Jha, Ashwani; Diehl, Beate; Strange, Bryan; Miserocchi, Anna; Chowdhury, Fahmida; McEvoy, Andrew W; Nachev, Parashkev; (2022) Orienting to fear under transient focal disruption of the human amygdala. Brain 10.1093/brain/awac032. (In press).

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Abstract

Responding to threat is under strong survival pressure, promoting the evolution of systems highly optimised for the task. Though the amygdala is implicated in detecting threat, its role in the action that immediately follows-orienting-remains unclear. Critical to mounting a targeted response, such early action requires speed, accuracy, and resilience optimally achieved through conserved, parsimonious, dedicated systems, insured against neural loss by a parallelized functional organisation. These characteristics tend to conceal the underlying substrate not only from correlative methods but also from focal disruption over time scales long enough for compensatory adaptation to take place. In a study of six patients with intracranial electrodes temporarily implanted for the clinical evaluation of focal epilepsy, here we investigate gaze orienting to fear during focal, transient, unilateral direct electrical disruption of the amygdala. We show that the amygdala is necessary for rapid gaze shifts towards faces presented in the contralateral hemifield regardless of their emotional expression, establishing its functional lateralisation. Behaviourally dissociating the location of presented fear from the direction of the response, we implicate the amygdala not only in detecting contralateral faces, but also in automatically orienting specifically towards fearful ones. This salience-specific role is demonstrated within a drift-diffusion model of action to manifest as an orientation bias towards the location of potential threat. Pixel-wise analysis of target facial morphology reveals scleral exposure as its primary driver, and induced gamma oscillations-obtained from intracranial local field potentials-as its time-locked electrophysiological correlate. The amygdala is here re-conceptualised as a functionally lateralised instrument of early action, reconciling previous conflicting accounts confined to detection, and revealing a neural organisation analogous to the superior colliculus, with which it is phylogenetically kin. Greater clarity on its role has the potential to guide therapeutic resection, still frequently complicated by impairments of cognition and behaviour related to threat, and inform novel focal stimulation techniques for the management of neuropsychiatric conditions.

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