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. 2021 Jun 30;41(26):5762-5770.
doi: 10.1523/JNEUROSCI.0261-21.2021. Epub 2021 May 21.

The Motor Basis for Misophonia

Affiliations

The Motor Basis for Misophonia

Sukhbinder Kumar et al. J Neurosci. .

Abstract

Misophonia is a common disorder characterized by the experience of strong negative emotions of anger and anxiety in response to certain everyday sounds, such as those generated by other people eating, drinking, and breathing. The commonplace nature of these "trigger" sounds makes misophonia a devastating disorder for sufferers and their families. How such innocuous sounds trigger this response is unknown. Since most trigger sounds are generated by orofacial movements (e.g., chewing) in others, we hypothesized that the mirror neuron system related to orofacial movements could underlie misophonia. We analyzed resting state fMRI (rs-fMRI) connectivity (N = 33, 16 females) and sound-evoked fMRI responses (N = 42, 29 females) in misophonia sufferers and controls. We demonstrate that, compared with controls, the misophonia group show no difference in auditory cortex responses to trigger sounds, but do show: (1) stronger rs-fMRI connectivity between both auditory and visual cortex and the ventral premotor cortex responsible for orofacial movements; (2) stronger functional connectivity between the auditory cortex and orofacial motor area during sound perception in general; and (3) stronger activation of the orofacial motor area, specifically, in response to trigger sounds. Our results support a model of misophonia based on "hyper-mirroring" of the orofacial actions of others with sounds being the "medium" via which action of others is excessively mirrored. Misophonia is therefore not an abreaction to sounds, per se, but a manifestation of activity in parts of the motor system involved in producing those sounds. This new framework to understand misophonia can explain behavioral and emotional responses and has important consequences for devising effective therapies.SIGNIFICANCE STATEMENT Conventionally, misophonia, literally "hatred of sounds" has been considered as a disorder of sound emotion processing, in which "simple" eating and chewing sounds produced by others cause negative emotional responses. Our data provide an alternative but complementary perspective on misophonia that emphasizes the action of the trigger-person rather than the sounds which are a byproduct of that action. Sounds, in this new perspective, are only a "medium" via which action of the triggering-person is mirrored onto the listener. This change in perspective has important consequences for devising therapies and treatment methods for misophonia. It suggests that, instead of focusing on sounds, which many existing therapies do, effective therapies should target the brain representation of movement.

Keywords: auditory; fMRI; mirror neurons; misophonia; motor system; resting state connectivity.

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Figures

Figure 1.
Figure 1.
Resting state functional connectivity of (A) right PT, (B) right V2, (C) right vPMC (the black curve in the top panel indicates the boundary of part of vPMC, which shows stronger connectivity to PT), and (D) left anterior insula. Connectivity of each of these seed regions was analyzed with the rest of the brain (seed-to-voxel analysis). The results shown are cluster-corrected with a cluster defining threshold of p = 0.001. The top row shows the seed regions; the middle two rows show the connectivity pattern overlaid on the sagittal and coronal sections of the structural image; the bottom row shows bar plots of connectivity strength in the two groups. Data in the bar plots represent mean ± SEM.
Figure 2.
Figure 2.
Sound-evoked functional connectivity of right orofacial motor cortex. The orofacial motor ROI (top) is selected from the resting state connectivity analysis. The two middle rows show brain regions with increased connectivity in the misophonia group in response to all sounds. Bar plot in the bottom row plots connectivity strengths in the two groups in response to sounds. The results shown are cluster-corrected with a cluster defining threshold of p = 0.001. Data in the bar plots represent mean ± SEM.
Figure 3.
Figure 3.
Activation of orofacial motor cortex and auditory cortex in response to three categories of sounds. Ai, The orofacial motor area represents a statistically significant (p = 0.002) group × sound category interaction. Aii, Bar plots represent β values for the orofacial motor cortex for the two groups in response to three sound categories. Aiii, Plots of variation of β values with the rating of misophonic distress in misophonia sufferers and of annoyance in control subjects. No group × sound category interaction is seen in the auditory cortex (B, middle column), which is confirmed by the bar plots of activation (B, first and third column) in response to sounds for the two groups. B, Middle column: white represents HG; black represents PT. Data in the bar plots represent mean ± SEM.

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