Dataset Information

A Bayesian Account of the Sensory-Motor Interactions Underlying Symptoms of Tourette Syndrome.

ABSTRACT: Tourette syndrome is a hyperkinetic movement disorder. Characteristic features include tics, recurrent movements that are experienced as compulsive and "unwilled"; uncomfortable premonitory sensations that resolve through tic release; and often, the ability to suppress tics temporarily. We demonstrate how these symptoms and features can be understood in terms of aberrant predictive (Bayesian) processing in hierarchical neural systems, explaining specifically: why tics arise, their "unvoluntary" nature, how premonitory sensations emerge, and why tic suppression works-sometimes. In our model, premonitory sensations and tics are generated through over-precise priors for sensation and action within somatomotor regions of the striatum. Abnormally high precision of priors arises through the dysfunctional synaptic integration of cortical inputs. These priors for sensation and action are projected into primary sensory and motor areas, triggering premonitory sensations and tics, which in turn elicit prediction errors for unexpected feelings and movements. We propose experimental paradigms to validate this Bayesian account of tics. Our model integrates behavioural, neuroimaging, and computational approaches to provide mechanistic insight into the pathophysiological basis of Tourette syndrome.

SUBMITTER: Rae CL

PROVIDER: S-EPMC6412155 | biostudies-other | 2019

REPOSITORIES: biostudies-other

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A Bayesian Account of the Sensory-Motor Interactions Underlying Symptoms of Tourette Syndrome.

Rae Charlotte L CL Critchley Hugo D HD Seth Anil K AK

Frontiers in psychiatry 20190305

Tourette syndrome is a hyperkinetic movement disorder. Characteristic features include tics, recurrent movements that are experienced as compulsive and "unwilled"; uncomfortable premonitory sensations that resolve through tic release; and often, the ability to suppress tics temporarily. We demonstrate how these symptoms and features can be understood in terms of aberrant predictive (Bayesian) processing in hierarchical neural systems, explaining specifically: why tics arise, their "unvoluntary" ...[more]

PMID: 30890965

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Project description:Objective: Tourette syndrome (TS) is a complicated sensorimotor disorder. Some patients with TS relieve their involuntary premonitory urges via tics. However, the effect of the motor system on the sensory system has not yet been elucidated. The purpose of the present study was to investigate changes in the excitability of the sensory cortex following repetitive transcranial magnetic stimulation (rTMS) of the motor cortex in patients with TS. Methods: Twenty-nine patients with TS and 20 healthy, age-matched controls were enrolled in this study. All subjects were divided into four groups: patients with rTMS, patients with sham-rTMS, controls with rTMS, and controls with sham-rTMS. The clinical severity of tics was evaluated using the Yale Global Tic Severity Scale. Single somatosensory evoked potentials (SEPs) and paired SEPs were recorded by stimulating the median nerve at the wrist of all subjects. The resting motor threshold (RMT) was tested in each subject in the rTMS group. Afterwards, all four groups were administered rTMS (1 Hz, 90% RMT) or sham-rTMS for 200 s, followed by a 15-min rest. Finally, single SEPs and paired SEPs were repeated for each subject. Results: No significant differences in RMT, the amplitudes of single SEPs, or the suppression of paired SEPs were observed between patients with TS and controls at baseline. After rTMS, a significant suppression of the peak-to-peak amplitude of the N20-P25 responses of single SEPs was observed in both controls (p = 0.049) and patients (p < 0.0001). The suppression of the N20-P25 peak-to-peak amplitude was more significant in patients than in controls (p = 0.039). A significant difference in the suppression of paired SEPs after rTMS was not observed between groups. Conclusions: The more significant suppression of N20-P25 components of single SEPs with normal suppressed paired SEPs in patients with TS after 1-Hz rTMS of the motor cortex suggests that the suppressive effect of the motor system on the sensory system might originate from the motor-sensory cortical circuits rather than the sensory system itself.

Project description:Tourette syndrome is a neurodevelopmental disorder, characterized by motor and phonic tics. Tics are typically experienced as avolitional, compulsive, and associated with premonitory urges. They are exacerbated by stress and can be triggered by external stimuli, including social cues like the actions and facial expressions of others. Importantly, emotional social stimuli, with angry facial stimuli potentially the most potent social threat cue, also trigger behavioural reactions in healthy individuals, suggesting that such mechanisms may be particularly sensitive in people with Tourette syndrome. Twenty-one participants with Tourette syndrome and 21 healthy controls underwent functional MRI while viewing faces wearing either neutral or angry expressions to quantify group differences in neural activity associated with processing social information. Simultaneous video recordings of participants during neuroimaging enabled us to model confounding effects of tics on task-related responses to the processing of faces. In both Tourette syndrome and control participants, face stimuli evoked enhanced activation within canonical face perception regions, including the occipital face area and fusiform face area. However, the Tourette syndrome group showed additional responses within the anterior insula to both neutral and angry faces. Functional connectivity during face viewing was then examined in a series of psychophysiological interactions. In participants with Tourette syndrome, the insula showed functional connectivity with a set of cortical regions previously implicated in tic generation: the presupplementary motor area, premotor cortex, primary motor cortex, and the putamen. Furthermore, insula functional connectivity with the globus pallidus and thalamus varied in proportion to tic severity, while supplementary motor area connectivity varied in proportion to premonitory sensations, with insula connectivity to these regions increasing to a greater extent in patients with worse symptom severity. In addition, the occipital face area showed increased functional connectivity in Tourette syndrome participants with posterior cortical regions, including primary somatosensory cortex, and occipital face area connectivity with primary somatosensory and primary motor cortices varied in proportion to tic severity. There were no significant psychophysiological interactions in controls. These findings highlight a potential mechanism in Tourette syndrome through which heightened representation within insular cortex of embodied affective social information may impact the reactivity of subcortical motor pathways, supporting programmed motor actions that are causally implicated in tic generation. Medicinal and psychological therapies that focus on reducing insular hyper-reactivity to social stimuli may have potential benefit for tic reduction in people with Tourette syndrome.

Project description:Experimental studies of speech production involving compensations for auditory and somatosensory perturbations and adaptation after training suggest that both types of sensory information are considered to plan and monitor speech production. Interestingly, individual sensory preferences have been observed in this context: subjects who compensate less for somatosensory perturbations compensate more for auditory perturbations, and vice versa. We propose to integrate this sensory preference phenomenon in a model of speech motor planning using a probabilistic model in which speech units are characterized both in auditory and somatosensory terms. Sensory preference is implemented in the model according to two approaches. In the first approach, which is often used in motor control models accounting for sensory integration, sensory preference is attributed to the relative precision (i.e., inverse of the variance) of the sensory characterization of the speech motor goals associated with phonological units (which are phonemes in the context of this paper). In the second, "more original" variant, sensory preference is implemented by modulating the sensitivity of the comparison between the predicted sensory consequences of motor commands and the sensory characterizations of the phonemes. We present simulation results using these two variants, in the context of the adaptation to an auditory perturbation, implemented in a 2-dimensional biomechanical model of the tongue. Simulation results show that both variants lead to qualitatively similar results. Distinguishing them experimentally would require precise analyses of partial compensation patterns. However, the second proposed variant implements sensory preference without changing the sensory characterizations of the phonemes. This dissociates sensory preference and sensory characterizations of the phonemes, and makes the account of sensory preference more flexible. Indeed, in the second variant the sensory characterizations of the phonemes can remain stable, when sensory preference varies as a response to cognitive or attentional control. This opens new perspectives for capturing speech production variability associated with aging, disorders and speaking conditions.

Project description:Youth with Tourette syndrome (TS) exhibit, compared to healthy, abnormal ability to lateralize digital sequential tasks. It is unknown whether this trait is related to inter-hemispheric connections, and whether it is preserved or lost in patients with TS persisting through adult life. We studied 13 adult TS patients and 15 age-matched healthy volunteers. All participants undertook: 1) a finger opposition task, performed with the right hand (RH) only or with both hands, using a sensor-engineered glove in synchrony with a metronome at 2 Hz; we calculated a lateralization index [(single RH-bimanual RH)/single RH X 100) for percentage of correct movements (%CORR); 2) MRI-based diffusion tensor imaging and probabilistic tractography of inter-hemispheric corpus callosum (CC) connections between supplementary motor areas (SMA) and primary motor cortices (M1). We confirmed a significant increase in the %CORR in RH in the bimanual vs. single task in TS patients (p<0.001), coupled to an abnormal ability to lateralize finger movements (significantly lower lateralization index for %CORR in TS patients, p = 0.04). The %CORR lateralization index correlated positively with tic severity measured with the Yale Global Tic Severity Scale (R = 0.55;p = 0.04). We detected a significantly higher fractional anisotropy (FA) in both the M1-M1 (p = 0.036) and the SMA-SMA (p = 0.018) callosal fibre tracts in TS patients. In healthy subjects, the %CORR lateralization index correlated positively with fractional anisotropy of SMA-SMA fibre tracts (R = 0.63, p = 0.02); this correlation was not significant in TS patients. TS patients exhibited an abnormal ability to lateralize finger movements in sequential tasks, which increased in accuracy when the task was performed bimanually. This abnormality persists throughout different age periods and appears dissociated from the transcallosal connectivity of motor cortical regions. The altered interhemispheric transfer of motor abilities in TS may be the result of compensatory processes linked to self-regulation of motor control.

Dataset Information

A Bayesian Account of the Sensory-Motor Interactions Underlying Symptoms of Tourette Syndrome.

Publications

A Bayesian Account of the Sensory-Motor Interactions Underlying Symptoms of Tourette Syndrome.

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