An afferent white matter pathway from the pulvinar to the amygdala facilitates fear recognition

Abstract

Our ability to rapidly detect threats is thought to be subserved by a subcortical pathway that quickly conveys visual information to the amygdala. This neural shortcut has been demonstrated in animals but has rarely been shown in the human brain. Importantly, it remains unclear whether such a pathway might influence neural activity and behavior. We conducted a multimodal neuroimaging study of 622 participants from the Human Connectome Project. We applied probabilistic tractography to diffusion-weighted images, reconstructing a subcortical pathway to the amygdala from the superior colliculus via the pulvinar. We then computationally modeled the flow of haemodynamic activity during a face-viewing task and found evidence for a functionally afferent pulvinar-amygdala pathway. Critically, individuals with greater fibre density in this pathway also had stronger dynamic coupling and enhanced fearful face recognition. Our findings provide converging evidence for the recruitment of an afferent subcortical pulvinar connection to the amygdala that facilitates fear recognition.Editorial note: This article has been through an editorial process in which the authors decide how to respond to the issues raised during peer review. The Reviewing Editor's assessment is that minor issues remain unresolved (see decision letter).

Neurophysiological and behavioural markers of compassion

“…In accordance with our data that compassion and criticism may recruit similar neural networks and regions, we suggest that the act of imagery generated while engaging in self-criticism may act upon similar subcortical routes for processing threatening stimuli in general, processes which may be stimulated automatically and unconsciously [42][43][44] . Interestingly, previous research has identified subconscious pathways for threat processing in the amygdala and visual cortex (lingual gyrus) apparent even under conditions of cortical blindness 45,46 , therefore we suggest that amygdala and lingual gyrus activation likewise identified within our research may subsume a similar route.…”

Direct structural connections between auditory and visual motion selective regions in humans

“…However, setting the same absolute threshold for different connections does not take into account that the probability of connections drops exponentially with the distance between the seed and target regions (101), or the difficulty to separate real from false connections (102). To take these into account, we compared the number of streamlines reconstructed by random tracking ('Null Distribution2' algorithm), with those generated by conventional tracking ('iFOD2' algorithm) (95,103). Since both algorithms conduct tractography using the same seed and target regions, we can directly compare the number of reconstructed streamlines between them without correcting for a possible difference in the distance between the seed and target regions or their sizes (95).…”

“…The only difference in the processing of data arises from the multi-shell nature of the acquisition as opposed to the single-shell acquisition of Dataset 1. Given the sample size, we selected a subset of 60 participants (~ half of the total sample) to create a representative population template and white matter mask (103). We used this template to normalize the white matter intensity of all 114 participants' dMRI volumes.…”

Ultra High Field fMRI of Human Superior Colliculi Activity during Affective Visual Processing

“…A recent study involving human participants has found greater activity in the SC when snake images are presented in the foveal compared to the peripheral visual field, consistent with the central bias in processing ecologically relevant threat stimuli 25 . In addition, in vivo diffusion tensor imaging and probabilistic tractography studies have predicted fiber connections between the human SC and the amygdala via the pulvinar, providing anatomical evidence supporting the SC's role in threat detection 22,[26][27][28] . SC activity is also influenced by descending projections from the extrastriate cortex, the midtemporal area, and the motor and premotor cortices in the primate brain 8,29 .…”

“…In humans and non-human primates, the SC has been proposed to play a role in rapid visual threat detection, as a part of the SC-pulvinar-amygdala subcortical magnocellular pathway [20][21][22][23] . Lesion experiments in infant monkeys have shown that the SC is involved in processing visually identifiable ecological threats 24 .…”