Aversive Conditioning of Spatial Position Sharpens Neural Population-level Tuning in VisualCortex and Selectively Reduces 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, however, both how such prioritization affects surrounding non-prioritized locations, and if a given retinotopic spatial position can attain enhanced cortical representation through experience rather than instruction. This work examined visuocortical response changes as human observers learned, through differential classical conditioning, to associate specific on-screen locations with aversive outcomes. Using dense-array EEG and pupillometry, we tested the pre-registered hypotheses of either sharpening or generalization around an aversively associated location following a single conditioning session. Specifically, competing hypotheses tested if 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 (ssVEP) responses were selectively heightened when viewing aversively paired locations and displayed a non-linear, difference-of-gaussian profile across neighboring locations, consistent with suppressive surround modulation of non-prioritized positions. Measures of alpha band (8 - 12.8 Hz) activity and pupil diameter also exhibited selectively heightened responses to noise-paired locations but did not evince any difference across the non-paired 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 all-or-none modulation. Significance StatementIt is increasingly recognized that early visual cortex is not a static processor of physical features, but is instead constantly shaped by perceptual experience. It remains unclear, however, to what extent the cortical representation of many fundamental features, including visual field location, is malleable by experience. Using EEG and an aversive classical conditioning paradigm, we observed sharpening of visuocortical responses to stimuli appearing at aversively associated locations along with location-selective facilitation of response systems indexed by pupil diameter and EEG alpha power. These findings highlight the experience-dependent flexibility of retinotopic spatial representations in visual cortex, opening avenues towards novel treatment targets in disorders of attention and spatial cognition.