The relation between neuronal firing, local field potentials and hemodynamic activity in the human amygdala in response to aversive dynamic visual stimuli

Tommaso Fedele,Athina Tzovara,Bettina Steiger,Peter Hilfiker,Thomas Grunwald,Lennart Stieglitz,Hennric Jokeit,Johannes Sarnthein

doi:10.1016/j.neuroimage.2020.116705

Abstract

The amygdala is a central part of networks of brain regions underlying perception and cognition, in particular related to processing of emotionally salient stimuli. Invasive electrophysiological and hemodynamic measurements are commonly used to evaluate functions of the human amygdala, but a comprehensive understanding of their relation is still lacking. Here, we aimed at investigating the link between fast and slow frequency amygdalar oscillations, neuronal firing and hemodynamic responses. To this aim, we recorded intracranial electroencephalography (iEEG), hemodynamic responses and single neuron activity from the amygdala of patients with epilepsy. Patients were presented with dynamic visual sequences of fearful faces (aversive condition), interleaved with sequences of neutral landscapes (neutral condition). Comparing responses to aversive versus neutral stimuli across participants, we observed enhanced high gamma power (HGP, >60 Hz) during the first 2 s of aversive sequence viewing, and reduced delta power (1–4 Hz) lasting up to 18 s. In 5 participants with implanted microwires, neuronal firing rates were enhanced following aversive stimuli, and exhibited positive correlation with HGP and hemodynamic responses. Our results show that high gamma power, neuronal firing and BOLD responses from the human amygdala are co-modulated. Our findings provide, for the first time, a comprehensive investigation of amygdalar responses to aversive stimuli, ranging from single-neuron spikes to local field potentials and hemodynamic responses.

Highlights

The human amygdala is a central hub of several networks underlying human perception and cognition
Our results show that high gamma power, neuronal firing and Blood Oxygen Level Dependent (BOLD) responses from the human amygdala are co-modulated
Neural oscillations in the amygdala have been well studied in rodents, in humans the vast majority of evidence stems from hemodynamic studies (Janak and Tye, 2015)

Summary

Introduction

The human amygdala is a central hub of several networks underlying human perception and cognition. Various tasks, such as novelty detection (Balderston et al, 2013), perception of faces (Adolphs and Spezio, 2006) and emotions (Wang et al, 2014), or aversive learning (Janak and Tye, 2015), rely on neural responses within the amygdala. Within the face perception network, the human amygdala is an important node (Duchaine and Yovel, 2015), but its role in dynamic face perception has been mainly investigated by means of Blood Oxygen Level Dependent (BOLD) responses (Krumhuber et al, 2013; Pitcher et al, 2019; Schacher et al, 2006), leaving its electrophysiological content severely under-explored (Zheng et al, 2017)

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