Active force perception depends on cerebellar function

Abstract

Damage to the cerebellum causes characteristic movement abnormalities but is thought to have minimal impact on somatosensory perception. Traditional clinical assessments of patients with cerebellar lesions reveal no perceptual deficits despite the fact that the cerebellum receives substantial somatosensory information. Given that abnormalities have been reported in predicting the visual consequences of movement, we suspect that the cerebellum broadly participates in perception when motor output is required (i.e., active perception). Thus we hypothesize that cerebellar integrity is essential for somatosensory perception that requires motor activity, but not passive somatosensory perception. We compared the perceptual acuity of human cerebellar patients to that of healthy control subjects in several different somatosensory perception tasks with minimal visual information. We found that patients were worse at active force and stiffness discrimination but similar to control subjects with regard to passive cutaneous force detection, passive proprioceptive detection, and passive proprioceptive discrimination. Furthermore, the severity of movement symptoms as assessed by a clinical exam was positively correlated with impairment of active force perception. Notably, within the context of these perceptual tasks, control subjects and cerebellar patients displayed similar movement characteristics, and hence differing movement strategies are unlikely to underlie the differences in perception. Our results are consistent with the hypothesis that the cerebellum is vital to sensory prediction of self-generated movement and suggest a general role for the cerebellum in multiple forms of active perception.

Fig. 1.

Task descriptions. A: tasks 1 and 2: torque and stiffness discrimination tasks. After subjects moved to start location, the robot applied elbow torques for 5 s. Subjects were instructed to keep movements within boundary lines (white bars located at elbow angles: 75° and 105°). Two environments were presented sequentially in each trial, and subjects reported which one was stronger. The label for each stimulus was indicated in the black square at the top left corner (I, magnitude one; II, magnitude two). B: task 3: position detection task. Robot-driven movements occurred while subjects remained passive; subjects reported if they felt a movement or not. A circular symbol changed color to indicate the end of the trial. C: task 4: position difference threshold task. Same as B with addition of second movement, and subjects reported which movement went farther. Gray arrows indicate passive, robot-driven movement, and black arrows indicate active, subject-driven movement. The light gray dotted lines depicting the arm of the subject are for illustrative purposes only, as vision of the arm was occluded throughout all tasks.

Fig. 2.

Conventions and example trials of perceptual tasks. A: schematic of conventions used to report elbow angle (θ_e) and applied torque (τ_e). The shoulder angle (θ_s) was fixed at 30° for all of the tasks. B and C: example trials of control (B) and cerebellar (C) subjects for torque discrimination task (1.20 Nm; 1st column), stiffness discrimination task (4.5 Nm/rad; 2nd column), position detection task (1.0° trial; 3rd column), and position discrimination task (10.0° trial; 4th column). Overhead view of fingertip position (top), elbow angle (middle), and commanded torque (bottom) are shown for given trials. Gray lines correspond to the visual boundary.

Fig. 3.

Cerebellar patients have impaired torque and stiffness perception but normal proprioception. A: torque Weber fraction (WF) was significantly higher for patient group (n = 11, P = 0.021). B: torque WFs were significantly correlated to International Cooperative Ataxia Rating Scale (ICARS) kinetic subscore of patients (n = 11, Pearson's correlation r = 0.72, P = 0.013). C: patients had a significantly higher average stiffness WF compared with matched control subjects (n = 11, P = 0.026). D: absolute threshold for position was similar across groups (n = 10, P = 0.89). Note that, because of limited availability, only 10 of 11 subjects from each group participated in task 3 (position detection). *P < 0.05. Error bars indicate SE.

Fig. 4.

Comparison of movement strategies during perceptual tasks. A: elbow angle vs. time profiles during example trials of task 1 for all subjects. Each subject is offset vertically from the others. Scaling is indicated by bars below A. B and C: maximum angle attained (B) and SD of angles (C) sampled during the single example trials. The vertical position corresponds to the profiles in A. D and E: comparison across groups of different average metrics across all trials for tasks 1 and 2 (torque and stiffness tasks): maximum angle (D) and SD (E) of angle. Error bars indicate SE. All comparisons between groups were not significant.

Fig. 5.

Comparison across tasks of subgroups that conducted the position discrimination task. A: torque WF was significantly higher for the patient subgroup (n = 6, P = 0.001). B: patient subgroup also had a significantly higher average stiffness WF compared with matched control subjects (n = 6, P = 0.006). C: WFs were similar in the proprioception task with a memory component (n = 6, P = 0.83). D: absolute threshold for position was similar across subgroups (n = 5, P = 0.56). Note that, because of limited availability, only 5 of 6 subjects from each subgroup participated in task 3 (position detection). *P < 0.05. Error bars indicate SE.