title: A Rapid Subcortical Amygdala Route for Faces Irrespective of Spatial Frequency and Emotion.
abstract: There is significant controversy over the existence and function of a direct subcortical visual pathway to the amygdala. It is thought that this pathway rapidly transmits low spatial frequency information to the amygdala independently of the cortex, and yet the directionality of this function has never been determined. We used magnetoencephalography to measure neural activity while human participants discriminated the gender of neutral and fearful faces filtered for low or high spatial frequencies. We applied dynamic causal modeling to demonstrate that the most likely underlying neural network consisted of a pulvinar-amygdala connection that was uninfluenced by spatial frequency or emotion, and a cortical-amygdala connection that conveyed high spatial frequencies. Crucially, data-driven neural simulations revealed a clear temporal advantage of the subcortical connection over the cortical connection in influencing amygdala activity. Thus, our findings support the existence of a rapid subcortical pathway that is nonselective in terms of the spatial frequency or emotional content of faces. We propose that that the "coarseness" of the subcortical route may be better reframed as "generalized."SIGNIFICANCE STATEMENTThe human amygdala coordinates how we respond to biologically relevant stimuli, such as threat or reward. It has been postulated that the amygdala first receives visual input via a rapid subcortical route that conveys "coarse" information, namely, low spatial frequencies. For the first time, the present paper provides direction-specific evidence from computational modeling that the subcortical route plays a generalized role in visual processing by rapidly transmitting raw, unfiltered information directly to the amygdala. This calls into question a widely held assumption across human and animal research that fear responses are produced faster by low spatial frequencies. Our proposed mechanism suggests organisms quickly generate fear responses to a wide range of visual properties, heavily implicating future research on anxiety-prevention strategies.
authors.affiliation: Queensland Brain Institute, The University of Queensland, Brisbane, 4072, QLD, Australia, j.mcfadyen@uq.edu.au.|Centre for Advanced Imaging, The University of Queensland, Brisbane, 4072, QLD, Australia.|Australian Research Council Centre of Excellence for Integrative Brain Function.
authors.forename: Jessica
authors.identifier: 0000-0003-1415-2286
authors.initials: J
authors.lastname: McFadyen
authors.affiliation: Universite Grenoble Alpes, LPNC, F-38000 Grenoble, France and CNRS, LPNC, F-38000 Grenoble, France.|Institut Universitaire de France, Paris 75005, France.
authors.forename: Martial
authors.identifier: 0000-0003-4367-7049
authors.initials: M
authors.lastname: Mermillod
authors.affiliation: Queensland Brain Institute, The University of Queensland, Brisbane, 4072, QLD, Australia.|School of Psychology, The University of Queensland, Brisbane, 4072, QLD, Australia, and.
authors.forename: Jason B
authors.identifier: 0000-0003-0929-9216
authors.initials: JB
authors.lastname: Mattingley
authors.affiliation: Queensland Brain Institute, The University of Queensland, Brisbane, 4072, QLD, Australia.
authors.forename: Veronika
authors.identifier: 0000-0001-8750-8015
authors.initials: V
authors.lastname: Halász
authors.affiliation: Queensland Brain Institute, The University of Queensland, Brisbane, 4072, QLD, Australia.|Centre for Advanced Imaging, The University of Queensland, Brisbane, 4072, QLD, Australia.|Australian Research Council Centre of Excellence for Integrative Brain Function.|School of Mathematics and Physics, The University of Queensland, Brisbane, 4072, QLD, Australia.
authors.forename: Marta I
authors.identifier: 0000-0003-0679-4959
authors.initials: MI
authors.lastname: Garrido
mesh_terms: D000293:Adolescent; D000328:Adult; D000679:Amygdala / Q000502:physiology*; D004644:Emotions / Q000502:physiology*; D005149:Facial Expression; D005260:Female; D006801:Humans; D015225:Magnetoencephalography / Q000379:methods; D008297:Male; D010364:Pattern Recognition, Visual / Q000502:physiology*; D010775:Photic Stimulation / Q000379:methods; D065855:Spatial Processing / Q000502:physiology*; D013997:Time Factors; D014795:Visual Pathways / Q000502:physiology*; D055815:Young Adult
keywords: amygdala; dynamic causal modeling; emotion; faces; pulvinar; spatial frequency