A subcortical pathway to the right amygdala mediating “unseen” fear

TLDR

Neuroimaging shows that the amygdala responds differently to masked emotional stimuli, yet the route by which unseen visual signals reach it remains unclear, with a potential superior colliculus–pulvinar pathway suggested by blindsight patients. The study aimed to determine whether a colliculo‑pulvinar pathway engages the right amygdala when processing unseen fear‑conditioned faces. The authors recorded right amygdala activity in volunteers viewing masked fear‑conditioned faces to assess engagement of a colliculo‑pulvinar pathway. Connectivity between the right amygdala, pulvinar, and superior colliculus increased for unseen versus seen fear‑conditioned faces, while connectivity with fusiform and orbitofrontal cortices decreased; the left amygdala showed no such changes, indicating a subcortical route to the right amygdala processes unseen visual events in parallel to a cortical route needed for conscious identification.

Abstract

Neuroimaging studies have shown differential amygdala responses to masked (“unseen”) emotional stimuli. How visual signals related to such unseen stimuli access the amygdala is unknown. A possible pathway, involving the superior colliculus and pulvinar, is suggested by observations of patients with striate cortex lesions who show preserved abilities to localize and discriminate visual stimuli that are not consciously perceived (“blindsight”). We used measures of right amygdala neural activity acquired from volunteer subjects viewing masked fear-conditioned faces to determine whether a colliculo-pulvinar pathway was engaged during processing of these unseen target stimuli. Increased connectivity between right amygdala, pulvinar, and superior colliculus was evident when fear-conditioned faces were unseen rather than seen. Right amygdala connectivity with fusiform and orbitofrontal cortices decreased in the same condition. By contrast, the left amygdala, whose activity did not discriminate seen and unseen fear-conditioned targets, showed no masking-dependent changes in connectivity with superior colliculus or pulvinar. These results suggest that a subcortical pathway to the right amygdala, via midbrain and thalamus, provides a route for processing behaviorally relevant unseen visual events in parallel to a cortical route necessary for conscious identification.