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

Yin, Shuai; Ke, Bo; Liu, Yuelu; Thigpen, Nina; Keil, Andreas; Ding, Mingzhou

doi:10.1093/scan/nsaa122

Cited by 18 publications

(27 citation statements)

References 74 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Unlike neutral conditioning where the main effect is to strengthen the response magnitude, the main effect of aversive conditioning is to significantly reduce neural response magnitude and the prevalence of cue-evoked persistent activity within V1. Previous studies have demonstrated that in primary sensory areas, fear conditioning results in a "sparsification" of sensory responses (Gdalyahu et al, 2012;Yin et al, 2020). The network dampening caused by aversive conditioning we observe here is consistent with these previous reports.…”

Section: Cue-evoked Persistent Activity In the Presence Of Non-rewardsupporting

confidence: 93%

Visual Cues Predictive of Behaviorally Neutral Outcomes Evoke Persistent but Not Interval Timing Activity in V1, Whereas Aversive Conditioning Suppresses This Activity

Monk

Allard

Shuler

2021

Front. Syst. Neurosci.

View full text Add to dashboard Cite

Cue-evoked persistent activity is neural activity that persists beyond stimulation of a sensory cue and has been described in many regions of the brain, including primary sensory areas. Nonetheless, the functional role that persistent activity plays in primary sensory areas is enigmatic. However, one form of persistent activity in a primary sensory area is the representation of time between a visual stimulus and a water reward. This “reward timing activity”—observed within the primary visual cortex—has been implicated in informing the timing of visually cued, reward-seeking actions. Although rewarding outcomes are sufficient to engender interval timing activity within V1, it is unclear to what extent cue-evoked persistent activity exists outside of reward conditioning, and whether temporal relationships to other outcomes (such as behaviorally neutral or aversive outcomes) are able to engender timing activity. Here we describe the existence of cue-evoked persistent activity in mouse V1 following three conditioning strategies: pseudo-conditioning (where unpaired, monocular visual stimuli are repeatedly presented to an animal), neutral conditioning (where monocular visual stimuli are paired with a binocular visual stimulus, at a delay), and aversive conditioning (where monocular visual stimuli are paired with a tail shock, at a delay). We find that these conditioning strategies exhibit persistent activity that takes one of three forms, a sustained increase of activity; a sustained decrease of activity; or a delayed, transient peak of activity, as previously observed following conditioning with delayed reward. However, these conditioning strategies do not result in visually cued interval timing activity, as observed following appetitive conditioning. Moreover, we find that neutral conditioning increases the magnitude of cue-evoked responses whereas aversive conditioning strongly diminished both the response magnitude and the prevalence of cue-evoked persistent activity. These results demonstrate that cue-evoked persistent activity within V1 can exist outside of conditioning visual stimuli with delayed outcomes and that this persistent activity can be uniquely modulated across different conditioning strategies using unconditioned stimuli of varying behavioral relevance. Together, these data extend our understanding of cue-evoked persistent activity within a primary sensory cortical network and its ability to be modulated by salient outcomes.

show abstract

Section: Cue-evoked Persistent Activity In the Presence Of Non-rewardsupporting

confidence: 93%

Visual Cues Predictive of Behaviorally Neutral Outcomes Evoke Persistent but Not Interval Timing Activity in V1, Whereas Aversive Conditioning Suppresses This Activity

Monk

Allard

Shuler

2021

Front. Syst. Neurosci.

View full text Add to dashboard Cite

show abstract

“…It has been assumed that re-entrant projections from fear-relevant areas centered around the amygdala prompt short- and long-term adaptions in threat-related feature-specific neurons 9 , 51 . However, a recent study, exploiting the benefits of simultaneous fMRI-EEG analysis, showed that threat-related visuocortical changes were associated with neural activity in the ventral attention network, but not in the amygdala 52 . The ventral attention network, including the temporoparietal and inferior frontal cortices, is specialized on detecting behaviorally relevant, salient stimuli 53 .…”

Section: Discussionmentioning

confidence: 99%

Associative learning shapes visual discrimination in a web-based classical conditioning task

Stegmann

Andreatta

Pauli

et al. 2021

Sci Rep

View full text Add to dashboard Cite

Threat detection plays a vital role in adapting behavior to changing environments. A fundamental function to improve threat detection is learning to differentiate between stimuli predicting danger and safety. Accordingly, aversive learning should lead to enhanced sensory discrimination of danger and safety cues. However, studies investigating the psychophysics of visual and auditory perception after aversive learning show divergent findings, and both enhanced and impaired discrimination after aversive learning have been reported. Therefore, the aim of this web-based study is to examine the impact of aversive learning on a continuous measure of visual discrimination. To this end, 205 participants underwent a differential fear conditioning paradigm before and after completing a visual discrimination task using differently oriented grating stimuli. Participants saw either unpleasant or neutral pictures as unconditioned stimuli (US). Results demonstrated sharpened visual discrimination for the US-associated stimulus (CS+), but not for the unpaired conditioned stimuli (CS−). Importantly, this finding was irrespective of the US’s valence. These findings suggest that associative learning results in increased stimulus salience, which facilitates perceptual discrimination in order to prioritize attentional deployment.

show abstract

“…A classical conditioning approach was used to pair one of three initially neutral pitches of a sine-wave tone with a loud noise. Three dependent variables with known sensitivity to generalization learning were considered: self-reported valence and emotional arousal in response to each pitch ( McTeague et al, 2015 ; Plog et al, 2022 ), as well as stimulus-induced reductions in parieto-occipital alpha power, a brain response linked to the attentive processing of aversively conditioned cues, auditory or visual ( Miskovic and Keil, 2012 ; Yin et al, 2020 ; Friedl and Keil, 2021 ). Self-reported symptoms on the MSS were used to quantify the intensity of Misophonia symptoms in each participant.…”

Section: Discussionmentioning

confidence: 99%

“…Parieto-occipital alpha-band power reduction has long been associated with responses to a salient external event, regardless of sensory modality ( Berger, 1929 ; Friedl and Keil, 2021 ). Recently, these changes have been shown to index aversive conditioning, including generalization learning ( Friedl and Keil, 2020 ; Yin et al, 2020 ). Consistent with the self-reported behavioral findings, we found that alpha-band power reduction showed pronounced activity patterns best fit by an all-or-nothing learning model across all participants at the predicted parieto-occipital regions where alpha power during rest is maximal.…”

Section: Discussionmentioning

confidence: 99%

The Relationship Between Self-Reported Misophonia Symptoms and Auditory Aversive Generalization Leaning: A Preliminary Report

et al. 2022

Self Cite

View full text Add to dashboard Cite

Misophonia is characterized by excessive aversive reactions to specific “trigger” sounds. Although this disorder is increasingly recognized in the literature, its etiological mechanisms and maintaining factors are currently unclear. Several etiological models propose a role of Pavlovian conditioning, an associative learning process heavily researched in similar fear and anxiety-related disorders. In addition, generalization of learned associations has been noted as a potential causal or contributory factor. Building upon this framework, we hypothesized that Misophonia symptoms arise as a consequence of overgeneralized associative learning, in which aversive responses to a noxious event also occur in response to similar events. Alternatively, heightened discrimination between conditioned threat and safety cues may be present in participants high in Misophonia symptoms, as predicted by associative learning models of Misophonia. This preliminary report (n = 34) examines auditory generalization learning using self-reported behavioral (i.e., valence and arousal ratings) and EEG alpha power reduction. Participants listened to three sine tones differing in pitch, with one pitch (i.e., CS+) paired with an aversive loud white noise blast, prompting aversive Pavlovian generalization learning. We assessed the extent to which overgeneralization versus heightened discrimination learning is associated with self-reported Misophonia symptoms, by comparing aversive responses to the CS+ and other tones similar in pitch. Behaviorally, all participants learned the contingencies between CS+ and noxious noise, with individuals endorsing elevated Misophonia showing heightened aversive sensitivity to all stimuli, regardless of conditioning and independent of hyperacusis status. Across participants, parieto-occipital EEG alpha-band power reduction was most pronounced in response to the CS+ tone, and this difference was greater in those with self-reported Misophonia symptoms. The current preliminary findings do not support the notion that overgeneralization is a feature of self-reported emotional experience in Misophonia, but that heightened sensitivity and discrimination learning may be present at the neural level.

show abstract

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

Cited by 18 publications

References 74 publications

Visual Cues Predictive of Behaviorally Neutral Outcomes Evoke Persistent but Not Interval Timing Activity in V1, Whereas Aversive Conditioning Suppresses This Activity

Visual Cues Predictive of Behaviorally Neutral Outcomes Evoke Persistent but Not Interval Timing Activity in V1, Whereas Aversive Conditioning Suppresses This Activity

Associative learning shapes visual discrimination in a web-based classical conditioning task

The Relationship Between Self-Reported Misophonia Symptoms and Auditory Aversive Generalization Leaning: A Preliminary Report

Contact Info

Product

Resources

About