Aversive Conditioning of Spatial Position Sharpens Neural Population-Level Tuning in Visual Cortex and Selectively Alters Alpha-Band Activity

Abstract

Processing capabilities for many low-level visual features are experientially malleable, aiding sighted organisms in adapting to dynamic environments. Explicit instructions to attend a specific visual field location influence retinotopic visuocortical activity, amplifying responses to stimuli appearing at cued spatial positions. It remains undetermined both how such prioritization affects surrounding nonprioritized locations, and if a given retinotopic spatial position can attain enhanced cortical representation through experience rather than instruction. The current report examined visuocortical response changes as human observers (N = 51, 19 male) learned, through differential classical conditioning, to associate specific screen locations with aversive outcomes. Using dense-array EEG and pupillometry, we tested the preregistered hypotheses of either sharpening or generalization around an aversively associated location following a single conditioning session. Competing hypotheses tested whether mean response changes would take the form of a Gaussian (generalization) or difference-of-Gaussian (sharpening) distribution over spatial positions, peaking at the viewing location paired with a noxious noise. Occipital 15 Hz steady-state visual evoked potential responses were selectively heightened when viewing aversively paired locations and displayed a nonlinear, difference-of-Gaussian profile across neighboring locations, consistent with suppressive surround modulation of nonprioritized positions. Measures of alpha-band (8-12 Hz) activity were differentially altered in anterior versus posterior locations, while pupil diameter exhibited selectively heightened responses to noise-paired locations but did not evince differences across the nonpaired locations. These results indicate that visuocortical spatial representations are sharpened in response to location-specific aversive conditioning, while top-down influences indexed by alpha-power reduction exhibit posterior generalization and anterior sharpening.

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

“…Synthesizing these findings, evidence of both generalization and sharpened tuning response patterns have been provided in human electroencephalography (EEG) research measuring visual sensory cortical responses ( Müller et al, 1998 ; Wieser et al, 2016 ), and alpha-band power, a signal reflecting attentional processing ( Deng et al, 2020 ) and heightened attentional engagement to a CS+ ( Panitz et al, 2019 ). Specifically, parietal alpha power ( Friedl and Keil, 2020 , 2021 ) and steady-state visual evoked potentials (i.e., ssVEPs) displayed Gaussian distributions across the generalization gradient ( McTeague et al, 2015 ), similar to neuroimaging work ( Greenberg et al, 2013 ; Lissek et al, 2014b ), and followed the generalization pattern shown in Figure 1A (Ghirlanda and Enquist, 2003 ). Parietal alpha-band activity (spectral power between 8 and 12 Hz) has been established as a robust index of stimulus saliency, linked to heightened attentional engagement with conditioned stimuli ( Yin et al, 2018 ).…”

“…During generalization learning, it is expected that as threat cues acquire increased task-relevance through conditioning, alpha power would show greater power reduction for the CS+ compared to the generalization stimuli. In contrast, ssVEPs recorded from occipital sites, commonly used to assess visual cortical perception, showed difference-of-Gaussian patterns (McTeague et al, 2015;Stegmann et al, 2020;Friedl and Keil, 2021). This suggests that non-sensory regions are likely to show Gaussian-like responses along a generalization gradient, while primary sensory cortices may yield sharpened tuning, both response patterns being adaptive, respectively, for optimizing perception (sharpening) and attentional orienting (generalization).…”

“…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.…”

“…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 ).…”

“…Such a response pattern would indicate suppression of the most similar GS, resulting in sharpening in sensory systems ( McTeague et al, 2015 ). We included an all-or-nothing discrimination learning model ( Figure 1C ) to assess the possibility that (H3C) the CS+ alone would elicit heightened responses in our dependent variables, with little to no difference in response to the other GS, an effect observed previously for alpha power changes in visual aversive conditioning paradigms ( Friedl and Keil, 2020 , 2021 ).…”