Forward model deficits and enhanced motor noise in Tourette syndrome?

Sir, We read with great interest the manuscript entitled ‘Impaired forward model updating in young adults with Tourette syndrome’ by Kim et al. (2019). Based on our own previous work (Ostendorf et al., 2010) and common practice in the literature, we wish to highlight three aspects of their study design in light of which the authors’ main conclusion of ‘less precise forward models [. . .] in individuals with Tourette syndrome’ (Kim et al., 2019) may be premature. Kim et al. (2019) compared performance of adolescents with Tourette syndrome versus healthy matched control subjects in a variant of a classic oculomotor paradigm (Hallett and Lightstone, 1976), the double-step task, which they adapted for pointing movements of the arm. They asked participants to point to the remembered location of a briefly presented visual target and then return to the remembered starting position of that movement. As movement kinematics inevitably vary from one repetition to the next, the second, return movement relied on monitoring metrics of the first. Given that hands were occluded from sight, the authors assumed this monitoring depended on estimates provided by an internal forward model. In support of this proposition, healthy subjects compensate for targeting errors of the first eye movement in oculomotor double-step tasks by adjusting second saccade metrics (Joiner, 2010), an ability that is impaired with dysfunctional internal monitoring pathways (Sommer and Wurtz, 2004; Ostendorf et al., 2010). While endpoint accuracy and variability of the first, outward movement were not significantly different between patients and controls, endpoints of the second, return movement were significantly less accurate and more variable in patients [a statistical test of a group (patients, controls) movement (outward, return) interaction effect was not reported, i.e. a confirmation that any performance deficit in Tourette syndrome is indeed specific to the second movement]. The authors interpreted these results as reflecting a deficit in estimating the endpoint of the first, outward movement via an internal forward model. An additional analysis demonstrated that the second, return movement partially compensated for trial-by-trial variability in first movement errors. Crucially, this correction did not differ between patients and control subjects (i.e. non-significant interaction of group error-estimate-type), hampering strong conclusions on forward model deficits in patients with Tourette syndrome. Forward models are considered critical for accurate, precise and adaptive motor control (Shadmehr et al., 2010; Franklin and Wolpert, 2011). Given that our motor commands are subject to noise, and motor execution is often perturbed, e.g. by a heavier-than-expected load, ongoing movements have to be monitored and, if necessary, corrected in order to fulfil their goals. However, due to sensory conduction delays, any correction that relies purely on sensory feedback is potentially outdated by the time it takes effect (Franklin and Wolpert, 2011). An internal model of the mechanics of our body and the environment, on the other hand, can simulate kinematics and dynamics that doi:10.1093/brain/awz266 BRAIN 2019: 142; 1–3 | e53