Conditioned up and down modulations of short latency gamma band oscillations in visual cortex during fear learning in humans

Abstract

Over the course of evolution, the human brain has been shaped to prioritize cues that signal potential danger. Thereby, the brain does not only favor species-specific prepared stimulus sets such as snakes or spiders but can learn associations between new cues and aversive outcomes. One important mechanism to achieve this is associated with learning induced plasticity changes in sensory cortex that optimizes the representation of motivationally relevant sensory stimuli. Animal studies have shown that the modulation of gamma band oscillations predicts plasticity changes in sensory cortices by shifting neurons’ responses to fear relevant features as acquired by Pavlovian fear conditioning. Here, we report conditioned gamma band modulations in humans during fear conditioning of orthogonally oriented sine gratings representing fear relevant and irrelevant conditioned cues. Thereby, pairing of a sine grating with an aversive loud noise not only increased short latency (during the first 180 ms) evoked visual gamma band responses, but was also accompanied by strong gamma power reductions for the fear irrelevant control grating. The current findings will be discussed in the light of recent neurobiological models of plasticity changes in sensory cortices and classic learning models such as the Rescorla–Wagner framework.

Oscillatory and non‐oscillatory brain activity reflects fear expression in an immediate and delayed fear extinction task

“…Our observations fit well into this framework. It is long known that threat‐predictive CS + induce central arousal, increase attention, and cause enhanced neural activity across the cortex (e.g., Antov et al, 2020; Armony, 2002; Santos‐Mayo et al, 2022; Yuan et al, 2018). Thus, the observed differences in the arrhythmic background spectrum between the CS + and CS − may reflect prioritized processing of the CS + , which is accomplished by amplified neural activity and leads to enhanced attention and increased arousal on the behavioral level.…”

Effects of Aversive Classical Conditioning on Pupil Dilation and Microsaccades

“…This work adds to a body of evidence suggesting early sensory systems are important targets of neural adaptation triggered by experienced aversive associations: In addition to visual (e.g. Friedl & Keil, 2020; 2021; McTeague, Gruss, & Keil, 2015; Santos-Mayo, de Echegaray, & Moratti, 2022), auditory (e.g. Letzkus et al 2011; Quirk, Armony, & LeDoux, 1997; Wood, Angeloni, Oxman, Clopath, & Geffen, 2022), and olfactory (You, Novak, Clancy, & Li, 2022) cortices, subcortical networks that drive eye movements and/or pupillary responses are implicated here.…”

Pavlovian conditioning-induced hallucinations reduce MMN amplitudes for duration but not frequency deviants

“…Therefore, the MMN reduction was induced by learning probably resulting in some short-term neuroplastic changes that affected the predictive coding process. Short-term neuroplastic changes by conditioning have been demonstrated in the auditory (e. g., Weinberger, 2015) and visual cortex (e. g. Santos-Mayo et al, 2022).…”

“…Fear conditioning results in short-term plasticity changes in the visual cortex in adult participants (e.g., Santos-Mayo et al, 2022). Therefore, it may be also possible that experiencing of AHs may result in neuroplastic changes in brain circuits that affect prediction error signalling and its associated MMN generation.…”