Predictive Modeling by the Cerebellum Improves Proprioception

Abstract

Because sensation is delayed, real-time movement control requires not just sensing, but also predicting limb position, a function hypothesized for the cerebellum. Such cerebellar predictions could contribute to perception of limb position (i.e., proprioception), particularly when a person actively moves the limb. Here we show that human cerebellar patients have proprioceptive deficits compared with controls during active movement, but not when the arm is moved passively. Furthermore, when healthy subjects move in a force field with unpredictable dynamics, they have active proprioceptive deficits similar to cerebellar patients. Therefore, muscle activity alone is likely insufficient to enhance proprioception and predictability (i.e., an internal model of the body and environment) is important for active movement to benefit proprioception. We conclude that cerebellar patients have an active proprioceptive deficit consistent with disrupted movement prediction rather than an inability to generally enhance peripheral proprioceptive signals during action and suggest that active proprioceptive deficits should be considered a fundamental cerebellar impairment of clinical importance.

Gait asymmetry during early split-belt walking is related to perception of belt speed difference

“…A role in the (predictive) integration of feedback inputs could explain the increased perception threshold we observed in these patients. This is supported by observations of impaired proprioception in severely ataxic cerebellar patients (Bhanpuri et al 2013;Maschke et al 2003). It is also supported by data from pointing and reaching experiments in less affected patients (Izawa et al 2012;Synofzik et al 2008).…”

“…In contrast to the cerebellar patient studies mentioned above (Bhanpuri et al 2013;Maschke et al 2003), we included patients with focal cerebellar lesions who were only mildly ataxic. This had a purpose because, in general, more localized lesions will result in more specific deficits but also less prominent ones.…”

“…This is of interest in relation to cerebellar patients. Severely ataxic patients with diffuse cerebellar damage have been observed to demonstrate deficits in locomotor adaptation (Morton and Bastian 2006) and also in proprioception (Bhanpuri et al 2013;Boisgontier and Swinnen 2014). In a companion article (Hoogkamer et al 2015), we evaluated split-belt adaptation in mildly ataxic patients with focal lesions in the cerebellum.…”

Assessing Proprioception

“…The unconscious component, controlled partially by the cerebellum, is seen soon after the infant gains neck movement control. It can be assessed by tilting body on one side and observing the eyes leveled to a horizontal line by tilting the head to opposite side (Bhanpuri, Okamura, & Bastian, 2013).…”

Muscle fatigue as an investigative tool in motor control: A review with new insights on internal models and posture–movement coordination

“…Altogether, these examples are evidence that the motor commands sent to the muscles are known by the CNS before movement onset. The internal models responsible for such predictions have been proposed to be located in the cerebellum (Bastian, 2006;Bhanpuri, Okamura, & Bastian, 2013;Cerminara, Apps, & Marple-Horvat, 2009;Diedrichsen, Verstynen, Lehman, & Ivry, 2005;Wolpert, Miall, & Kawato, 1998) and in the parietal cortex (Desmurget & Sirigu, 2009;Sirigu, Daprati, Pradat-Diehl, Franck, & Jeannerod, 1999;Wolpert, Goodbody, & Husain, 1998) (For reviews tackling these two views, see Desmurget & Grafton, 2000 as well as Blakemore & Sirigu, 2003). Regarding cerebellar internal models, neuroimaging studies have shown the strong involvement of the cerebellum during both eye-hand tracking motions (Miall & Reckess, 2002) and grip force-load force coupling (Tamada, Miyauchi, Imamizu, Yoshioka, & Kawato, 1999).…”