Sensory processing in Parkinson's and Huntington's disease

Abstract

There is conjoining experimental and clinical evidence supporting a fundamental role of the basal ganglia as a sensory analyser engaged in central somatosensory control. This study was aimed at investigating the functional anatomy of sensory processing in two clinical conditions characterized by basal ganglia dysfunction, i.e. Parkinson's and Huntington's disease. Based on previously recorded data of somatosensory evoked potentials, we expected deficient sensory-evoked activation in cortical areas that receive modulatory somatosensory input via the basal ganglia. Eight Parkinson's disease patients, eight Huntington's disease patients and eight healthy controls underwent repetitive H(2)(15)O-PET activation scans during two experimental conditions in random order: (i) continuous unilateral high-frequency vibratory stimulation applied to the immobilized metacarpal joint of the index finger and (ii) rest (no vibratory stimulus). In the control cohort, the activation pattern was lateralized to the side opposite to stimulus presentation, including cortical [primary sensory cortex (S1); secondary sensory cortex (S2)] and subcortical (globus pallidus, ventrolateral thalamus) regional cerebral blood flow (rCBF) increases (P < 0.001). Between-group comparisons (P < 0.01) of vibration-induced rCBF changes between patients and controls revealed differences in central sensory processing: (i) in Parkinson's disease, decreased activation of contralateral sensorimotor (S1/M1) and lateral premotor cortex, contralateral S2, contralateral posterior cingulate, bilateral prefrontal cortex (Brodmann area 10) and contralateral basal ganglia; (ii) in Huntington's disease, decreased activation of contralateral S2, parietal areas 39 and 40, and lingual gyrus, bilateral prefrontal cortex (Brodmann areas 8, 9, 10 and 44), S1 (trend only) and contralateral basal ganglia; (iii) in both clinical conditions relative enhanced activation of ipsilateral sensory cortical areas, notably caudal S1, S2 and insular cortex. Our data show that Parkinson's disease and Huntington's disease, beyond well-established deficits in central motor control, are characterized by abnormal cortical and subcortical activation on passive sensory stimulation. Furthermore, the finding that activation increases in ipsilateral sensory cortical areas may be interpreted as an indication of either altered central focusing and gating of sensory impulses, or enhanced compensatory recruitment of associative sensory areas in the presence of basal ganglia dysfunction. Altered sensory processing is thought to contribute to pertinent motor deficits in both conditions.

Early Huntington’s disease affects movements in transformed sensorimotor mappings

“…HD patients can show abnormal somatosensory processing (Abbruzzese, Dall'Agata, Morena, Reni, & Favale, 1990;Boecker et al, 1999;Kuwert et al, 1993;Topper, Schwarz, Podoll, Domges, & Noth, 1993). However, in patients with somatosensory deafferentation, impaired proprioception can actually facilitate mirror-inverted movements (Lajoie et al, 1992).…”

Control of manipulative forces during unimanual and bimanual tasks in patients with Huntington’s disease

“…Alternatively, a reduced efficiency of sensorimotor processing may induce an increased force specification. Disturbed sensorimotor activity in HD has been suggested because of a total suppression or reduced activity of the reactive EMG response (Fellows et al 1997;Noth et al 1985), an abnormal (sub)cortical activation during passive sensory stimulation (Boecker et al 1999), changes in somatosensory evoked potentials (Noth et al 1984;Töpper et al 1993) and deficits in feedback control when external perturbations are introduced during reaching movements (Smith et al 2000).…”

Dopaminergic contributions to distance estimation in Parkinson's disease: A sensory-perceptual deficit?

“…The basal ganglia (BG) are an important part of a complex neural network that processes and integrates various sensory inputs in order to produce and modulate motor outputs (Contreras-Vidal, 1999;Graziano & Gross, 1993;Houk & Wise, 1995;Nagy, Eordegh, Paroczy, Markus, & Benedek, 2006). Boecker and colleagues termed the BG a "sensory analyzer" engaged in central somatosensory control, suggesting interconnections between the cortex, BG and thalamus that make up an indirect BG-sensory loop (Boecker et al, 1999b). In Parkinson's disease (PD) there is a degeneration of dopaminergic neurons in the BG, specifically in the substantia nigra pars compacta, which impairs the basal ganglia-cortical circuitry.…”

“…Studies have shown that individuals with PD have abnormal processing of sensory information, specifically proprioceptive inputs (Klockgether et al, 1995;Rickards & Cody, 1997;Schneider et al, 1987;Zia et al, 2000). Abnormal vibration-induced movement errors have been observed in PD during joint flexion-extension tasks (Rickards & Cody, 1997;Schrader et al, 2008), and PET imaging studies of passive finger vibration have demonstrated a reduction in sensory evoked brain activations in the cortical (parietal and frontal) and subcortical (BG) areas of the brain (Boecker et al, 1999a). During limb position tasks, individuals with PD make more errors then healthy control participants when required to identify the occurrence and/or direction of passive movements (Schneider et al, 1987) as well as demonstrating greater errors in matching static limb position, detecting limb displacements, or using the lower limbs to estimate the size of an object (Martens & Almeida, 2011;O'Suilleabhain, Bullard, & Dewey, 2001;Zia et al, 2000).…”