Differential effects of cerebellar degeneration on feedforward versus feedback control across speech and reaching movements

Abstract

Errors that result from a mismatch between predicted movement outcomes and sensory afference are used to correct ongoing movements through feedback control and to adapt feedforward control of future movements. The cerebellum has been identified as a critical part of the neural circuit underlying implicit adaptation across a wide variety of movements (reaching, gait, eye movements, and speech). The contribution of this structure to feedback control is less well understood: although it has recently been shown in the speech domain that individuals with cerebellar degeneration produce even larger online corrections for sensory perturbations than control participants, similar behavior has not been observed in other motor domains. Currently, comparisons across domains are limited by different population samples and potential ceiling effects in existing tasks. To assess the relationship between changes in feedforward and feedback control associated with cerebellar degeneration across motor domains, we evaluated adaptive (feedforward) and compensatory (feedback) responses to sensory perturbations in reaching and speech production in individuals with cerebellar degeneration and neurobiologically healthy controls. As expected, the cerebellar group demonstrated impaired adaptation in both reaching and speech. In contrast, the groups did not differ in their compensatory response in either domain. Moreover, compensatory and adaptive responses in the cerebellar group were not correlated within or across motor domains. Together, these results point to a general impairment in feedforward control with spared feedback control in cerebellar degeneration. However, the magnitude of feedforward impairments and potential changes in feedback-based control manifest in a domain-specific manner across individuals.

Understanding implicit sensorimotor adaptation as a process of proprioceptive re-alignment

“…Adaptation was attenuated by around 30% in the latter condition (Figure 9A) (but see: (Avraham, Keizman, et al, 2020)). The impairment in sensorimotor adaptation in individuals with cerebellar pathology has also been mechanistically attributed to an impairment in generating sensory predictions (Figure 9B) (Criscimagna-Hemminger et al, 2010; Gibo et al, 2013; Hadjiosif et al, 2014; Izawa et al, 2012; Martin et al, 1996; Miall et al, 2007; Parrell et al, 2021; Singh et al, 2019; Tseng et al, 2007; Tzvi et al, 2021).…”

A single exposure to altered auditory feedback causes observable sensorimotor adaptation in speech

“…Here, we aim to further investigate the mechanisms underlying sensorimotor adaptation by measuring one-shot adaptation in speech. To detect this potentially small effect, data from six prior studies (Niziolek et al, 2014;Niziolek & Guenther, 2013;Niziolek & Parrell, 2021;Parrell et al, 2017Parrell et al, , 2021 were compiled for this analysis (131 total participants, 18-40 participants per study). In all studies, participants read aloud monosyllabic words while receiving real-time auditory playback of their speech.…”