Extinction Learning in Humans

Phelps, Elizabeth A.; Delgado, Mauricio R.; Nearing, Katherine; LeDoux, Joseph E.

doi:10.1016/j.neuron.2004.08.042

Cited by 1,584 publications

(746 citation statements)

References 29 publications

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“…In short, emotional stimuli provoke an increase in the amygdala's reactivity, which overwhelms the inhibitory activity in prefrontal top‐down control regions, resulting in an impaired capacity of individuals to self‐regulate. This mechanism, which echoes the basic neuroanatomy of fear‐conditioning (LeDoux, 2000; Phelps, Delgado, Nearing, & LeDoux, 2004), likely contributes to increased risk for later psychological disorders like PTSD and major depression (Shin & Liberzon, 2010). However, this mechanism of dysregulated amygdala activity has previously been studied without taking into account the often‐reported broader cognitive deficits in executive functions that are seen in many individuals exposed to I‐ELT (van der Kolk, 2003).…”

Section: Discussionmentioning

confidence: 85%

Interpersonal early‐life trauma alters amygdala connectivity and sustained attention performance

et al. 2017

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IntroductionInterpersonal early life trauma (I‐ELT) is associated with a myriad of functional impairments in adulthood, increased risk of drug addiction, and neuropsychiatric disorders. While deficits in emotional regulation and amygdala functioning are well characterized, deficits in general cognitive functioning have also been documented. However, the neural underpinnings of cognitive dysfunction in adults with a history of I‐ELT and the potential relationship between amygdala‐based functional connectivity and behavioral performance are currently poorly understood. This study examined how I‐ELT affects the cognitive and neural mechanisms supporting sustained attention.MethodsA total of 66 Veterans (18 with and 48 without a history of I‐ELT) completed a nonemotional sustained attention task during functional MRI.ResultsThe individuals with I‐ELT showed significant impairments in sustained attention (i.e., higher error rates, greater response variability). This cohort exhibited increased amygdala functional connectivity with the prefrontal cortex and decreased functional connectivity with the parahippocampal gyrus when compared to those without I‐ELT. These connections were significantly correlated with individual differences in sustained attention performance. Notably, classification analyses revealed that the pattern of amygdala connectivity across the whole brain was able to classify I‐ELT status with 70% accuracy.ConclusionThese results provide evidence of a lasting negative impact for those with a history of I‐ELT on sustained attention ability. They also highlight a critical role for amygdala functioning in cognitive control and sustained attention for those with a history of I‐ELT, which may underlie the observed attention deficits in clinical assessments and cognitive tests involving both emotional and nonemotional stimuli.

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Section: Discussionmentioning

confidence: 85%

Interpersonal early‐life trauma alters amygdala connectivity and sustained attention performance

et al. 2017

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“…Before discarding any data, adequacy of conditioning was examined as defined by CS+ > CS− during conditioning, and CS+ during conditioning >CS+ during habituation (Asthana et al., 2013; Mungee et al., 2014, 2016; Phelps et al., 2004; van ‘t Wout et al., 2013). Following this definition, five participants did not condition appropriately and were removed from subsequent analyses.…”

Section: Resultsmentioning

confidence: 99%

“…Animal models and human studies of PTSD have highlighted aberrations in neural circuitry including hyperactivity in the amygdala and dorsal anterior cingulate cortex, regions that promote fear responses, alongside hypoactivity in the ventromedial prefrontal cortex (vmPFC), a region that is thought to suppress fear responses (Milad & Quirk, 2012; Quirk, Garcia, & González‐Lima, 2006; VanElzakker et al., 2014). More specifically, vmPFC engagement during extinction learning predicts extinction success and is associated with “top‐down” modulation of amygdala‐driven fear expression (Do‐Monte, Manzano‐Nieves, Quiñones‐Laracuente, Ramos‐Medina, & Quirk, 2015; Lebrón, Milad, & Quirk, 2004; Milad et al., 2005, 2007; Phelps, Delgado, Nearing, & LeDoux, 2004; Quirk, Likhtik, Pelletier, & Paré, 2003; Rosenkranz, Moore, & Grace, 2003). Results from studies with PTSD patients revealed deficits in extinction recall (Milad et al., 2008), reduced vmPFC volume, and activation during fear extinction compared to controls (Bremner et al., 2005; Milad et al., 2009; Rauch et al., 2003; Rougemont‐Bücking et al., 2011; Shin, Rauch, & Pitman, 2006).…”

Section: Introductionmentioning

confidence: 99%

Transcranial direct current stimulation may modulate extinction memory in posttraumatic stress disorder

et al. 2017

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BackgroundAbnormalities in fear extinction and recall are core components of posttraumatic stress disorder (PTSD). Data from animal and human studies point to a role of the ventromedial prefrontal cortex (vmPFC) in extinction learning and subsequent retention of extinction memories. Given the increasing interest in developing noninvasive brain stimulation protocols for psychopathology treatment, we piloted whether transcranial direct current stimulation (tDCS) during extinction learning, vs. during consolidation of extinction learning, might improve extinction recall in veterans with warzone‐related PTSD.MethodsTwenty‐eight veterans with PTSD completed a 2‐day Pavlovian fear conditioning, extinction, and recall paradigm. Participants received one 10‐min session of 2 mA anodal tDCS over AF3, intended to target the vmPFC. Fourteen received tDCS that started simultaneously with extinction learning onset, and the remaining 14 participants received tDCS during extinction consolidation. Normalized skin conductance reactivity (SCR) was the primary outcome measure. Linear mixed effects models were used to test for effects of tDCS on late extinction and early extinction recall 24 hr later.ResultsDuring early recall, veterans who received tDCS during extinction consolidation showed slightly lower SCR in response to previously extinguished stimuli as compared to veterans who received tDCS simultaneous with extinction learning (p = .08), generating a medium effect size (Cohen's d = .38). There was no significant effect of tDCS on SCR during late extinction.ConclusionsThese preliminary findings suggest that testing the effects of tDCS during consolidation of fear extinction may have promise as a way of enhancing extinction recall.

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“…Continuous CS-UCS parings (100%) usually results in rapid acquisition, but also in rapid extinction in human participants (LaBar, Gatenby, Gore, LeDoux, & Phelps, 1998). Therefore, a partial reinforcement schedule was chosen to decrease extinction learning (Phelps, Delgado, Nearing, & LeDoux, 2004) and, thereby, allow us to examine the impact of fear acquisition in a test phase where no more US were presented (see Alpers, Ruhleder, Walz, Mühlberger, & Pauli, 2005). Trials were separated by inter-trial-intervals (ITIs) ranging from 20 s to 35 s. During five ITIs in each block, a startle probe was delivered with inter-probe-intervals of at least 15 s. During fear conditioning, SCRs and startle eyeblink responses were measured as physiological indices of fear acquisition.…”

Section: Methodsmentioning

confidence: 99%

Acquisition of behavioral avoidance: Task-irrelevant conditioned stimuli trigger costly decisions.

Pittig¹,

Schulz²,

Craske³

et al. 2014

Journal of Abnormal Psychology

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Individuals avoid stimuli which are associated with aversive experience to preserve safety. However, behavioral avoidance also causes impairments and prevents the individual from attaining positive rewards. Little is known about the link between fear acquisition and the development of behavioral avoidance in the presence of potential rewards. Therefore, two experiments investigated the impact of fear conditioning on a subsequent gambling task. In an experimental group (n ϭ 30) advantageous choices (higher reward probability) were linked to a fear-relevant stimulus that was associated with an aversive unconditioned stimulus (US) during fear conditioning (conditioned stimulus, CSϩ). A disadvantageous choice (lower reward probability) was, however, linked to a safe stimulus that was never associated with the US (CSϪ). In a control group (n ϭ 25), fear conditioning was followed by a similar gambling task with novel stimuli. A second experiment focused on individual predictors of avoidant decisions (n ϭ 81). Compared with the control group, individuals in the experimental groups avoided the advantageous CS ϩ choice despite fewer gains. The predictor analysis further clarified that avoidant decisions were pronounced in highly trait anxious participants who exhibited higher fear responses. On the other hand, findings also indicated a reduction in absolute avoidance across the task. Combined, these findings demonstrate that fear conditioning can lead to avoidant decision making, especially in vulnerable individuals. The resulting costs parallel impairments caused by behavioral avoidance. Such an emotional decision-making style may be a link between aversive experience and the development of habitual pathological avoidance. Introducing rewards for approach, however, may counteract avoidant decisions.

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Extinction Learning in Humans

Cited by 1,584 publications

References 29 publications

Interpersonal early‐life trauma alters amygdala connectivity and sustained attention performance

Interpersonal early‐life trauma alters amygdala connectivity and sustained attention performance

Transcranial direct current stimulation may modulate extinction memory in posttraumatic stress disorder

Acquisition of behavioral avoidance: Task-irrelevant conditioned stimuli trigger costly decisions.

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