Aim We instinctively look towards faces expressing strong emotions such as fear. This survival-critical response – potentially alerting us to danger – requires rapid detection (sensory) and orientation (motor) towards a face in advance of conscious recognition of the emotion. But the neural basis of this response is unclear. Correlative evidence suggests the amygdala may play a role, but rare studies of humans with chronic amygdala damage conflict variously reporting impaired,¹ unaffected² or heightened³ detection of fear. How the amygdala contributes to a spatially specific oculomotor response also requires explanation. We aimed to investigate the neural mechanisms underlying this instinctive response.

Methods We studied six patients with intracranial unilateral amygdala electrodes temporarily implanted for the clinical evaluation of focal epilepsy. We invited them to perform a custom behavioural task designed to dissociate the location of fearful face presentation (sensory) from the direction of the orientation response (motor). We recorded eye-movements with and without focal, transient, unilateral direct electrical disruption of the amygdala in a block design. Saccade latencies and choices were modelled with multi-level Bayesian models.

Results We analysed 1064 trials. Amygdala disruption delayed gaze shifts towards faces presented in the contralateral hemifield regardless of their emotional expression establishing the functional lateralisation of the human amygdala. Dissociating face location from response direction implicated the amygdala not only in detecting contralateral faces, but also in automatically orienting specifically towards fearful ones. This salience-specific role manifested, within a drift-diffusion model of action, as an orientation bias towards the location of potential threat. Pixel-wise analysis of target facial morphology revealed scleral exposure as its primary driver.

Conclusions 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, and inform novel focal stimulation techniques for the management of neuropsychiatric conditions.

References

1. Adolphs R, et al. Nature 1994;372:669–672.

2. Gamer M, et al. Curr Biol 2013;23:R917–R918.

3. Terburg D, et al. Transl Psychiatry 2012;2:e115–10.