Literature DB >> 32945260

Acetylcholine is released in the basolateral amygdala in response to predictors of reward and enhances the learning of cue-reward contingency.

Richard B Crouse1,2, Kristen Kim1,2, Hannah M Batchelor1,2, Eric M Girardi1, Rufina Kamaletdinova1,3, Justin Chan1, Prithviraj Rajebhosale4,5, Steven T Pittenger1, Lorna W Role5, David A Talmage6, Miao Jing7, Yulong Li8,9,10, Xiao-Bing Gao11, Yann S Mineur1, Marina R Picciotto1,2.   

Abstract

The basolateral amygdala (BLA) is critical for associating initially neutral cues with appetitive and aversive stimuli and receives dense neuromodulatory acetylcholine (ACh) projections. We measured BLA ACh signaling and activity of neurons expressing CaMKIIα (a marker for glutamatergic principal cells) in mice during cue-reward learning using a fluorescent ACh sensor and calcium indicators. We found that ACh levels and nucleus basalis of Meynert (NBM) cholinergic terminal activity in the BLA (NBM-BLA) increased sharply in response to reward-related events and shifted as mice learned the cue-reward contingency. BLA CaMKIIα neuron activity followed reward retrieval and moved to the reward-predictive cue after task acquisition. Optical stimulation of cholinergic NBM-BLA terminal fibers led to a quicker acquisition of the cue-reward contingency. These results indicate BLA ACh signaling carries important information about salient events in cue-reward learning and provides a framework for understanding how ACh signaling contributes to shaping BLA responses to emotional stimuli.

Entities:  

Keywords:  GCaMP; cholinergic; fiber photometry; grabach3.0; mouse; neuroscience; optogenetics; reward learning

Mesh:

Substances:

Year:  2020        PMID: 32945260      PMCID: PMC7529459          DOI: 10.7554/eLife.57335

Source DB:  PubMed          Journal:  Elife        ISSN: 2050-084X            Impact factor:   8.140


  59 in total

1.  Involvement of the amygdala in stimulus-reward associations: interaction with the ventral striatum.

Authors:  M Cador; T W Robbins; B J Everitt
Journal:  Neuroscience       Date:  1989       Impact factor: 3.590

2.  Amygdala neurons differentially encode motivation and reinforcement.

Authors:  Kay M Tye; Patricia H Janak
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3.  Rapid strengthening of thalamo-amygdala synapses mediates cue-reward learning.

Authors:  Kay M Tye; Garret D Stuber; Bram de Ridder; Antonello Bonci; Patricia H Janak
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Authors:  Cheng-Hang Liu; Jason E Coleman; Heydar Davoudi; Kechen Zhang; Marshall G Hussain Shuler
Journal:  Curr Biol       Date:  2015-05-21       Impact factor: 10.834

Review 5.  Dual-transmitter systems regulating arousal, attention, learning and memory.

Authors:  Sherie Ma; Balázs Hangya; Christopher S Leonard; William Wisden; Andrew L Gundlach
Journal:  Neurosci Biobehav Rev       Date:  2017-07-27       Impact factor: 8.989

6.  High-performance calcium sensors for imaging activity in neuronal populations and microcompartments.

Authors:  Hod Dana; Yi Sun; Boaz Mohar; Brad K Hulse; Aaron M Kerlin; Jeremy P Hasseman; Getahun Tsegaye; Arthur Tsang; Allan Wong; Ronak Patel; John J Macklin; Yang Chen; Arthur Konnerth; Vivek Jayaraman; Loren L Looger; Eric R Schreiter; Karel Svoboda; Douglas S Kim
Journal:  Nat Methods       Date:  2019-06-17       Impact factor: 28.547

7.  Visual responses of neurons in the dorsolateral amygdala of the alert monkey.

Authors:  M K Sanghera; E T Rolls; A Roper-Hall
Journal:  Exp Neurol       Date:  1979-03       Impact factor: 5.330

8.  Prefrontal acetylcholine release controls cue detection on multiple timescales.

Authors:  Vinay Parikh; Rouba Kozak; Vicente Martinez; Martin Sarter
Journal:  Neuron       Date:  2007-10-04       Impact factor: 17.173

9.  Corelease of acetylcholine and GABA from cholinergic forebrain neurons.

Authors:  Arpiar Saunders; Adam J Granger; Bernardo L Sabatini
Journal:  Elife       Date:  2015-02-27       Impact factor: 8.140

10.  State-specific gating of salient cues by midbrain dopaminergic input to basal amygdala.

Authors:  Andrew Lutas; Hakan Kucukdereli; Osama Alturkistani; Crista Carty; Arthur U Sugden; Kayla Fernando; Veronica Diaz; Vanessa Flores-Maldonado; Mark L Andermann
Journal:  Nat Neurosci       Date:  2019-10-14       Impact factor: 24.884

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1.  Target-specific control of olfactory bulb periglomerular cells by GABAergic and cholinergic basal forebrain inputs.

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Journal:  Elife       Date:  2022-02-28       Impact factor: 8.140

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

Authors:  Blaise Robert; Eyal Y Kimchi; Yurika Watanabe; Tatenda Chakoma; Miao Jing; Yulong Li; Daniel B Polley
Journal:  Elife       Date:  2021-11-25       Impact factor: 8.140

3.  ACh signaling modulates activity of the GABAergic signaling network in the basolateral amygdala and behavior in stress-relevant paradigms.

Authors:  Yann S Mineur; Tenna N Mose; Kathrine Lefoli Maibom; Steven T Pittenger; Alexa R Soares; Hao Wu; Seth R Taylor; Yaqing Huang; Marina R Picciotto
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4.  Global and subtype-specific modulation of cortical inhibitory neurons regulated by acetylcholine during motor learning.

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5.  Acetylcholine is released in the basolateral amygdala in response to predictors of reward and enhances the learning of cue-reward contingency.

Authors:  Richard B Crouse; Kristen Kim; Hannah M Batchelor; Eric M Girardi; Rufina Kamaletdinova; Justin Chan; Prithviraj Rajebhosale; Steven T Pittenger; Lorna W Role; David A Talmage; Miao Jing; Yulong Li; Xiao-Bing Gao; Yann S Mineur; Marina R Picciotto
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6.  Cholinergic neurotransmission in the basolateral amygdala during cued fear extinction.

Authors:  Devin M Kellis; Kris Ford Kaigler; Eric Witherspoon; Jim R Fadel; Marlene A Wilson
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Review 7.  Amygdala-cortical collaboration in reward learning and decision making.

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8.  A bidirectional corticoamygdala circuit for the encoding and retrieval of detailed reward memories.

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Journal:  Elife       Date:  2021-06-18       Impact factor: 8.140

9.  Chronic Ethanol Exposure Potentiates Cholinergic Neurotransmission in the Basolateral Amygdala.

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