Action perception recruits the cerebellum and is impaired in patients with spinocerebellar ataxia

Abdelgabar, Abdel R.; Suttrup, Judith; Broersen, Robin; Bhandari, Ritu; Picard, Samuel; Keysers, Christian; Zeeuw, Chris I. De; Gazzola, Valeria

doi:10.1093/brain/awz337

Cited by 43 publications

(33 citation statements)

References 80 publications

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“…1 D ; peak at: −18, −16, 78; t (29) = 4.82; p < 0.001, q(FDR) < 0.05; cluster size = 383) and cerebellum ( Table 3 ). This part of the cerebellum (lobule 6) is known to be involved in mirroring and observation of bodily actions of others ( Van Overwalle et al, 2014 ; Abdelgabar et al, 2019 ). Stronger coupling of vPMC containing orofacial motor cortex and cerebellum to anterior insula supports “mirroring” as a likely mechanism for the autonomic and emotional reaction in misophonia mediated by the anterior insula.…”

Section: Resultsmentioning

confidence: 99%

The Motor Basis for Misophonia

et al. 2021

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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.

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Section: Resultsmentioning

confidence: 99%

The Motor Basis for Misophonia

et al. 2021

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“…2010 ), cerebellar ischemia ( Cattaneo et al. 2012 ), or spinocerebellar ataxia ( Abdelgabar et al. 2019 ), can affect the ability of the patients to identify others’ actions.…”

Section: Introductionmentioning

confidence: 99%

Functional Imaging of the Cerebellum during Action Execution and Observation

Raos

Savaki

2021

Cerebral Cortex Communications

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We employed the 14C-deoxyglucose autoradiographic method to map the activity in the cerebellar cortex of rhesus monkeys who performed forelimb movements either in the light or in the dark, and of monkeys who observed forelimb movements executed by a human experimenter. The execution of forelimb movements, both in the light and in the dark, activated the forelimb representations in the cerebellar hemispheric extensions of (i) vermian lobules IV-VI and (ii) vermian lobule VIIIB, ipsilaterally to the moving forelimb. Activations in the former forelimb representation involved both a paravermal and a lateral hemispheric region. Also, Crus II posterior in the ansiform lobule (the hemispheric expansion of lobule VIIB) was activated bilaterally by execution of movements in the light but not in the dark. Action observation activated the lateralmost region of the forelimb representation in the lateral hemispheric extension of vermian lobules IV-VI, as well as the crus II posterior, bilaterally. Our results demonstrate that the cerebellar cortex, in addition to its involvement in the generation of movement, is also recruited in the perception of observed movements. Moreover, our findings suggest a modularity gradient in the primate cerebellar cortex, which progresses from unimodal (medially) to multimodal (laterally) functional areas.

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“…In general terms, the finding of normal eyeblink conditioning in people with dystonia does reveal that there must be a relative subtlety to any cerebellar involvement in dystonia. Neurodegenerative disorders such as spinocerebellar ataxia (type 6) affect the cerebellum relatively uniformly and are associated with broad functional impairments ranging from delayed eyeblink conditioning and force adaptation in reaching [24][25][26][27][28] and to abnormalities in predictive timing in sequence control 29 and cognition 30,31 . More circumscribed cerebellar deficits, e.g.…”

Section: Discussionmentioning

confidence: 99%

The final blink: intact eyeblink conditioning in isolated dystonia

Sadnicka

Rocchi

Latorre

et al. 2021

Preprint

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Impaired eyeblink conditioning is often cited as evidence for cerebellar dysfunction in isolated dystonia. However, the results from individual studies are conflicting and underpowered. This collaborative project collated all published data and systematically re-examined the contribution of the predictors dystonia and its subtypes within a statistical model which controlled for the co-variates age and sex. Original neurophysiological data were shared and a sex and age matched control group were collected (dystonia n=52, controls n=50). Two raters blinded to participant identity rescored all recordings (6732 trials). After high inter-rater agreement was confirmed, mean conditioning per block was entered into a mixed repetitive measures model to evaluate the influence of sex, age, dystonia subtype (focal hand dystonia, cervical dystonia, DYT-TOR1A and DYT-THAP1) and clinical features such as tremor. There was a wide range of conditioning behavior across individuals in both groups. Young age (p=0.031) was associated with higher conditioning. All dystonia versus controls showed no difference in conditioning (p=0.517). Analysis of dystonia subgroup, with age and sex as co-variates, showed that conditioning in cervical dystonia, focal hand dystonia and DYT-TOR1A was comparable to controls. DYT-THAP1 was characterized by high levels of conditioning. Clinical features such as tremor did not significantly influence conditioning. Sample size estimates for future work are provided based on the variance observed. Eyeblink conditioning, a proxy for cerebellar function, appears intact in the subtypes of isolated dystonia examined. Precise mechanisms for how the cerebellum interplays mechanistically with other key neuroanatomical nodes within the dystonic network remains elusive.

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Action perception recruits the cerebellum and is impaired in patients with spinocerebellar ataxia

Cited by 43 publications

References 80 publications

The Motor Basis for Misophonia

The Motor Basis for Misophonia

Functional Imaging of the Cerebellum during Action Execution and Observation

The final blink: intact eyeblink conditioning in isolated dystonia

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