Increased scale-free and aperiodic neural activity during sensorimotor integration—a novel facet in Tourette syndrome

Abstract

Tourette syndrome is a common neurodevelopmental disorder defined by multiple motor and phonic tics. Tics in Tourette syndrome resemble spontaneously occurring movements in healthy controls and are therefore sometimes difficult to distinguish from these. Tics may in fact be mis-interpreted as a meaningful action, i.e. a signal with social content, whereas they lack such information and could be conceived a surplus of action or ‘motor noise’. These and other considerations have led to a ‘neural noise account’ of Tourette syndrome suggesting that the processing of neural noise and adaptation of the signal-to-noise ratio during information processing is relevant for the understanding of Tourette syndrome. So far, there is no direct evidence for this. Here, we tested the ‘neural noise account’ examining 1/ f noise, also called scale-free neural activity as well as aperiodic activity, in n = 74 children, adolescents and adults with Tourette syndrome and n = 74 healthy controls during task performance using EEG data recorded during a sensorimotor integration task. In keeping with results of a previous study in adults with Tourette syndrome, behavioural data confirmed that sensorimotor integration was also stronger in this larger Tourette syndrome cohort underscoring the relevance of perceptual-action processes in this disorder. More importantly, we show that 1/ f noise and aperiodic activity during sensorimotor processing is increased in patients with Tourette syndrome supporting the ‘neural noise account’. This implies that asynchronous/aperiodic neural activity during sensorimotor integration is stronger in patients with Tourette syndrome compared to healthy controls, which is probably related to abnormalities of GABAergic and dopaminergic transmission in these patients. Differences in 1/ f noise and aperiodic activity between patients with Tourette syndrome and healthy controls were driven by high-frequency oscillations and not lower-frequency activity currently discussed to be important in the pathophysiology of tics. This and the fact that Bayesian statistics showed that there is evidence for the absence of a correlation between neural noise and clinical measures of tics, suggest that increased 1/ f noise and aperiodic activity are not directly related to tics but rather represents a novel facet of Tourette syndrome.

The aperiodic exponent of subthalamic field potentials reflects excitation/inhibition balance in Parkinsonism: a cross-species study in vivo

“…Only recently did the aperiodic exponent gain more attention and was attributed a physiological meaning. Aperiodic exponents in LFP, EEG and ECoG recordings vary by age (He et al, 2019; Schaworonkow and Voytek, 2021; Voytek et al, 2015), cortical depth (Halgren et al, 2021), psychiatric disorders (Adelhöfer et al, 2021; Molina et al, 2020; Robertson et al, 2019; Veerakumar et al, 2019) and Parkinson’s disease (PD) (Mostile et al, 2019). They track sensory stimuli (Waschke et al, 2021) and change with movement (Belova et al, 2021).…”

Tourette syndrome research highlights from 2021

“…Another study using EEG was conducted to calculate scale-free activity (1/ f neural noise) based on the theory that tics are behavioral surplus, or “motor noise”. 56 Although task-related 1/ f noise and high-frequency band aperiodic activity were found to be increased in patients with TS during sensory-motor processing, there was no evidence that scale-free and aperiodic activity was related to the process of tic development. The authors suggested that increased 1/ f noise and aperiodic activity are not directly related to tics, but more likely related to a new aspect of TS.…”

Profiling the low-beta characteristics of the subthalamic nucleus in early- and late-onset Parkinson’s disease

“…The aperiodic exponent has been related to the integration of the synaptic currents ( Buzsáki et al, 2012 ). Recent studies have found the 1/f-like aperiodic components, which had been considered as noise before, have a unique function and are associated with brain activity ( Adelhöfer et al, 2021 ; Zhang et al, 2021 ) and age ( Voytek et al, 2015 ; Schaworonkow and Voytek, 2021 ). Here, our study found the results analogous to previous research, in which offset ( r = 0.305, corrected p = 0.047, Figure 5A ) and exponent ( r = 0.271, corrected p = 0.050, Figure 5B ) were positively correlated with age.…”