The amygdala encodes specific sensory features of an aversive reinforcer

Dębiec, Jacek; Díaz-Mataix, Lorenzo; Bush, David E.; Doyère, Valérie; LeDoux, Joseph E.

doi:10.1038/nn.2520

Cited by 87 publications

(108 citation statements)

References 12 publications

(12 reference statements)

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“…2C). This pattern of results demonstrates that two distinct stimuli separately paired with the same US within the same training session can undergo reconsolidation independently of each other, thus confirming the high selectivity of the reconsolidation process we reported previously in our earlier studies using a similar dual threat conditioning protocol (Doyère et al 2007;Debiec et al 2010;Diaz-Mataix et al 2011). More importantly, in this study we demonstrate that this high selectivity can be lost when the stimuli have been conditioned together as a compound stimulus.…”

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confidence: 90%

“…Using Pavlovian threat conditioning in rats and pharmacological manipulations in the LA, we have previously shown that reconsolidation processes are stimulus selective (Debiec et al 2006(Debiec et al , 2010Doyère et al 2007;Diaz-Mataix et al 2011). In one of these studies, we used a dual auditory threat conditioning protocol in which two distinct acoustic CSs were each paired in separate trials with the same electric footshock US (Doyère et al 2007).…”

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confidence: 99%

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The selectivity of aversive memory reconsolidation and extinction processes depends on the initial encoding of the Pavlovian association

Dębiec¹,

Díaz-Mataix²,

Bush³

et al. 2013

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In reconsolidation studies, memories are typically retrieved by an exposure to a single conditioned stimulus (CS). We have previously demonstrated that reconsolidation processes are CS-selective, suggesting that memories retrieved by the CS exposure are discrete and reconsolidate separately. Here, using a compound stimulus in which two distinct CSs are concomitantly paired with the same aversive unconditioned stimulus (US), we show in rats that reexposure to one of the components of the compound CS triggers extinction or reconsolidation of the other component. This suggests that the original training conditions play a critical role in memory retrieval and reconsolidation.

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confidence: 90%

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confidence: 99%

The selectivity of aversive memory reconsolidation and extinction processes depends on the initial encoding of the Pavlovian association

Dębiec¹,

Díaz-Mataix²,

Bush³

et al. 2013

Learn. Mem.

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“…Pups' brains were removed and processed for autoradiography. Areas of interest were the amygdala, a key structure for FC (10), and olfactory structures (20). Significant differences were found throughout amygdala nuclei: lateral (LA) (Fig.…”

Section: Amygdala and Olfactory Autoradiography Of Mother-to-infantmentioning

confidence: 99%

“…Most of what we know about fear learning comes from studies using fear conditioning (FC) (10). In FC, a neutral sensory cue [conditioned stimulus (CS)] is paired with a noxious event [unconditioned stimulus (US)].…”

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confidence: 99%

“…In FC, a neutral sensory cue [conditioned stimulus (CS)] is paired with a noxious event [unconditioned stimulus (US)]. Animal studies indicate that the amygdala's lateral and basal nuclei (LBA) play an important role in FC (10). However, FC in infant rats is naturally attenuated until postnatal day (PND) 10 due to low levels of the stress hormone corticosterone (CORT) during the stress hyporesponsive period (11)(12)(13)(14)(15).…”

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Intergenerational transmission of emotional trauma through amygdala-dependent mother-to-infant transfer of specific fear

Dębiec

Sullivan

2014

Proc. Natl. Acad. Sci. U.S.A.

142

115

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Emotional trauma is transmitted across generations. For example, children witnessing their parent expressing fear to specific sounds or images begin to express fear to those cues. Within normal range, this is adaptive, although pathological fear, such as occurs in posttraumatic stress disorder or specific phobias, is also socially transmitted to children and is thus of clinical concern. Here, using a rodent model, we report a mother-to-infant transfer of fear to a novel peppermint odor, which is dependent on the mother expressing fear to that smell in pups' presence. Examination of pups' neural activity using c-Fos early gene expression and 14 C 2-deoxyglucose autoradiography during mother-to-infant fear transmission revealed lateral and basal amygdala nuclei activity, with a causal role highlighted by pharmacological inactivation of pups' amygdala preventing the fear transmission. Maternal presence was not needed for fear transmission, because an elevation of pups' corticosterone induced by the odor of the frightened mother along with a novel peppermint odor was sufficient to produce pups' subsequent aversion to that odor. Disruption of axonal tracts from the Grueneberg ganglion, a structure implicated in alarm chemosignaling, or blockade of pups' alarm odor-induced corticosterone increase prevented transfer of fear. These memories are acquired at younger ages compared with amygdala-dependent odorshock conditioning and are more enduring following minimal conditioning. Our results provide clues to understanding transmission of specific fears across generations and its dependence upon maternal induction of pups' stress response paired with the cue to induce amygdala-dependent learning plasticity. Results are discussed within the context of caregiver emotional responses and adaptive vs. pathological fears social transmission.necklace glomeruli | pheromone | olfaction | PTSD | social referencing

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Effect of Selective Inhibition of Reactivated Nicotine-Associated Memories With Propranolol on Nicotine Craving

et al. 2017

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IMPORTANCE A relapse into nicotine addiction during abstinence often occurs after the reactivation of nicotine reward memories, either by acute exposure to nicotine (a smoking episode) or by smoking-associated conditioned stimuli (CS). Preclinical studies suggest that drug reward memories can undergo memory reconsolidation after being reactivated, during which they can be weakened or erased by pharmacological or behavioral manipulations. However, translational clinical studies using CS-induced memory retrieval-reconsolidation procedures to decrease drug craving reported inconsistent results. OBJECTIVE To develop and test an unconditioned stimulus (UCS)-induced retrieval-reconsolidation procedure to decrease nicotine craving among people who smoke. DESIGN, SETTING, AND PARTICIPANTS A translational rat study and human study in an academic outpatient medical center among 96 male smokers (aged 18–45 years) to determine the association of propranolol administration within the time window of memory reconsolidation (after retrieval of the nicotine-associated memories by nicotine UCS exposure) with relapse to nicotine-conditioned place preference (CPP) and operant nicotine seeking in rats, and measures of preference to nicotine-associated CS and nicotine craving among people who smoke. INTERVENTION The study rats were injected noncontingently with the UCS (nicotine 0.15 mg/kg, subcutaneous) in their home cage, and the human study participants administered a dose of propranolol (40 mg, per os; Zhongnuo Pharma). MAIN OUTCOMES AND MEASURES Nicotine CPP and operant nicotine seeking in rats, and preference and craving ratings for newly learned and preexisting real-life nicotine-associated CS among people who smoke. RESULTS Sixty-nine male smokers completed the experiment and were included for statistical analysis: 24 in the group that received placebo plus 1 hour plus UCS, 23 who received propranolol plus 1 hour plus UCS, and 22 who received UCS plus 6 hours plus propranolol. In rat relapse models, propranolol injections administered immediately after nicotine UCS-induced memory retrieval inhibited subsequent nicotine CPP and operant nicotine seeking after short (CPP, d = 1.72, 95% CI, 0.63–2.77; operant seeking, d = 1.61, 95% CI, 0.59–2.60) or prolonged abstinence (CPP, d = 1.46, 95% CI, 0.42–2.47; operant seeking: d = 1.69, 95% CI, 0.66–2.69), as well as nicotine priming-induced reinstatement of nicotine CPP (d = 1.28, 95% CI, 0.27–2.26) and operant nicotine seeking (d = 1.61, 95% CI, 0.59–2.60) after extinction. Among the smokers, oral propranolol administered prior to nicotine UCS-induced memory retrieval decreased subsequent nicotine preference induced by newly learned nicotine CS (CS1, Cohen d =0.61, 95% CI, 0.02–1.19 and CS2, d = 0.69, 95% CI, 0.10–1.28, respectively), preexisting nicotine CS (d = 0.57, 95% CI, −0.02 to 1.15), and nicotine priming (CS1, d = 0.82, 95% CI, 0.22–1.41 and CS2, d = 0.78, 95% CI, 0.18–1.37, respectively; preexisting nicotine CS, d = 0.92, 95% CI, 0.31–1.52), as well as nicotine c...

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The amygdala encodes specific sensory features of an aversive reinforcer

Cited by 87 publications

References 12 publications

The selectivity of aversive memory reconsolidation and extinction processes depends on the initial encoding of the Pavlovian association

The selectivity of aversive memory reconsolidation and extinction processes depends on the initial encoding of the Pavlovian association

Intergenerational transmission of emotional trauma through amygdala-dependent mother-to-infant transfer of specific fear

Effect of Selective Inhibition of Reactivated Nicotine-Associated Memories With Propranolol on Nicotine Craving

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