Dissociating timing and coordination as functions of the cerebellum

Abstract

The function of the cerebellum in motor control is a long-standing puzzle because cerebellar damage is associated with both timing and coordination deficits. Timing is the ability to produce consistent intervals between movements based on an internal representation of time. Coordination, in contrast, is a state-dependent control process in which motor commands to one effector depend on the predicted state of another effector. Here we considered a task consisting of two components, an arm movement and an isometric press with the thumb. We found that when the two components temporally overlapped, the brain controlled the thumb using an estimate of the state of the arm. In contrast, when the components did not temporally overlap, the brain controlled the thumb solely based on an internal estimate of time. Using functional magnetic resonance imaging, we contrasted these two conditions and found that lobule V of the cerebellum ipsilateral to the arm movement was consistently more activated during state-dependent control. When the brain learned time-dependent control, no region of the cerebellum showed consistently increased activity compared with state-dependent control. Rather, the consistent activity associated with time-dependent control was found in language areas of the left cerebral hemisphere along the Sylvian fissure. We suggest that timing and coordination are behaviorally distinct modes of motor control and that the anterior cerebellum is a crucial node in state-dependent motor control, computing a predictive state estimate of one effector (e.g., the arm) to coordinate actions of another effector (the thumb).

Figures

Figure 1.

Unilateral thumb-arm task (experiment 1). A, Participants held the handle of a robotic arm and placed their thumb on a load cell. They were instructed to reach toward a visual target by moving a cursor and to produce a thumb press. Note that during the fMRI study, the task was performed bilaterally with the right arm and the left thumb. B, Visual feedback. After each trial, feedback about movement time was provided by an arrow, indicating whether the cursor reached the target in time, too early, or too late. If the movement time was within 65 ms of the goal, feedback was provided to indicate the relative timing (ΔT) of the two components (ellipse on the left side of the screen). C, Different groups of participants were trained to produce a thumb press (dashed line) in a specific temporal relationship to movement start (ΔT). D, Exemplary data of one participant in the ΔT = 350 ms group. The target movement time and ΔT are shown in dashed black lines. Six training blocks were followed by a spontaneous generalization test without feedback for ΔT (gray bar). A proportional transfer test (T1) and an absolute transfer test (T2) were separated by an interposed training block. E, State- and time-dependent control can be distinguished in how the skill generalizes to a slower movement. State-dependent control predicts that ΔT and the duration of the thumb press (black line) scale proportionally with movement time. Time-dependent control predicts that ΔT and the length of the thumb press do not change.

Figure 2.

Results of the unilateral coordination task (experiment 1) for 10 groups of participants, each trained on a different temporal interval between movement onset and thumb press (ΔT). Results for the two control groups (see text) are shown in white. A, B, Change in ΔT (A) and change in the duration of thumb press (B) from the last two training blocks to the first spontaneous generalization test. The gray line indicates the predicted change under the state-dependent control hypothesis, and the dashed line predicted the change under the time-dependent control hypothesis. C, D, Constant (C) and variable error (SD; D) of ΔT in the absolute and proportional transfer tests. Error bars indicate SEM. Cntrl, Control.

Figure 3.

Result of the bilateral coordination task (experiment 2). A, Change in ΔT from the last training block to the first spontaneous generalization test, and prediction of the state-dependent (gray line) and time-dependent control hypothesis (dashed line). B, C, Constant error (B) and variable error of ΔT (C) in the absolute and proportional transfer tests. Error bars indicate SEM.

Figure 4.

Cerebellar activity in experiments 3 and 4. A, Thumb-only task compared with rest. B, Arm-only task compared with rest. C, D, Contrast between state- and time-dependent control. Areas that were more activated during state-dependent control are shown in blue and areas more activated during time-dependent control are shown in red. Data are shown on coronal section of a high-resolution cerebellar atlas template (Diedrichsen, 2006). E, F, Bar graphs show the percentage of signal change in each of the four conditions (thumb-only, arm-only, time-dependent control, state-dependent) versus rest for left and right lobule V and lobule VI. The hemisphere ipsilateral to the thumb movement is shown in red, the hemisphere ipsilateral to the arm movement in blue. Error bars indicate SEM. Exp., Experiment.

Figure 5.

A, Areas of the cerebral hemispheres contralateral to the arm movement (left) and contralateral to the thumb movement (right) showing more activity during state-dependent control (blue). B, Areas in the left hemisphere showing more activation during time-dependent control (red). Group analysis was performed using a surface-based atlas and activity differences were thresholded at t(20) > 3.53, p < 0.001. C, Percentage of signal change versus rest for the four experimental conditions, for symmetric locations in experiments 3 and 4. The hemisphere contralateral to the arm movement is shown in blue, the hemisphere contralateral to the thumb movement is shown in red. Error bars indicate SEM. CiS, Cingulate sulcus; CS, central sulcus; IPS, intraparietal sulcus; PoCS, postcentral sulcus; SF, Sylvian fissure; SFS, superior frontal sulcus; STS, superior temporal sulcus; M1, primary motor cortex; SMA, supplementary motor area; PMd, dorsal premotor area; aIPS, anterior intraparietal sulcus; PT, planum temporale.