Extinction-resistant attention to long-term conditioned threat is indexed by selective visuocortical alpha suppression in humans

Panitz, Christian; Keil, Andreas; Mueller, Erik M.

doi:10.1101/533141

Cited by 9 publications

(12 citation statements)

References 71 publications

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“…Supporting this interpretation, a previous study found the adaptation of limbic brain areas to be accompanied by increased engagement of visual cortex during fear conditioning ( Lithari et al , 2016 ). Such persistent visuocortical engagement with the threat cue may be particularly adaptive in conditioning regimes with intermittent pairing, in which not all CS+ trials include a US presentation, promoting exploration behavior and scanning of the environment for contingency cues—a hypothesis that is readily testable in future research and consistent with extinction-resistant alpha power changes during a 2-day conditioning regimen ( Panitz et al , 2019 ). Notably, heightened attention to the threat cue is unlikely to explain the cross-species observation that extensive conditioning over time prompts selectively heightened visuocortical responses at very short latencies and in retinotopic visual areas.…”

Section: Discussionmentioning

confidence: 99%

Fear conditioning prompts sparser representations of conditioned threat in primary visual cortex

Yin

Liu

et al. 2020

Social Cognitive and Affective Neuroscience

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Repeated exposure to threatening stimuli alters sensory responses. We investigated the underlying neural mechanism by re-analyzing previously-published simultaneous EEG-fMRI data from humans viewing oriented gratings during Pavlovian fear conditioning. In acquisition, one grating (CS+) was paired with a noxious noise, the unconditioned stimulus (US). The other grating (CS-) was never paired with the US. In habituation, which preceded acquisition, and in extinction, the same two gratings were presented without US. Using fMRI-BOLD multivoxel patterns in primary visual cortex during habituation as reference, we found that during acquisition, aversive learning selectively prompted systematic changes in multivoxel patterns evoked by CS+. Specifically, CS+ evoked voxel patterns in V1 became sparser as aversive learning progressed, and the sparsified pattern appeared to be preserved in extinction. Concomitant with the voxel pattern changes, occipital alpha oscillations were increasingly more desynchronized during CS+ (but not CS-) trials. Across acquisition trials, the rate of change in CS+-related alpha desynchronization was correlated with the rate of change in multivoxel pattern representations of CS+. Furthermore, alpha oscillations co-varied with BOLD in the ventral attention network, but not with BOLD in the amygdala. Thus, fear conditioning prompts persistent sparsification of voxel patterns evoked by threat, likely mediated by attention-related mechanisms.

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Section: Discussionmentioning

confidence: 99%

Fear conditioning prompts sparser representations of conditioned threat in primary visual cortex

Yin

Liu

et al. 2020

Social Cognitive and Affective Neuroscience

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“…Alpha blocking has been shown to correlate with enhanced cortical processing of low-level stimulus properties such as color and motion when these dimensions are made task-relevant (Snyder & Foxe, 2010), and here we demonstrate that the alpha-band response is also sensitive to SF-associated contingencies. In addition, although alpha suppression in response to naturally foreboding stimuli is well established (e.g., Vagnoni, Lourenco, & Longo, 2015;De Cesarei & Codispoti, 2011;Huster, Stevens, Gerlach, & Rist, 2009;Güntekin & Basar, 2007), only recently (Panitz, Keil, & Mueller, 2019) has this effect been linked to conditioned threat cues. The present work shows that conditioned alpha blocking extends to a visual feature as basic as spatial frequency when such information provides the only basis for discriminating threatening from nonthreatening stimuli.…”

Section: Alpha Powermentioning

confidence: 99%

Effects of Experience on Spatial Frequency Tuning in the Visual System: Behavioral, Visuocortical, and Alpha-band Responses

Friedl

Keil

2020

Journal of Cognitive Neuroscience

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Using electrophysiology and a classic fear conditioning paradigm, this work examined adaptive visuocortical changes in spatial frequency tuning in a sample of 50 undergraduate students. High-density EEG was recorded while participants viewed 400 total trials of individually presented Gabor patches of 10 different spatial frequencies. Patches were flickered to produce sweep steady-state visual evoked potentials (ssVEPs) at a temporal frequency of 13.33 Hz, with stimulus contrast ramping up from 0% to 41% Michelson over the course of each 2800-msec trial. During the final 200 trials, a selected range of Gabor stimuli (either the lowest or highest spatial frequencies, manipulated between participants) were paired with an aversive 90-dB white noise auditory stimulus. Changes in spatial frequency tuning from before to after conditioning for paired and unpaired gratings were evaluated at the behavioral and electrophysiological level. Specifically, ssVEP amplitude changes were evaluated for lateral inhibition and generalization trends, whereas change in alpha band (8–12 Hz) activity was tested for a generalization trend across spatial frequencies, using permutation-controlled F contrasts. Overall time courses of the sweep ssVEP amplitude envelope and alpha-band power were orthogonal, and ssVEPs proved insensitive to spatial frequency conditioning. Alpha reduction (blocking) was most pronounced when viewing fear-conditioned spatial frequencies, with blocking decreasing along the gradient of spatial frequencies preceding conditioned frequencies, indicating generalization across spatial frequencies. Results suggest that alpha power reduction—conceptually linked to engagement of attention and alertness/arousal mechanisms—to fear-conditioned stimuli operates independently of low-level spatial frequency processing (indexed by ssVEPs) in primary visual cortex.

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“…However, there has been limited empirical research on alpha-band suppression during aversive conditioning ( Chien et al. , 2017 ; Panitz et al. , 2019 ; Friedl and Keil, 2020 , 2021 ; Yin et al.…”

Section: Introductionmentioning

confidence: 99%

Alpha-band EEG suppression as a neural marker of sustained attentional engagement to conditioned threat stimuli

Bacigalupo

Luck

2022

Social Cognitive and Affective Neuroscience

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Attention helps us to be aware of the external world, and this may be especially important when a threat stimulus predicts an aversive outcome. EEG alpha-band suppression has long been considered as a neural signature of attentional engagement. The present study was designed to test whether attentional engagement, as indexed by alpha-band suppression, is increased in a sustained manner following a conditioned stimulus (CS) that is paired with an aversive (CS+) vs. neutral (CS-) outcome. We tested 70 healthy young adults in aversive conditioning and extinction paradigms. One of three colored circles served as the CS+, which was paired in 50% of the trials with a noise burst (unconditioned stimulus, US). The other colored circles (CS-) were never paired with the US. For conditioning, we found greater alpha-band suppression for the CS+ compared to the CS-; this suppression was sustained through the time of the predicted US. This effect was significantly reduced for extinction. These results indicate that conditioned threat stimuli trigger an increase in attentional engagement as subjects monitor the environment for the predicted aversive stimulus. Moreover, this alpha-band suppression effect may be valuable for future studies examining normal or pathological increases in attentional monitoring following threat stimuli.

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Extinction-resistant attention to long-term conditioned threat is indexed by selective visuocortical alpha suppression in humans

Cited by 9 publications

References 71 publications

Fear conditioning prompts sparser representations of conditioned threat in primary visual cortex

Fear conditioning prompts sparser representations of conditioned threat in primary visual cortex

Effects of Experience on Spatial Frequency Tuning in the Visual System: Behavioral, Visuocortical, and Alpha-band Responses

Alpha-band EEG suppression as a neural marker of sustained attentional engagement to conditioned threat stimuli

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