Beyond Threat: Changes in Visuocortical Engagement and Oscillatory Brain Activity during Non-Aversive Associative Learning

Abstract

Aversive conditioning produces selectively heightened visuocortical responses to conditioned stimuli stimulus (CS) that predict aversive unconditioned events (US). However, it is unclear whether similar neural signatures emerge as a consequence of mere association formation between a CS-US pair, i.e., when a CS predicts a neutral event. To address this, we paired a soft tone (65 dB) with one of two high-contrast circular gratings (15{degrees} or 75{degrees}; CS+; counterbalanced), while two intermediate orientations (35{degrees}, 55{degrees}) were never paired with the neutral tone, serving as generalization stimuli (GS). A sample of 22 participants viewed each grating for 3000 ms, with the tone presented during the last 1000 ms of each grating presentation. Gratings were flickered (turned on and off) at a temporal rate of 15 Hz, to evoked steady-state Visual Evoked Potentials (ssVEPs), a metric of visuocortical engagement. Time-frequency decomposition via Morlet wavelets quantified changes in the amplitude of alpha-band (8-13 Hz) oscillations--an additional electrophysiological index that has been shown to be sensitive to aversive conditioning. Contrary to findings observed during aversive conditioning, alpha amplitude increased, rather than decreased, during CS+ trials relative to GSs. Likewise, ssVEP amplitude was higher for GSs than for the CS+, which again is the opposite of what is found during aversive conditioning. These findings suggest that a CS paired with non-aversive outcomes engages mechanisms consistent with working memory, anticipation, or imagery processes, reflected in heightened alpha amplitude and attenuated ssVEP, rather than the defensive potentiation observed during aversive conditioning.