Contributions of the Motor Cortex to Adaptive Control of Reaching Depend on the Perturbation Schedule

Abstract

During adaptation, motor commands tend to repeat as performance plateaus. It has been hypothesized that this repetition produces plasticity in the motor cortex (M1). Here, we considered a force field reaching paradigm, varied the perturbation schedule to potentially alter the amount of repetition, and quantified the interaction between disruption of M1 using transcranial magnetic stimulation (TMS) and the schedule of perturbations. In the abrupt condition (introduction of the perturbation on a single trial followed by constant perturbation), motor output adapted rapidly and was then followed by significant repetition as performance plateaued. TMS of M1 had no effect on the rapid adaptation phase but reduced adaptation at the plateau. In the intermediate condition (introduction of the perturbation over 45 trials), disruption of M1 had no effect on the phase in which motor output changed but again impaired adaptation when performance had plateaued. Finally, when the perturbation was imposed gradually (over 240 trials), the motor commands continuously changed during adaptation and never repeated, and disruption of M1 had no effect on performance. Therefore, TMS of M1 appeared to reduce adaptation of motor commands during a specific phase of learning: when motor commands tended to repeat.

Interactions Among Learning Stage, Retention, and Primary Motor Cortex Excitability in Motor Skill Learning

“…Our results agree with those of a previous study [19]. Previous study demonstrated that the disruption of the M1 function by TMS in the slow-learning stage of adaptive learning could impede the adaptation [12]. As mentioned above, the repeated use of optimal motor commands during the slow-learning stage induces changes in M1 excitability.…”

“…Masamizu et al (2014) found that accuracy of lever movement (forelimb movement learned through training) predicted from neuronal ensemble activity in layer 5a of the forelimb M1 improves during the late stage of learning [34]. Previous study demonstrated that the disruption of M1 function by TMS in the slow-learning stage of adaptive learning could reduce adaptation [12]. Taken together, these findings suggest that plastic changes in the M1 such as LTP or rewiring of the neuronal circuits might occur during the slow-learning stage.…”

“…Thus, we considered that changes in M1 excitability induced by motor skill learning might be learning stage dependent. A recent study suggested that same motor commands acquired during the fast-learning stage are repeatedly used to perform the task during the slow-learning stage [12]. Therefore, we hypothesized that changes in M1 excitability occur during the slow-learning stage because the M1 exhibits usedependent plasticity [13].…”

Modulation of error-sensitivity during a prism adaptation task in people with cerebellar degeneration

“…In a visuomotor reach adaptation paradigm, there are changes in the excitability of the human cerebellum during an abrupt protocol, but these changes are smaller in the gradual protocol (Schlerf et al 2012). Disruption of the human motor cortex impairs adaptation in the force field paradigm during an abrupt protocol, but the same disruption appears to spare adaptation during a gradual protocol in force fields (Orban de Xivry et al 2011) and visuomotor rotations (Hadipour-Niktarash et al 2007). The state of the human motor cortex and the corticospinal network, as measured by motor-evoked potentials, changes during adaptation in a force field paradigm with an abrupt protocol, but not with a gradual protocol (Orban de Xivry et al 2013).…”

Effects of Kinesthetic and Cutaneous Stimulation During the Learning of a Viscous Force Field

“…Recent studies have suggested that the rate of introduction of a perturbation may affect the duration of the after effects, the amount of retention, and the pattern of generalization [45]. Moreover, this may also call into play different neural substrates to drive the adaptation [46]. It is therefore possible that the rate of introduction of the perturbation, and the type of feedback, may interact to affect these factors as well.…”