Reward contingency gates selective cholinergic suppression of amygdala neurons

Author:

Kimchi Eyal Y12ORCID,Burgos-Robles Anthony13ORCID,Matthews Gillian A1ORCID,Chakoma Tatenda1,Patarino Makenzie1,Weddington Javier C1,Siciliano Cody14ORCID,Yang Wannan1,Foutch Shaun1,Simons Renee1,Fong Ming-fai15ORCID,Jing Miao6,Li Yulong7,Polley Daniel B89ORCID,Tye Kay M110ORCID

Affiliation:

1. The Picower Institute for Learning and Memory, Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology

2. Department of Neurology, Northwestern University

3. The Department of Neuroscience, Developmental, and Regenerative Biology, Neuroscience Institute & Brain Health Consortium, University of Texas at San Antonio

4. Vanderbilt Center for Addiction Research, Department of Pharmacology, Vanderbilt University

5. Coulter Department of Biomedical Engineering, Georgia Tech & Emory University

6. Chinese Institute for Brain Research

7. State Key Laboratory of Membrane Biology, Peking University School of Life Sciences; PKUIDG/McGovern Institute for Brain Research; Peking-Tsinghua Center for Life Sciences

8. Eaton-Peabody Laboratories, Massachusetts Eye and Ear

9. Department of Otolaryngology – Head and Neck Surgery, Harvard Medical School

10. HHMI Investigator, Member of the Kavli Institute for Brain and Mind, and Wylie Vale Professor at the Salk Institute for Biological Studies

Abstract

Basal forebrain cholinergic neurons modulate how organisms process and respond to environmental stimuli through impacts on arousal, attention, and memory. It is unknown, however, whether basal forebrain cholinergic neurons are directly involved in conditioned behavior, independent of secondary roles in the processing of external stimuli. Using fluorescent imaging, we found that cholinergic neurons are active during behavioral responding for a reward – even prior to reward delivery and in the absence of discrete stimuli. Photostimulation of basal forebrain cholinergic neurons, or their terminals in the basolateral amygdala (BLA), selectively promoted conditioned responding (licking), but not unconditioned behavior nor innate motor outputs. In vivo electrophysiological recordings during cholinergic photostimulation revealed reward-contingency-dependent suppression of BLA neural activity, but not prefrontal cortex. Finally, ex vivo experiments demonstrated that photostimulation of cholinergic terminals suppressed BLA projection neuron activity via monosynaptic muscarinic receptor signaling, while also facilitating firing in BLA GABAergic interneurons. Taken together, we show that the neural and behavioral effects of basal forebrain cholinergic activation are modulated by reward contingency in a target-specific manner.

Funder

NIH Office of the Director

Howard Hughes Medical Institute

Nancy Lurie Marks Family Foundation

JPB Foundation

New York Stem Cell Foundation

Kavli Institute for Brain and Mind, University of California, San Diego

Publisher

eLife Sciences Publications, Ltd

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