Reward contingency gates selective cholinergic suppression of amygdala neurons
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...
| Main Authors: | , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2024-02-01
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| Series: | eLife |
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| Online Access: | https://elifesciences.org/articles/89093 |
| _version_ | 1797302009155551232 |
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| author | Eyal Y Kimchi Anthony Burgos-Robles Gillian A Matthews Tatenda Chakoma Makenzie Patarino Javier C Weddington Cody Siciliano Wannan Yang Shaun Foutch Renee Simons Ming-fai Fong Miao Jing Yulong Li Daniel B Polley Kay M Tye |
| author_facet | Eyal Y Kimchi Anthony Burgos-Robles Gillian A Matthews Tatenda Chakoma Makenzie Patarino Javier C Weddington Cody Siciliano Wannan Yang Shaun Foutch Renee Simons Ming-fai Fong Miao Jing Yulong Li Daniel B Polley Kay M Tye |
| author_sort | Eyal Y Kimchi |
| collection | DOAJ |
| description | 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. |
| first_indexed | 2024-03-07T23:30:43Z |
| format | Article |
| id | doaj.art-8a7093e4310c45d99114b872c8e6802c |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-03-07T23:30:43Z |
| publishDate | 2024-02-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-8a7093e4310c45d99114b872c8e6802c2024-02-20T15:49:02ZengeLife Sciences Publications LtdeLife2050-084X2024-02-011210.7554/eLife.89093Reward contingency gates selective cholinergic suppression of amygdala neuronsEyal Y Kimchi0https://orcid.org/0000-0003-4327-1102Anthony Burgos-Robles1https://orcid.org/0000-0002-6729-2648Gillian A Matthews2https://orcid.org/0000-0001-6754-0333Tatenda Chakoma3Makenzie Patarino4Javier C Weddington5Cody Siciliano6https://orcid.org/0000-0001-9871-2089Wannan Yang7Shaun Foutch8Renee Simons9Ming-fai Fong10https://orcid.org/0000-0002-2336-4531Miao Jing11Yulong Li12Daniel B Polley13https://orcid.org/0000-0002-5120-2409Kay M Tye14https://orcid.org/0000-0002-2435-0182The Picower Institute for Learning and Memory, Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, United States; Department of Neurology, Northwestern University, Chicago, United StatesThe Picower Institute for Learning and Memory, Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, United States; The Department of Neuroscience, Developmental, and Regenerative Biology, Neuroscience Institute & Brain Health Consortium, University of Texas at San Antonio, San Antonio, United StatesThe Picower Institute for Learning and Memory, Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, United StatesThe Picower Institute for Learning and Memory, Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, United StatesThe Picower Institute for Learning and Memory, Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, United StatesThe Picower Institute for Learning and Memory, Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, United StatesThe Picower Institute for Learning and Memory, Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, United States; Vanderbilt Center for Addiction Research, Department of Pharmacology, Vanderbilt University, Nashville, United StatesThe Picower Institute for Learning and Memory, Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, United StatesThe Picower Institute for Learning and Memory, Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, United StatesThe Picower Institute for Learning and Memory, Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, United StatesThe Picower Institute for Learning and Memory, Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, United States; Coulter Department of Biomedical Engineering, Georgia Tech & Emory University, Atlanta, United StatesChinese Institute for Brain Research, Beijing, ChinaState Key Laboratory of Membrane Biology, Peking University School of Life Sciences; PKUIDG/McGovern Institute for Brain Research; Peking-Tsinghua Center for Life Sciences, Beijing, ChinaEaton-Peabody Laboratories, Massachusetts Eye and Ear, Boston, United States; Department of Otolaryngology – Head and Neck Surgery, Harvard Medical School, Boston, United StatesThe Picower Institute for Learning and Memory, Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, United States; HHMI Investigator, Member of the Kavli Institute for Brain and Mind, and Wylie Vale Professor at the Salk Institute for Biological Studies, La Jolla, United StatesBasal 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.https://elifesciences.org/articles/89093acetylcholineamygdalacortexrewardelectrophysiology |
| spellingShingle | Eyal Y Kimchi Anthony Burgos-Robles Gillian A Matthews Tatenda Chakoma Makenzie Patarino Javier C Weddington Cody Siciliano Wannan Yang Shaun Foutch Renee Simons Ming-fai Fong Miao Jing Yulong Li Daniel B Polley Kay M Tye Reward contingency gates selective cholinergic suppression of amygdala neurons eLife acetylcholine amygdala cortex reward electrophysiology |
| title | Reward contingency gates selective cholinergic suppression of amygdala neurons |
| title_full | Reward contingency gates selective cholinergic suppression of amygdala neurons |
| title_fullStr | Reward contingency gates selective cholinergic suppression of amygdala neurons |
| title_full_unstemmed | Reward contingency gates selective cholinergic suppression of amygdala neurons |
| title_short | Reward contingency gates selective cholinergic suppression of amygdala neurons |
| title_sort | reward contingency gates selective cholinergic suppression of amygdala neurons |
| topic | acetylcholine amygdala cortex reward electrophysiology |
| url | https://elifesciences.org/articles/89093 |
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