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

Alejandro Santos-Mayo,Stephan Moratti,Javier De Echegaray

doi:10.1038/s41598-022-06596-8

Alejandro Santos-Mayo, Stephan Moratti + Show 1 more

Open Access

https://doi.org/10.1038/s41598-022-06596-8

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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.

Highlights

Over the course of evolution, the human brain has been shaped to prioritize cues that signal potential danger
Detection rates did not depend on the experimental phase or condition (CS+ vs. conditioned stimuli (CS)−) as indicated by a non-significant interaction experimental phase by condition (F(2, 58) = 0.25, p = 0.771, ε = 0.97, η2 = 0.009)
We show that conditioned neural gain increases and decreases in the human visual cortex were greatest around 100 ms after stimulus onset for acquired fear relevant and irrelevant stimuli, respectively

Summary

Introduction

Over the course of evolution, the human brain has been shaped to prioritize cues that signal potential danger. Steady state responses have the advantage of high signal to noise ratios but lack sufficient time resolution in order to determine if these opposing neural gain modulations occur at short latency visual cortex responses These studies showed rather late latency effects on steady state power changes evoked by flickering stimuli just before US onset[6]. SsVEPs or ssVEFs likely represent reentrant oscillatory activity from higher to lower order visual cortex and it is difficult to disentangle at which processing stage these neural gain modulations occur[11] We extend these previous findings by investigating if such opposing adaptive neural gain changes for fear relevant and irrelevant visual stimuli, that facilitate best stimulus discrimination, occur during very early processing stages in the visual cortex. During extinction none of the conditioned stimuli were paired with the US (see Fig. 1A and “Methods” for a detailed description)

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