Cerebellar damage impairs detection of somatosensory input changes. A somatosensory mismatch-negativity study

Abstract

Several recent studies support the view that the cerebellum's contribution to sensory processing is not limited to movement regulation. In a previous paper (Restuccia D, Valeriani M, Barba C, Le Pera D, Capecci M, Filippini V, Molinari M. Functional changes of the primary somatosensory cortex in patients with unilateral cerebellar lesions. Brain 2001; 124: 757-68) we showed that the cerebellum influences somatosensory input processing at very early stages. The present study was aimed at verifying whether an analogous influence is also exerted at higher levels. For some time it has been known that in the auditory modality a specific event-related potential (ERP), that is, mismatch negativity (MMN), reflects preattentive detection of changes in the incoming stimulus by comparing the new stimulus with sensory memory traces. To test the cerebellar influence on the processing of incoming somatosensory stimuli we first verified whether the electrical stimulation of fingers, according to an 'oddball' paradigm within a stimulus-ignored condition, was able to elicit event-related components specifically linked to the preattentive detection of change. We analysed scalp responses obtained from eight healthy volunteers during frequent and rare electrical stimulation of the first and fifth finger of the left hand, respectively. To ensure that responses to deviant stimuli were due to changes in detection mechanisms, rather than to activation of new afferents, we also analysed responses to rare stimulation alone ('standard-omitted' condition). The 'oddball' stimulation was able to elicit a parieto-occipital extra negativity that was different in scalp distribution and latency from the N140 response to the 'standard-omitted' stimulation. We considered that this response was related to changes in detection mechanisms and labelled it somatosensory mismatch negativity (S-MMN). When the same procedure was applied to six patients with unilateral cerebellar lesions we found that the S-MMN was clearly abnormal after stimulation of the affected hand (ipsilateral to the affected cerebellar hemisphere). Earlier ERPs, as well as ERPs elicited during the 'standard-omitted' condition, were fully normal. Present data indicate that cerebellar processing is involved in preattentive detection of somatosensory input changes. In conclusion, this study demonstrates the reliability of S-MMN recordings and indicates that subjects with cerebellar damage may be impaired in the cortical processing of incoming somatosensory inputs.