A human colliculus-pulvinar-amygdala pathway encodes negative emotion

• Type of Material: Article
• Authors: Philip Kragel, Emory University; Marta Čeko, University of Colorado Boulder; Jordan Theriault, Northeastern University; Danlei Chen, Northeastern University; Ajay B Satpute, Northeastern University; Lawrence W Wald, Massachusetts General Hospital; Martin A Lindquist, Johns Hopkins University; Lisa Feldman Barrett, Northeastern University; Tor D Wager, University of Colorado Boulder
• Language: English
• Date: 2021-08-04
• Publisher: Emory University Libraries
• Publication Version: Author Accepted Manuscript (After Peer Review)
• Copyright Statement: © 2021 Elsevier Inc.
• License: Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International
• Final Published Version (URL): http://dx.doi.org/10.1016/j.neuron.2021.06.001
• Title of Journal or Parent Work: Neuron
• Volume: 109
• Issue: 15
• Start Page: 2404
• End Page: 2412.e5
• Grant/Funding Information: This work was supported by the National Institutes of Health grants R01 MH076136, DA046064, MH116026, and EB026549 and National Cancer Institute grant U01 CA193632.
• Keywords: multivariate pathway identification; fMRI; pulvinar; amygdala; Humans; Emotions; functional connectivity; negative emotion; superior colliculus; Amygdala; Pulvinar; Superior Colliculi; Magnetic Resonance Imaging; Neural Pathways

Abstract

Animals must rapidly respond to threats to survive. In rodents, threat-related signals are processed through a subcortical pathway from the superior colliculus to the amygdala, a putative “low road” to affective behavior. This pathway has not been well characterized in humans. We developed a novel pathway identification framework that uses pattern recognition to identify connected neural populations and optimize measurement of inter-region connectivity. We first verified that the model identifies known thalamocortical pathways with high sensitivity and specificity in 7 T (n = 56) and 3 T (n = 48) fMRI experiments. Then we identified a human functional superior colliculus-pulvinar-amygdala pathway. Activity in this pathway encodes the intensity of normative emotional responses to negative images and sounds but not pleasant images or painful stimuli. These results provide a functional description of a human “low road” pathway selective for negative exteroceptive events and demonstrate a promising method for characterizing human functional brain pathways.