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.

Detecting violations of sensory expectancies following cerebellar degeneration: A mismatch negativity study

“…For instance, the two imaging studies that have reported cerebellar activation in an auditory duration MMN task used a fixed SOA (Dittmann-Balçar et al, 2001;Schall et al, 2003). A fixed SOA was also used in a study showing a diminished somatosensory MMN in patients with unilateral cerebellar damage (Restuccia et al, 2007). The present results suggest that these effects might be related to the periodicity of the stimuli.…”

“…In humans, two imaging studies have reported cerebellar activation in duration MMN paradigms (Dittman-Balçar et al, 2001;Schall et al, 2003). One patient study reported a diminished somatosensory mismatch response to deviant tactile stimuli applied to the affected (ipsilesional) hand of patients with unilateral cerebellar lesions compared to stimuli applied to the unaffected hand (Restuccia et al, 2007). In contrast, two of the patients showed normal MMN responses on an auditory task using a pitch deviant.…”

Understanding and supporting occupational therapists clinical decision-making for the management of upper limb post stoke sensory impairment

“…Restuccia et al (2007) concluded the cerebellum plays a role in pre-attentive detection of novel or deviant somatosensory stimuli, though consistent sensory impairment has not demonstrated with cerebellar impairments. Restuccia et al (2007) found reports of weight discrimination and kinaesthesia impairments as well as sensory dysgraphia resulting from cerebellar impairments. Further studies to understand the role the cerebellum plays and the impact of cerebellar lesions on somatosensory processing are needed.…”

“…The cerebellum also has an influence on inhibitory circuits in the S-I and may modulate receptive fields and hence optimise cutaneous discrimination (Restuccia et al, 2007). Restuccia et al (2007) concluded the cerebellum plays a role in pre-attentive detection of novel or deviant somatosensory stimuli, though consistent sensory impairment has not demonstrated with cerebellar impairments. Restuccia et al (2007) found reports of weight discrimination and kinaesthesia impairments as well as sensory dysgraphia resulting from cerebellar impairments.…”

“…Furthermore, it would also be important to actually see which sensory measures and interventions therapists are using to address ULPSSI and to understand their CDM as they choose how to address ULPSSI. & Hielman, 2008;Carey, 1995;Jacobs & Lowe, 1999; Kim, 2007;Restuccia, Marca, Valeriani, Leggio, & Molinari, 2007;Swenson, 2006;Yekutiel, 2000) Sensory impairments significantly limit the ability to use the upper limb after stroke. …”