Neural substrates of fear conditioning, extinction, and spontaneous recovery in passive avoidance learning: A c-fos study in rats

Huang, Andrew Chih Wei; Shyu, Bai-Chuang; Hsiao, Sigmund; Chen, Jeremy Tsung-Chieh; He, Alan Bo-Han

doi:10.1016/j.bbr.2012.09.024

Cited by 21 publications

(17 citation statements)

References 54 publications

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“…Mice were assessed for learning and memory of conditioned fear, as previously described (Huang et al, 2013), using the Near-Infrared image tracking system (MED Associates, Burlington, VT, USA). On the first day of this three-day test, mice were placed in a sound-attenuating box and allowed to explore for 2 min before three exposures to a 30-s tone of 90 dB (conditioned stimulus; CS), followed by a two-sec scrambled foot shock of 0.6 mA (unconditioned stimulus; US) separated by a random interval.…”

Section: Methodsmentioning

confidence: 99%

Effects of sex and deletion of neuropeptide Y2 receptors from GABAergic neurons on affective and alcohol drinking behaviors in mice

McCall

Sprow

Delpire

et al. 2013

Front. Integr. Neurosci.

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A large literature has demonstrated that neuropeptide Y (NPY) regulates many emotional and reward-related behaviors via its primary receptors, Y1R and Y2R. Classically, NPY actions at postsynaptic Y1R decrease anxiety, depression, and alcohol drinking, while its actions at presynaptic Y2R produce the opposite behavioral phenotypes. However, emerging evidence suggests that activation of Y2R can also produce anxiolysis in a brain region and neurotransmitter system-dependent fashion. Further, numerous human and rodent studies have reported that females display higher levels of anxiety, depression, and alcohol drinking. In this study, we evaluated sex differences and the role of Y2R on GABAergic transmission in these behaviors using a novel transgenic mouse that lacks Y2R specifically in VGAT-expressing neurons (VGAT-Y2R knockout). First, we confirmed our genetic manipulation by demonstrating that Y2R protein expression was decreased and that a Y2R agonist could not alter GABAergic transmission in the extended amygdala, a limbic brain region critically implicated in the regulation of anxiety and alcohol drinking behaviors, using immunofluorescence and slice electrophysiology. Then, we tested male and female VGAT-Y2R knockout mice on a series of behavioral assays for anxiety, depression, fear, anhedonia, and alcohol drinking. We found that females displayed greater basal anxiety, higher levels of ethanol consumption, and faster fear conditioning than males, and that knockout mice exhibited enhanced depressive-like behavior in the forced swim test. Together, these results confirm previous studies that demonstrate higher expression of negative affective and alcohol drinking behaviors in females than males, and they highlight the importance of Y2R function in GABAergic systems in the expression of depressive-like behavior.

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Section: Methodsmentioning

confidence: 99%

Effects of sex and deletion of neuropeptide Y2 receptors from GABAergic neurons on affective and alcohol drinking behaviors in mice

McCall

Sprow

Delpire

et al. 2013

Front. Integr. Neurosci.

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“…nociceptive stimuli) [7]. Although the exact neural substrates and their roles involved in expression of CR are not known, several brain areas are suggested to play a role, including the amygdala, hippocampus and prefrontal cortex [9]–[13]. Strain differences in Pavlovian fear conditioning are reported [14], [15], but only few strains have been compared directly.…”

Section: Introductionmentioning

confidence: 99%

Nociception and Conditioned Fear in Rats: Strains Matter

et al. 2013

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When using rats in pain research, strain-related differences in outcomes of tests for pain and nociception are acknowledged. However, very little is known about the specific characteristics of these strain differences. In this study four phylogenetically distant inbred rat strains, i.e. Wistar Kyoto (WKY), Fawn Hooded (FH), Brown Norway (BN) and Lewis (LE), were investigated in different tests related to pain and nociception. During Pavlovian fear conditioning, the LE and WKY showed a significantly longer duration of freezing behaviour than the FH and BN. Additionally, differences in c-Fos expression in subregions of the prefrontal cortex and amygdala between rat strains during retrieval and expression of conditioned fear were found. For example, the BN did not show recruitment of the basolateral amygdala, whereas the WKY, FH and LE did. During the hot plate test, the WKY and LE showed a lower thermal threshold compared to the BN and FH. In a follow-up experiment, the two most contrasting strains regarding behaviour during the hot plate test and Pavlovian fear conditioning (i.e. FH and WKY) were selected and the hot plate test, Von Frey test and somatosensory-evoked potential (SEP) were investigated. During the Von Frey test, the WKY showed a lower mechanical threshold compared to the FH. When measuring the SEP, the FH appeared to be less reactive to increasing stimulus intensities when considering both peak amplitudes and latencies. Altogether, the combined results indicate various differences between rat strains in Pavlovian fear conditioning, nociception related behaviours and nociceptive processing. These findings demonstrate the necessity of using multiple rat strains when using tests including noxious stimuli and suggest that the choice of rat strains should be considered. When selecting a strain for a particular study it should be considered how this strain behaves during the tests used in that study.

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“…Indeed, the previously reported enhancement of contextual fear conditioning could be partially explained by reinforcement enhancement, that is, NIC-induced enhancement of the ability of the shock-paired cue to drive freezing behavior. It is also unlikely that the current results reflect NIC-induced disruption of extinction of CPA; avoidance of a LiCl- 18 or FS-paired chamber 24 does not significantly extinguish in 3 days. In the present study, NIC enhanced avoidance above baseline levels, while NIC given during fear extinction training does not enhance freezing above baseline.…”

Section: Discussionmentioning

confidence: 88%

Nicotine Enhances Footshock- and Lithium Chloride-Conditioned Place Avoidance in Male Rats

Buffalari

Mollica

Smith

et al. 2016

NICTOB

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Introduction: Numerous studies have shown that nicotine (NIC) can enhance the reinforcing effects of non-NIC stimuli through a nonassociative mechanism. To date, it is unclear whether NIC reinforcement enhancement serves to increase behaviors motivated by rewarding stimuli only, or whether NIC potentiates behavior motivated by all stimuli, regardless of valence. Methods: The current study used a place conditioning procedure to examine whether acute NIC injection modulates avoidance of an environment previously associated with an aversive stimulus. Separate groups of rats underwent place conditioning using either lithium chloride (125 mg/kg/ml, i.p.) or footshock (0.75 mA) as the aversive stimulus. Other rats served as nonconditioned controls. The magnitude of place avoidance was assessed after acute NIC (0.1 or 0.4 mg/kg/ml, s.c.) or saline. Results: Rats avoided chambers previously paired with either lithium chloride or footshock, and conditioned place avoidance was significantly enhanced by NIC pre-treatment.Conclusions: These results demonstrate that the ability of NIC to enhance motivated behavior extends to behaviors elicited by aversive stimuli, evidence that NIC affects behavior motivated by a broader range of stimuli than previously appreciated. Implications: The current study examined whether the reinforcement enhancement properties of NIC apply to aversive stimuli by testing NIC enhancement of conditioned place avoidance in rats. The results demonstrate that NIC enhances the motivational impact of these distinct aversive stimuli, providing novel evidence that NIC affects behavior motivated by a broader range of stimuli than has previously been demonstrated.

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Neural substrates of fear conditioning, extinction, and spontaneous recovery in passive avoidance learning: A c-fos study in rats

Cited by 21 publications

References 54 publications

Effects of sex and deletion of neuropeptide Y2 receptors from GABAergic neurons on affective and alcohol drinking behaviors in mice

Effects of sex and deletion of neuropeptide Y2 receptors from GABAergic neurons on affective and alcohol drinking behaviors in mice

Nociception and Conditioned Fear in Rats: Strains Matter

Nicotine Enhances Footshock- and Lithium Chloride-Conditioned Place Avoidance in Male Rats

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