The cerebellum predicts the temporal consequences of observed motor acts

Abstract

It is increasingly clear that we extract patterns of temporal regularity between events to optimize information processing. The ability to extract temporal patterns and regularity of events is referred as temporal expectation. Temporal expectation activates the same cerebral network usually engaged in action selection, comprising cerebellum. However, it is unclear whether the cerebellum is directly involved in temporal expectation, when timing information is processed to make predictions on the outcome of a motor act. Healthy volunteers received one session of either active (inhibitory, 1 Hz) or sham repetitive transcranial magnetic stimulation covering the right lateral cerebellum prior the execution of a temporal expectation task. Subjects were asked to predict the end of a visually perceived human body motion (right hand handwriting) and of an inanimate object motion (a moving circle reaching a target). Videos representing movements were shown in full; the actual tasks consisted of watching the same videos, but interrupted after a variable interval from its onset by a dark interval of variable duration. During the 'dark' interval, subjects were asked to indicate when the movement represented in the video reached its end by clicking on the spacebar of the keyboard. Performance on the timing task was analyzed measuring the absolute value of timing error, the coefficient of variability and the percentage of anticipation responses. The active group exhibited greater absolute timing error compared with the sham group only in the human body motion task. Our findings suggest that the cerebellum is engaged in cognitive and perceptual domains that are strictly connected to motor control.

Fig 1. A schematic view of the experimental design.

Healthy volunteers received one session of either active, inhibitory, 1Hz (Group1) or sham (Group2) repetitive transcranial magnetic stimulation (rTMS) covering the right lateral cerebellum prior the execution of a temporal expectation task. Two videos were shown once to the subjects: “writing” video showed a common movement of a human body segment (a right hand writing a sentence), while “ball” video showed a movement of an inanimate object (a ball reaching a target). The task consisted in watching the same video, but interrupted, after a variable interval from its onset by a dark interval of variable duration (6, 9 and 12 seconds). During the dark interval subjects were required to judge the duration of video clicking on space bar when they reckoned that the movement had reached its end.

Fig 2. Effect of 1Hz-rTMS and Sham rTMS on lateral cerebellum on the absolute value of timing error.

Abscissa: the type of conditioning stimulation (1Hz-rTMS and Sham). Ordinate: the duration of the absolute value of error expressed as percentage of the duration the target interval. Panel A depicts the results of the human body motion perceptual task, whereas panel B depicts the results of the inanimate object motion task. Colours code the duration of the dark interval: dark grey, 6 seconds; light grey, 9 seconds; white, 12 seconds. Mean data + standard error mean (SEM) are shown. Asterisks indicate that the absolute timing error, at all target intervals, was significant larger in the human body motion task (handwriting) with respect to sham (*p<0.05).”

Fig 3. Effect of 1Hz-rTMS and Sham rTMS on lateral cerebellum on the coefficient of variability calculated as standard deviation/mean of the reproduced intervals.

Abscissa: the type of conditioning stimulation (1Hz-rTMS and Sham). Ordinate: the value of the coefficient of variability. Panel A depicts the results of the human body motion perceptual task, whereas panel B depicts the results of the inanimate object motion task. Colours code the duration of the dark interval: dark grey, 6 seconds; light grey, 9 seconds; white, 12 seconds. Mean data + standard error mean (SEM) are shown.

Fig 4. Effect of 1Hz-rTMS and Sham rTMS on lateral cerebellum on the percentage of responses in anticipation.

Abscissa: the type of conditioning stimulation (1Hz-rTMS and Sham). Ordinate: the percentage of the response in anticipation with respect to the total number of trials. Panel A depicts the results of the human body motion perceptual task, whereas panel B depicts the results of the inanimate object motion task. Colours code the duration of the dark interval: dark grey, 6 seconds; light grey, 9 seconds; white, 12 seconds. Mean data + standard error mean (SEM) are shown.