Anticipatory cerebellar responses during somatosensory omission in man

The traditional view of cerebellum is a structure that modifies and synchronizes elements of motor performance. Recent evidence indicates that human cerebellum is involved in a wide range of nonmotor sensory and cognitive functions. A common feature in these diverse motor and nonmotor tasks may be the capacity of cerebellar neuronal circuits to process and anticipate sensory input with high temporal acuity. We present evidence supporting this hypothesis from measurements of the magnetic field at the scalp evoked by neuronal population activity in human cerebellum. Intermittent electrical stimulation of the finger and the median nerve elicited stimulus-locked cerebellar responses with oscillatory components at 6-12 Hz and 25-35 Hz. Sustained oscillatory activity followed random stimulus omissions, with initiation of cerebellar responses prior to the next overt stimulus. These responses indexed processing of temporal features of somatosensory input independent of motor performance or response. The refractory behavior of the responses suggested that a neuronal trace of the temporal pattern of somatosensory stimulation remained in cerebellar circuits for 2-4 s. The cerebellar activity elicited by violation of an established temporal pattern was enhanced when attention was directed to somatosensory stimuli, in concordance with recent imaging studies suggesting participation of cerebellum in attentional networks. The attentional enhancement of the cerebellar responses supports the salience of cerebellar activity in the processing of purely somatosensory input. The short-term maintenance of cerebellar templates for predictable sensory input may reflect a physiological substrate for fine-grained temporal tuning and optimization of performance in large-scale sensory and integrative systems.