Potentiation of cholinergic and corticofugal inputs to the lateral amygdala in threat learning
Summary: The amygdala, cholinergic basal forebrain, and higher-order auditory cortex (HO-AC) regulate brain-wide plasticity underlying auditory threat learning. Here, we perform multi-regional extracellular recordings and optical measurements of acetylcholine (ACh) release to characterize the develo...
| Main Authors: | , , , |
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| Format: | Article |
| Language: | English |
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Elsevier
2023-10-01
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| Series: | Cell Reports |
| Subjects: | |
| Online Access: | http://www.sciencedirect.com/science/article/pii/S2211124723011798 |
| _version_ | 1797674926783594496 |
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| author | Meenakshi M. Asokan Yurika Watanabe Eyal Y. Kimchi Daniel B. Polley |
| author_facet | Meenakshi M. Asokan Yurika Watanabe Eyal Y. Kimchi Daniel B. Polley |
| author_sort | Meenakshi M. Asokan |
| collection | DOAJ |
| description | Summary: The amygdala, cholinergic basal forebrain, and higher-order auditory cortex (HO-AC) regulate brain-wide plasticity underlying auditory threat learning. Here, we perform multi-regional extracellular recordings and optical measurements of acetylcholine (ACh) release to characterize the development of discriminative plasticity within and between these brain regions as mice acquire and recall auditory threat memories. Spiking responses are potentiated for sounds paired with shock (CS+) in the lateral amygdala (LA) and optogenetically identified corticoamygdalar projection neurons, although not in neighboring HO-AC units. Spike- or optogenetically triggered local field potentials reveal enhanced corticofugal—but not corticopetal—functional coupling between HO-AC and LA during threat memory recall that is correlated with pupil-indexed memory strength. We also note robust sound-evoked ACh release that rapidly potentiates for the CS+ in LA but habituates across sessions in HO-AC. These findings highlight a distributed and cooperative plasticity in LA inputs as mice learn to reappraise neutral stimuli as possible threats. |
| first_indexed | 2024-03-11T22:07:15Z |
| format | Article |
| id | doaj.art-c494319a47f24dd5872133a4378bb077 |
| institution | Directory Open Access Journal |
| issn | 2211-1247 |
| language | English |
| last_indexed | 2024-03-11T22:07:15Z |
| publishDate | 2023-10-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Cell Reports |
| spelling | doaj.art-c494319a47f24dd5872133a4378bb0772023-09-25T04:12:10ZengElsevierCell Reports2211-12472023-10-014210113167Potentiation of cholinergic and corticofugal inputs to the lateral amygdala in threat learningMeenakshi M. Asokan0Yurika Watanabe1Eyal Y. Kimchi2Daniel B. Polley3Eaton-Peabody Laboratories, Massachusetts Eye and Ear, Boston, MA 02114, USA; Division of Medical Sciences, Harvard Medical School, Boston, MA 02114, USA; Corresponding authorEaton-Peabody Laboratories, Massachusetts Eye and Ear, Boston, MA 02114, USAEaton-Peabody Laboratories, Massachusetts Eye and Ear, Boston, MA 02114, USA; Department of Neurology, Massachusetts General Hospital, Boston, MA 02114, USAEaton-Peabody Laboratories, Massachusetts Eye and Ear, Boston, MA 02114, USA; Division of Medical Sciences, Harvard Medical School, Boston, MA 02114, USA; Department of Otolaryngology – Head and Neck Surgery, Harvard Medical School, Boston, MA 02114, USASummary: The amygdala, cholinergic basal forebrain, and higher-order auditory cortex (HO-AC) regulate brain-wide plasticity underlying auditory threat learning. Here, we perform multi-regional extracellular recordings and optical measurements of acetylcholine (ACh) release to characterize the development of discriminative plasticity within and between these brain regions as mice acquire and recall auditory threat memories. Spiking responses are potentiated for sounds paired with shock (CS+) in the lateral amygdala (LA) and optogenetically identified corticoamygdalar projection neurons, although not in neighboring HO-AC units. Spike- or optogenetically triggered local field potentials reveal enhanced corticofugal—but not corticopetal—functional coupling between HO-AC and LA during threat memory recall that is correlated with pupil-indexed memory strength. We also note robust sound-evoked ACh release that rapidly potentiates for the CS+ in LA but habituates across sessions in HO-AC. These findings highlight a distributed and cooperative plasticity in LA inputs as mice learn to reappraise neutral stimuli as possible threats.http://www.sciencedirect.com/science/article/pii/S2211124723011798CP: Neuroscience |
| spellingShingle | Meenakshi M. Asokan Yurika Watanabe Eyal Y. Kimchi Daniel B. Polley Potentiation of cholinergic and corticofugal inputs to the lateral amygdala in threat learning Cell Reports CP: Neuroscience |
| title | Potentiation of cholinergic and corticofugal inputs to the lateral amygdala in threat learning |
| title_full | Potentiation of cholinergic and corticofugal inputs to the lateral amygdala in threat learning |
| title_fullStr | Potentiation of cholinergic and corticofugal inputs to the lateral amygdala in threat learning |
| title_full_unstemmed | Potentiation of cholinergic and corticofugal inputs to the lateral amygdala in threat learning |
| title_short | Potentiation of cholinergic and corticofugal inputs to the lateral amygdala in threat learning |
| title_sort | potentiation of cholinergic and corticofugal inputs to the lateral amygdala in threat learning |
| topic | CP: Neuroscience |
| url | http://www.sciencedirect.com/science/article/pii/S2211124723011798 |
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