Cholinergic neurotransmission in the basolateral amygdala during cued fear extinction

Kellis, Devin M.; Kaigler, Kris F.; Witherspoon, Eric; Fadel, Jim R.; Wilson, Marlene A.

doi:10.1016/j.ynstr.2020.100279

Cited by 26 publications

(52 citation statements)

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“…Experimental procedures were adapted from our previous protocols in males demonstrating individual differences in fear extinction ( Sharko et al, 2017 ; Kellis et al, 2020 ; Figure 1A ). For fear acquisition on day 1, rats were placed in a shock box (Context A) within a sound-attenuating chamber containing a ventilation fan, speaker, and a house light (CleverSys, Inc., Reston, VA, United States), with a microphone for recording USVs below the box (Noldus Information Technology, Leesburg, VA, United States).…”

Section: Methodsmentioning

confidence: 99%

“…Percent freezing was calculated as the percent of time spent freezing in each 1-min bin that included each tone and the following inter-tone interval. As described previously for males ( Sharko et al, 2017 ; Kellis et al, 2020 ), females were divided into ER (high freezing) and EC (low freezing) groups using a median split of average freezing during the last 10 min (10 tones) of extinction learning.…”

Section: Methodsmentioning

confidence: 99%

“…Extinction resistant and EC groups were determined using a median split of freezing during the last 10 tones of extinction learning (as described previously for males) ( Sharko et al, 2017 ; Kellis et al, 2020 ). Freezing behavior during each trial was recorded and calculated by FreezeScan software as percent freezing per 1 min time bin.…”

Section: Methodsmentioning

confidence: 99%

“…Our lab and others have used preclinical Pavlovian fear learning and extinction models to show that like humans, rodents demonstrate varied levels of fear extinction ( Milad and Quirk, 2002 ; Bush et al, 2007 ; Galatzer-Levy et al, 2013 ; Holmes and Singewald, 2013 ; Shumake et al, 2014 ; Gruene et al, 2015b ; Sharko et al, 2017 ; Monfils et al, 2019 ; Kellis et al, 2020 ). In these models, rodents are exposed to an unconditioned aversive stimulus (US), such as a foot shock, in conjunction with a neutral conditional stimulus (CS), such as a tone.…”

Section: Introductionmentioning

confidence: 99%

“…To address this gap, the present study examined freezing and other behaviors, as well as both 22 and 50 kHz USVs, in a sample of female rats during a fear conditioning and cued fear extinction paradigm. Based on the reviewed literature and our previous findings in Long–Evans male rats ( Sharko et al, 2017 ; Kellis et al, 2020 ), we hypothesized that like males, female rats would exhibit individual differences in fear extinction responses, presenting either extinction competent (EC) or extinction resistant (ER) phenotypes. We predicted these individual differences in fear might be observed not only in freezing, but also in more affective differences in 22 and 50 kHz USVs and/or other behaviors such as rearing, grooming, or darting.…”

Section: Introductionmentioning

confidence: 99%

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Individual Differences in Conditioned Fear and Extinction in Female Rats

Tryon

Kellis

Kaigler

et al. 2021

Front. Behav. Neurosci.

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The inability to extinguish a traumatic memory is a key aspect of post-traumatic stress disorder (PTSD). While PTSD affects 10–20% of individuals who experience a trauma, women are particularly susceptible to developing the disorder. Despite this notable female vulnerability, few studies have investigated this particular resistance to fear extinction observed in females. Similar to humans, rodent models of Pavlovian fear learning and extinction show a wide range of individual differences in fear learning and extinction, although female rodents are considerably understudied. Therefore, the present study examined individual differences in fear responses, including freezing behavior and ultrasonic vocalizations (USVs), of female Long–Evans rats during acquisition of fear conditioning and cued fear extinction. Similar to prior studies in males, female rats displayed individual variation in freezing during cued fear extinction and were divided into extinction competent (EC) and extinction resistant (ER) phenotypes. Differences in freezing between ER and EC females were accompanied by shifts in rearing during extinction, but no darting was seen in any trial. Freezing behavior during fear learning did not differ between the EC and ER females. Vocalizations emitted in the 22 and 50 kHz ranges during fear learning and extinction were also examined. Unlike vocalizations seen in previous studies in males, very few 22 kHz distress vocalizations were emitted by female rats during fear acquisition and extinction, with no difference between ER and EC groups. Interestingly, all female rats produced significant levels of 50 kHz USVs, and EC females emitted significantly more 50 kHz USVs than ER rats. This difference in 50 kHz USVs was most apparent during initial exposure to the testing environment. These results suggest that like males, female rodents show individual differences in both freezing and USVs during fear extinction, although females appear to vocalize more in the 50 kHz range, especially during initial periods of exposure to the testing environment, and emit very few of the 22 kHz distress calls that are typically observed in males during fear learning or extinction paradigms. Overall, these findings show that female rodents display fear behavior repertoires divergent from males.

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Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

Individual Differences in Conditioned Fear and Extinction in Female Rats

Tryon

Kellis

Kaigler

et al. 2021

Front. Behav. Neurosci.

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Functional neuroanatomy of basal forebrain projections to the basolateral amygdala: Transmitters, receptors, and neuronal subpopulations

McDonald

2024

J of Neuroscience Research

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The projections of the basal forebrain (BF) to the hippocampus and neocortex have been extensively studied and shown to be important for higher cognitive functions, including attention, learning, and memory. Much less is known about the BF projections to the basolateral nuclear complex of the amygdala (BNC), although the cholinergic innervation of this region by the BF is actually far more robust than that of cortical areas. This review will focus on light and electron microscopic tract‐tracing and immunohistochemical (IHC) studies, many of which were published in the last decade, that have analyzed the relationship of BF inputs and their receptors to specific neuronal subtypes in the BNC in order to better understand the anatomical substrates of BF‐BNC circuitry. The results indicate that BF inputs to the BNC mainly target the basolateral nucleus of the BNC (BL) and arise from cholinergic, GABAergic, and perhaps glutamatergic BF neurons. Cholinergic inputs mainly target dendrites and spines of pyramidal neurons (PNs) that express muscarinic receptors (MRs). MRs are also expressed by cholinergic axons, as well as cortical and thalamic axons that synapse with PN dendrites and spines. BF GABAergic axons to the BL also express MRs and mainly target BL interneurons that contain parvalbumin. It is suggested that BF‐BL circuitry could be very important for generating rhythmic oscillations known to be critical for emotional learning. BF cholinergic inputs to the BNC might also contribute to memory formation by activating M1 receptors located on PN dendritic shafts and spines that also express NMDA receptors.

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Scopolamine infusion in the basolateral amygdala after saccharin intake induces conditioned taste avoidance in rats

Torres-García,

Rodríguez-Nava,

Alcántara-Rivas

et al. 2024

Psychopharmacology

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Rationale Muscarinic receptor activity in the basolateral amygdala (BLA) is known to be involved in plasticity mechanisms that underlie emotional learning. The BLA is involved in the Attenuation of Neophobia, an incidental taste learning task in which a novel taste becomes familiar and recognized as safe. Objective Here we assessed the role of muscarinic receptor activity in the BLA in incidental taste learning. Methods Young adult male Wistar rats were bilaterally implanted with cannulas aimed at BLA. After recovery, rats were randomly assigned to either vehicle or muscarinic antagonist group, for each experiment. We tested the effect of specific and non-specific muscarinic antagonists administered either 1) 20 min before novel taste presentation; 2) immediately after novel taste presentation; 3) immediately after retrieval (the second taste presentation on Day 5 -S2-) or immediately after the fifth taste presentation on Day 8 (S5). Results Non-specific muscarinic receptor antagonist scopolamine infused prior to novel taste, while not affecting novel taste preference, abolished AN, i.e., the increased preference observed in control animals on the second presentation. When administered after taste consumption, intra-BLA scopolamine not only prevented AN but caused a steep decrease in the taste preference on the second presentation. This scopolamine-induced taste avoidance was not dependent on taste novelty, nor did it generalize to another novel taste. Targeting putative postsynaptic muscarinic receptors with specific M1 or M3 antagonists appeared to produce a partial taste avoidance, while M2 antagonism had no effect. Conclusion These data suggest that if a salient gustatory experience is followed by muscarinic receptors antagonism in the BLA, it will be strongly and persistently avoided in the future. The study also shows that scopolamine is not just an amnesic drug, and its cognitive effects may be highly dependent on the task and the structure involved.

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Cholinergic neurotransmission in the basolateral amygdala during cued fear extinction

Cited by 26 publications

References 93 publications

Individual Differences in Conditioned Fear and Extinction in Female Rats

Individual Differences in Conditioned Fear and Extinction in Female Rats

Functional neuroanatomy of basal forebrain projections to the basolateral amygdala: Transmitters, receptors, and neuronal subpopulations

Scopolamine infusion in the basolateral amygdala after saccharin intake induces conditioned taste avoidance in rats

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