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

Abstract

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.

Aversive Conditioning of Spatial Position Sharpens Neural Population-level Tuning in Visual Cortex and Selectively Reduces Alpha-band Activity

“…The same all-or-none alpha-power modulation following aversive conditioning emerged in a previous study where centrally presented Gabor patches varied along a narrowly spaced continuum of spatial frequencies (Friedl & Keil, 2020). This is notable, as it suggests that alpha change circumscribed to a conditioned stimulus does not depend upon the conditioned stimulus being as perceptually distinct as were the easily discriminated spatial positions employed in the current paradigm.…”

“…Here, we show that an experientially acquired spatial association with an unpleasant stimulus prompts a similar facilitation of neural mass activity in visual cortex for stimuli presented at a conditioned location. Conditioning studies manipulating features other than visual field location (e.g., McTeague et al, 2015; Friedl & Keil, 2020) provide evidence that such facilitation manifests differently for alpha band and ssVEP signals.…”

Effects of affective content and motivational context on neural gain functions during naturalistic scene perception

“…Its parameters also capture differences in "baseline" contrast levels (i.e., time periods where the contrast is too low to be reflected in the ssVEP amplitude) as well as any differences in latency between conditions that may occur in this initial sensitivity to low contrast. We have observed this same phenomenon across several previous sweep ssVEP studies (e.g., Friedl & Keil, 2020).…”

No evidence for entrainment: endogenous gamma oscillations and rhythmic flicker responses coexist in visual cortex

“…Recent studies applying photic stimulation in the alpha band, have pointed to a coexistence of endogenous alpha oscillations and flicker responses, similar to the one we report here for the gamma band. While retinotopic alpha modulation has been associated with suppression of unattended stimuli, allocating attention to a stimulus flickering in the alpha band results in enhanced, phaselocked activity (Keitel et al, 2019;Gundlach et al, 2020, also see Antonov et al 2020;Friedl and Keil 2020 for stimulation at frequencies adjacent to the alpha-band). While the presented study does not allow nor aim to make generalized claims in favor or against neuronal entrainment, it is worth noting that the ability of rhythmic sensory stimulation to entrain endogenous oscillations is still a matter of debate.…”