies were supported by NIH grant DC017078 (DP), The Nancy Lurie Marks Family Foundation (DP), a Herchel Smith Harvard Scholarship (BR), a Fondation Zdenek et Michaela Bakala Scholarship (BR), and NIH grant K08MH116135 (EK).

Keywords

  • Acetylcholine
  • Auditory
  • Basal forebrain
  • Cholinergic
  • Horizontal limb diagonal band
  • Learning
  • Nucleus basalis
  • Punishment
  • Reward
  • Substantia innominata

ASJC Scopus subject areas

  • General Neuroscience
  • General Biochemistry, Genetics and Molecular Biology
  • General Immunology and Microbiology

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