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Influence of contingency awareness on neural, electrodermal and evaluative responses during fear conditioning.

ABSTRACT: In an fMRI study, effects of contingency awareness on conditioned responses were assessed in three groups comprising 118 subjects. A differential fear-conditioning paradigm with visual conditioned stimuli, an electrical unconditioned stimulus and two distractors was applied. The instructed aware group was informed about the contingencies, whereas the distractors prevented contingency detection in the unaware group. The third group (learned aware) was not informed about the contingencies, but learned them despite the distractors. Main effects of contingency awareness on conditioned responses emerged in several brain structures. Post hoc tests revealed differential dorsal anterior cingulate, insula and ventral striatum responses in aware conditioning only, whereas the amygdala was activated independent of contingency awareness. Differential responses of the hippocampus were specifically observed in learned aware subjects, indicating a role in the development of contingency awareness. The orbitofrontal cortex showed varying response patterns: lateral structures showed higher responses in instructed aware than unaware subjects, the opposite was true for medial parts. Conditioned subjective and electrodermal responses emerged only in the two aware groups. These results confirm the independence of conditioned amygdala responses from contingency awareness and indicate specific neural circuits for different aspects of fear acquisition in unaware, learned aware and instructed aware subjects.

SUBMITTER: Tabbert K

PROVIDER: S-EPMC3150860 | biostudies-other | 2011 Sep

REPOSITORIES: biostudies-other

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Influence of contingency awareness on neural, electrodermal and evaluative responses during fear conditioning.

Tabbert Katharina K Merz Christian J CJ Klucken Tim T Schweckendiek Jan J Vaitl Dieter D Wolf Oliver T OT Stark Rudolf R

Social cognitive and affective neuroscience 20100806 4

In an fMRI study, effects of contingency awareness on conditioned responses were assessed in three groups comprising 118 subjects. A differential fear-conditioning paradigm with visual conditioned stimuli, an electrical unconditioned stimulus and two distractors was applied. The instructed aware group was informed about the contingencies, whereas the distractors prevented contingency detection in the unaware group. The third group (learned aware) was not informed about the contingencies, but lea ...[more]

PMID: 20693389

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Project description:BackgroundDysregulation of fear learning has been associated with psychiatric disorders that have altered positive and negative valence domain function. While amygdala-insula-prefrontal circuitry is considered important for fear learning, there have been inconsistencies in neural findings in healthy and clinical human samples. This study aimed to delineate the neural substrates and behavioral responses during fear learning in a large, transdiagnostic sample with predominantly depressive and/or anxious dysfunction.MethodsTwo-hundred and eighty-two individuals (52 healthy participants; 230 participants with depression and/or anxiety-related problems) from the Tulsa 1000 study, an ongoing, naturalistic longitudinal study based on a dimensional psychopathological framework, completed a Pavlovian fear learning task during functional magnetic resonance imaging. Linear mixed-effects analyses examined condition-by-time effects on brain activation (CS+, CS- across familiarization, conditioning, and extinction trials). A data-driven latent profile analysis (LPA) examined distinct patterns of behavioral and neural responses to threat across fear conditioning and extinction, while logistic regression analyses evaluated cognitive-affective predictors of latent profiles.ResultsWhole-brain analyses revealed a condition-by-time interaction in the anterior insula, postcentral gyrus, superior temporal gyrus, middle frontal gyrus, and cerebellum but not amygdala. The LPA identified distinct latent profiles across subjective and neural levels of measurement. Anterior insula profiles were characterized by marginal differences in age and state anxiety.ConclusionsOur findings demonstrate that human fear learning recruits a distributed network of regions involved in interoceptive, cognitive, motivational, and psychomotor processes. Data-driven analyses identified distinct profiles of subjective and neural responses during fear learning that transcended clinical diagnoses, but no robust relationships to demographic or cognitive-affective variable were identified.

Project description:ImportanceThe fear conditioning and extinction neurocircuitry has been extensively studied in healthy and clinical populations, with a particular focus on posttraumatic stress disorder. Despite significant overlap of symptoms between posttraumatic stress disorder and anxiety disorders, the latter has received less attention. Given that dysregulated fear levels characterize anxiety disorders, examining the neural correlates of fear and extinction learning may shed light on the pathogenesis of underlying anxiety disorders.ObjectivesTo investigate the psychophysiological and neural correlates of fear conditioning and extinction recall in anxiety disorders and to document how these features differ as a function of multiple diagnoses or anxiety severity.Design, setting, and participantsThis investigation was a cross-sectional, case-control, functional magnetic resonance imaging study at an academic medical center. Participants were healthy controls and individuals with at least 1 of the following anxiety disorders: generalized anxiety disorder, social anxiety disorder, specific phobia, and panic disorder. The study dates were between March 2013 and May 2015.ExposuresTwo-day fear conditioning and extinction paradigm.Main outcomes and measuresSkin conductance responses, blood oxygenation level-dependent responses, trait anxiety scores from the State Trait Anxiety Inventory-Trait Form, and functional connectivity.ResultsThis study included 21 healthy controls (10 women) and 61 individuals with anxiety disorders (36 women). P values reported for the neuroimaging results are all familywise error corrected. Skin conductance responses during extinction recall did not differ between individuals with anxiety disorders and healthy controls (ηp2 = 0.001, P = .79), where ηp2 is partial eta squared. The anxiety group had lower activation of the ventromedial prefrontal cortex (vmPFC) during extinction recall (ηp2 = 0.178, P = .02). A similar hypoactive pattern was found during early conditioning (ηp2 = 0.106, P = .009). The vmPFC hypoactivation was associated with anxiety symptom severity (r = -0.420, P = .01 for conditioning and r = -0.464, P = .004 for extinction recall) and the number of co-occuring anxiety disorders diagnosed (ηp2 = 0.137, P = .009 for conditioning and ηp2 = 0.227, P = .004 for extinction recall). Psychophysiological interaction analyses revealed that the fear network connectivity differed between healthy controls and the anxiety group during fear learning (ηp2 range between 0.088 and 0.176 and P range between 0.02 and 0.003) and extinction recall (ηp2 range between 0.111 and 0.235 and P range between 0.02 and 0.002).Conclusions and relevanceDespite no skin conductance response group differences during extinction recall, brain activation patterns between anxious and healthy individuals differed. These findings encourage future studies to examine the conditions longitudinally and in the context of treatment trials to improve and guide therapeutics via advanced neurobiological understanding of each disorder.

Dataset Information

Influence of contingency awareness on neural, electrodermal and evaluative responses during fear conditioning.

Publications

Influence of contingency awareness on neural, electrodermal and evaluative responses during fear conditioning.

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