Investigating the Subcortical Route to the Amygdala Across Species and in Disordered Fear Responses

Abstract

Over the past few decades, evidence has come to light that there is a rapid subcortical shortcut that transmits visual information to the amygdala, effectively bypassing the visual cortex. This pathway purportedly runs from the superior colliculus to the amygdala via the pulvinar, and thus presents a methodological challenge to study noninvasively in the human brain. Here, we present our recent work where we reliably reconstructed the white matter structure and directional flow of neural signal along this pathway in over 600 healthy young adults. Critically, we found structure-function relationships for the pulvinar-amygdala connection, where people with greater fibre density had stronger functional neural coupling and were also better at recognising fearful facial expressions. These results tie together recent anatomical evidence from other visual primates with very recent optogenetic research on rodents demonstrating a functional role of this pathway in producing fear responses. Here, we discuss how this pathway might operate alongside other thalamo-cortical circuits (such as pulvinar to middle temporal area) and how its structure and function may change according to the sensory input it receives. This newly established circuit might play a potentially important role in autism and/or anxiety disorders.

Maternal cortisol is associated with neonatal amygdala microstructure and connectivity in a sexually dimorphic manner

“…In addition, as the network architecture underlying socio-emotional function in early life becomes more certain with technological advances, it may be useful to focus image analyses on individual networks. The subcortical-gaze pathway is of specific interest because in adults there is evidence that structural connectivity of the superior colliculus and amygdala is related to processing of facial expressions ( McFadyen, 2019 ), which is one of the earliest social cognitive abilities to develop and is foundational to other trajectories of cognitive development.…”

Visual Attention Software: A New Tool for Understanding the “Subliminal” Experience of the Built Environment

“…The retina itself is more than just a photoreceptor array: horizontal interconnectivity between retinal cells allows for that first level of processing, which is reflected in the relay station of the LGN, while further steps of spatial processing are taking place in the early visual cortical areas. About 10% of the retinal output takes another pathway, leading to the phylogenetically more primitive system of the superior colliculus and the pulvinar nucleus of the thalamus, responsible for early responses to motion in the peripheral visual field [26], as well as fear responses by direct input from the pulvinar to the amygdala, for example when sighting predators [27].…”

“…There is no contradiction here. We are wired to respond to threat before we know what we are looking at, including fear responses; for example when predators appear in our visual field [27]. After rapidly identifying the visual information, our brain can promote a further, conscious fearful response if appropriate.…”

The Role of the Thalamus in Post-Traumatic Stress Disorder

“…The geniculostriate system contributes to form (ventral stream) and space (dorsal stream) perception in visual processing. Both the geniculostriate and the retinotectal pathways contribute to visual processing, and the latter in particular mediates implicit processing of fearful stimuli [ 76 , 77 ]. Further research is needed to clarify the function of the retinotectal pathway; however, it has been demonstrated that this circuit contributes to fear learning [ 78 ].…”