What is the difference between huntingtons disease and parkinsons disease

Types of Huntington's Disease

Huntington's disease has two subtypes:

• Adult-onset Huntington's disease. This is the most common form of Huntington's disease. People with adult-onset Huntington's disease usually develop symptoms in their mid-40s and 50s.
• Juvenile Huntington's disease. Children and teenagers have this form of Huntington's disease, which is very rare. Children with Huntington's disease often have symptoms similar to Parkinson's disease. They may also develop problems with schoolwork.

OBJECTIVES

• 1) Discuss the demographics and etiology of idiopathic Parkinson’s (PD) and Huntington’s diseases (HD)

• 2) Compare and contrast the pathological features and pathogenesis of idiopathic PD, PD plus syndromes, and HD

• 3) Differentiate between the diagnosis of idiopathic PD and HD

• 4) Compare and contrast typical signs and symptoms of idiopathic PD and HD

• 5) Describe the clinical course, prognosis, and medical and surgical treatment of idiopathic PD and HD

• 6) Discuss evidence-based examination of the client with PD and HD

• 7) Discuss evidence-based management of the client with PD and HD

• 8) Compare and contrast examination and management of early, middle, and late stage PD and HD

Parkinson’s disease and Huntington’s disease are progressive neurodegenerative disorders of the basal ganglia and its connections that profoundly impact motor, cognitive, and psychiatric functions of affected individuals. Parkinson’s disease was named for James Parkinson, an English physician, whose work “An Essay on the Shaking Palsy” published in 1817 described six individuals with symptoms of the disease. Huntington’s disease was named for George Huntington, an American physician, who published an article entitled “On Chorea” in 1872 that described the disease.

EPIDEMIOLOGY

Parkinson’s disease (PD) is the second most common neurodegenerative disorder, after Alzheimer’s disease, with an estimated 1 million Americans and 7–10 million people worldwide affected by the disease. There are approximately 60,000 new cases annually of PD in the United States.1 The average age of onset is 60, and prevalence and incidence rates are very low in individuals under 40 years, increasing with age and peaking by age 80.2 The disease is approximately 1.5 times more common in men than women. The incidence of PD was reported to be highest among Hispanics, followed by non-Hispanic whites, Asians, and Blacks in one study conducted in a multi-ethnic population in California.3

ETIOLOGY AND RISK FACTORS FOR PARKINSON’S DISEASE

Parkinsonism refers to a group of disorders with a variety of different underlying pathologies that can cause Parkinson’s-like symptoms, including slowing movement (bradykinesia), tremor, rigidity or stiffness, and balance problems. PD, or idiopathic parkinsonism, is the most common disorder, affecting about 78% of individuals. Secondary parkinsonism results from identifiable causes such as toxins, trauma, multiple strokes, infections, metabolic disorders, and drugs. There are also conditions, called parkinson-plus syndromes that mimic PD in some ways but are caused by other neurodegenerative disorders.

IDIOPATHIC PARKINSON’S DISEASE

The exact cause of Parkinson’s disease remains unknown,4 but most scientists believe that it is caused by an interaction between genetic and environmental factors. Family history has been shown to be a strong risk factor for PD with a person’s risk of developing PD 2.9 times greater if a first-degree relative had PD.5 Twin studies have reported either no difference ...

Journal Article

H. Boecker,

Henning Boecker, MD, Neurologische Klinik, TU München, Klinikum rechts der Isar, Möhlstrasse 28, D–81675 München, Germany E-mail:

Search for other works by this author on:

Received:

19 February 1999

Published:

01 September 1999

• PDF
• Split View
• • Article contents
  • Figures & tables
  • Video
  • Audio
  • Supplementary Data

• Cite

  Cite

  H. Boecker, A. Ceballos-Baumann, P. Bartenstein, A. Weindl, H. R. Siebner, T. Fassbender, F. Munz, M. Schwaiger, B. Conrad, Sensory processing in Parkinson's and Huntington's disease: Investigations with 3D H215O-PET, Brain, Volume 122, Issue 9, September 1999, Pages 1651–1665, https://doi.org/10.1093/brain/122.9.1651

  Close

• • Email
  • Twitter
  • Facebook
  • More

Close

Navbar Search Filter Microsite Search Term Search

Abstract

AIMS, Abnormal Involuntary Movement Scale, BA, Brodmann area, FDG, [18F]fluorodeoxyglucose, HD-ADL, Huntington's Disease Activities of Daily Living, M1, primary motor cortex, MPTP, 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine, MWT-B, Multiple Choice Word Test—B, SMA, supplementary motor area, SSEP, somatosensory evoked potential, S1, primary sensory cortex, S2, secondary sensory cortex, UHDRS, Unified Huntington's Disease Rating Scale, UPDRS, Unified Parkinson's Disease Rating Scale

Introduction

Parkinson's disease and Huntington's disease are both disorders with established basal ganglia pathology. In addition to characteristic motor signs, both entities are associated with variable degrees of sensory dysfunction. This is thought to be due, at least to some extent, to processing deficits at basal ganglia level and hence disturbed interaction within subcorticocortical networks, as is supported by conjoining clinical, animal model and electrophysiological evidence.

In Parkinson's disease, besides descriptions of subjective sensory symptoms including numbness, coldness, burning or painful limb sensations (Koller, 1984), a number of somatosensory deficits have been described on objective clinical testing. These include inadequate kinaesthesis (Klockgether et al., 1995; Demirci et al., 1997; Jobst et al., 1997), tracking and targeting movements on the basis of sensory feedback (Schneider et al., 1986, 1987; Klockgether et al., 1995), two-point discrimination (Schneider et al., 1986, 1987), roughness discrimination (Sathian et al., 1997), tactile stimulus location (Schneider et al., 1986), proprioception (Schneider et al., 1986; 1987; Jobst et al., 1997) and higher order proprioceptive integration, i.e. abnormal reflex and/or voluntary motor responses to proprioceptive signals (Rickards and Cody, 1997). Moreover, despite some controversy in the literature (Nakashima et al., 1992; Huttunen and Teravainen, 1993; Drory et al., 1998) there have been documentations (Rossini et al., 1989, 1993; de Mari et al., 1995; Traversa et al., 1995) of decreased parietal N20 and frontal N30 components of somatosensory evoked potentials (SSEP) that reverse after apomorphine challenge (Rossini et al., 1993; de Mari et al., 1995; Traversa et al., 1995) and chronic l-dopa therapy (Traversa et al., 1995). Analogous findings have been reported (Onofrj et al., 1990) in primates rendered parkinsonian with the neurotoxin 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP).

In contrast, clinical descriptions of sensory phenomena in Huntington's disease are less consistent. There have been reports on painful somatosensory limb phenomena (Albin and Young, 1988) along with other signs of perceptual sensory impairment, for instance, visual discrimination deficits (Brouwers et al., 1984). On experimental testing, Huntington's disease patients show response delays when loadings are applied unexpectedly to objects held in precision grip, a finding that has been interpreted as an indication of `a reduction in somatosensory input to cortex caused by disruption of basal ganglia structures' (Fellows et al., 1997). Even more consistently than in Parkinson's disease, parietal and frontal SSEP amplitudes have been reported to be diminished or even absent in Huntington's disease patients (Abbruzzese et al., 1990; Yamada et al., 1991; Topper et al., 1993) and analogous observations have been made in the quinolinic acid animal Huntington's disease model (Schwarz et al., 1992). Interestingly, SSEP abnormalities in Huntington's disease are evident even in at-risk subjects and patients with early stages of disease and no clinical signs of chorea (Noth et al., 1984). These observations at early stages of disease, when cortical involvement is less pronounced, lend indirect support to the theory that cortical sensory processing is affected by basal ganglia dysfunction.

Based on these converging findings, the aim of this study was twofold: (i) to reinvestigate participation of the basal ganglia during a robust vibratory stimulation paradigm in healthy controls using 3D PET measurements, and (ii) to determine differences in sensory evoked central activation patterns in Parkinson's disease and Huntington's disease. As indicated by previous evoked potential recordings, we expected to identify impaired activation in frontal and parietal areas.

Subjects and methods

Subjects

Eight Parkinson's disease patients (mean age 59.8 ± 6.3 years, five male, three female), eight Huntington's disease patients (mean age 49.9 ± 9.1 years, six male, two female) and eight healthy volunteers (mean age 51.8 ± 9.0 years, five male, three female) were included in the study. Vibratory stimulation was applied to the dominant (right) side in each control subject. In order to enhance sensitivity for detecting differences between patients and controls, sensory stimulation in the patient groups was applied to the clinically most affected side. A priori, patients with major hyperkinetic motor signs were excluded from the study in order to ensure equal stimulus presentation in patients and controls. All selected patients had been investigated prior to PET while placed in a comfortable lying position to exclude exacerbation of clinical signs in this position. During PET, on-line video was used to monitor head and arm movements, and consequently one Huntington's disease patient had to be excluded from subsequent analyses due to large amplitude head movements towards the end of the PET session. One control subject withdrew because of claustrophobic sensations.

All Parkinson's disease patients had experienced unilateral disease onset and those patients under anti-parkinsonian medication (n = 7) were l-dopa-sensitive. One patient (no. 6) had early, mild Parkinson's disease, but characteristic right-dominant clinical signs had not been treated with l-dopa until the time of PET. Disability `off' medication (drug withdrawal of at least 12 h) was rated according to the Unified Parkinson's Disease Rating Scale, i.e. UPDRS motor scale (Fahn et al., 1987), the Hoehn and Yahr score (Fahn et al., 1987) and the Schwab and England scale (Fahn et al., 1987). Furthermore, bilateral latencies and amplitudes of the N20 component of median nerve SSEPs were recorded. In four of the eight Parkinson's disease patients, additional N30 SEP components were recorded and three of these showed relatively decreased amplitudes of the frontal N30 component when stimulated on their dominant side. None of the Parkinson's disease patients were taking anti-parkinsonian medication at the time of PET (drug-free interval of at least 12 h). The Parkinson's disease patients' clinical details and rating scores are summarized in Table 1.

All Huntington's disease patients had a positive family history and their diagnosis was confirmed genetically by determination of CAG trinucleotide repeat lengths ≥37 (Duyao et al., 1993). In six of the eight patients, bicaudate indices were determined either on CT or MRI scans (Harris et al., 1992). Patients were assessed clinically and their disability rated `off' medication (drug withdrawal of at least 12 h) according to an adapted version (Siesling et al., 1997) of the Unified Huntington's Disease Rating Scale (UHDRS), the Abnormal Involuntary Movement Scale (AIMS) (Lane et al., 1985), the Multiple Choice Word Test-B (MWT-B) as a screening measure of general intellectual capacities (Blaha and Pater, 1979), along with the Huntington's disease Activities of Daily Living (HD-ADL) classification (Bylsma et al., 1993). None of the participants were taking medication at the time of PET (drug-free interval of at least 12 h). All Huntington's disease patients' clinical details and rating scores, along with the electrophysiological measures (see above) are summarized in Table 2.

According to the unpaired non-parametric Mann–Whitney two sample test, age differences between patient groups and controls were not statistically significant (Parkinson's disease versus controls: two-tailed P value = 0.13, not significant; Huntington's disease versus controls: two-tailed P value = 0.96, not significant). Our control cohort had no history of neurologic or psychiatric disease and none were taking medication at the time of PET. Tenets of the Declaration of Helsinki were followed and written informed consent was given by all participants prior to PET. The studies were approved by the Ethics Committee of the Faculty of Medicine of the Technische Universität München. Permission to administer radioactivity was obtained from the local radiation safety institution.

Experimental design

Repeated measurements of regional cerebral blood flow (rCBF) (range between four and six per condition) were performed in each subject with H215O-PET during two experimental conditions acquired in a random order setting: (i) unilateral continuous high frequency vibratory stimulation (Vibrameter Type III, Somedic AB, Stockholm, Sweden; frequency: 150 Hz, load: 4 N) applied to the metacarpal joint of the immobilized right index finger, (ii) rest (no vibratory stimulus). Before PET, the identical vibratory stimulus was applied to all participants over a 1-min test period in order to familiarize each subject with the experimental set-up. The 10-min inter-scan interval was used to inform subjects whether vibratory stimulation would appear or not during the following scan. Subjects were neither asked to attend to nor to ignore the stimulus, in order to reduce attentional bias. According to an oral questionnaire after the scanning session, no painful sensations or sensory phenomena other then the applied stimulus were experienced by the participants during PET. All subjects were scanned in supine position with their ears unplugged, the acoustic input (background noise from the electronic equipment) being kept constant throughout rest and activation conditions. During PET acquisition periods the scanner room was dimmed and subjects were asked to keep their eyes closed. Head fixation was accomplished with polystyrene head moulds and an elastic ribbon (surrounding front and head mould) to provide external support. Moreover, head movements were monitored continuously by use of three laser beams adjusted to corresponding face markers and, if necessary, corrected manually.

Data acquisition

Measurements of the regional distribution of radioactivity were performed with a Siemens 951 R/31 PET camera (CTI, Knoxville, Tenn., USA) in 3D mode with a total axial field of view of 10.5 cm (no interplane dead space) covering the entire cerebral cortex at the expense of cerebellar and brainstem structures. Prior to collecting activation data, individual transmission scans were acquired with an external 68Ga/68Ge ring source (septa in place) to correct for the attenuation from skull and brain. After this initial step, repetitive semi-bolus intravenous injections of 7.5 mCi/run of H215O in 20 ml of normal saline solution were administered over 30 s. The acquisition protocol consisted of a single 50 s frame starting with the beginning of tracer arrival in the brain. The experimental condition started ~15 s prior to data acquisition, and was continued until the completion of the scan. This process was repeated for each scan, with between-scan intervals of 10 min to allow decay of radiation to background levels. Following corrections for randoms, dead time and scatter, images were reconstructed by filtered back projection (Hanning filter, cut-off frequency 0.4 cycles/projection element) to 31 consecutive axial planes with a 128 × 128 matrix (pixel sizes measuring 2.09 × 2.09) and inter-plane separation of 3.375 mm.

Data transformation

All calculations and image transformations were performed on Sun SPARC 2 work-stations (Sun Computers Europe Inc., Surrey, UK). For data analysis, we used statistical parametric mapping software (SPM 96b, Wellcome Department of Cognitive Neurology, London, UK) implemented in the PRO Matlab environment (Mathworks Inc., Natic, Mass., USA) (for review, see Friston, 1997).

In the first stage of analysis, the scans of each subject were co-aligned to the first of the series. In this automated realignment procedure, the six parameter rigid-body transformations were estimated using a least squares approach (Friston et al., 1995a). Thereby, an aligned set of images and a mean image (each of 31 planes) were generated for each individual subject. The mean image, characterized by the highest anatomical detail, was then transformed into standard stereotactic space (Talairach and Tournoux, 1988). This procedure of spatial normalization involves linear and non-linear 3D transformations on a slice-by-slice basis (Friston et al., 1995a). The same transformations were then applied to each of the subject's realigned images to ensure identical orientation in standard space. As a final pre-processing step, the normalized data were smoothed using an isotropic Gaussian kernel of 12 mm (full width at half maximum) to increase signal to noise ratio and to reduce variance due to individual differences in gyral anatomy (Friston et al., 1995a). The resulting normalized and smoothed images contained 26 planes with pixel sizes of 2 × 2 mm and inter-plane distances of 4 mm. In patients with left-sided stimulation, data were flipped prior to group statistical analyses.

Statistical analysis

To remove the effect of variations in global flow across subjects and scans, an analysis of covariance (ANCOVA) was applied with global flow as the confounding variable. (Friston et al., 1990, 1995b). Subsequently, mean rCBF was scaled to an arbitrary level of 50 ml/100 ml/min and these adjusted rCBF voxel values were used for further statistical analyses. To test our hypothesis about condition specific regional effects, appropriately weighted formal categorical comparisons between resting and activation conditions were performed in each of the three individual groups (i.e. within group subtraction analyses). Each resulting set of voxel values constitutes an SPM{t} map which was then transformed into normally distributed Z statistics (Friston et al., 1995b; Friston, 1997) The significance of each SPM{Z} contrast was estimated by comparison of the observed and expected t statistic under the null hypothesis (Friston, 1997).

Since the pattern of rCBF changes induced by the experimental condition (i.e. unilateral high-frequency vibration) has been established in healthy control subjects with previous functional neuroimaging (for review, see Paulesu et al., 1997), an anatomically constrained hypothesis was used and only activation foci within this network [i.e. including primary sensory cortex (S1), adjoining parietal cortical areas, secondary sensory cortex (S2), insular cortex, supplementary motor area (SMA), thalamus and basal ganglia; this latter area was predicted on the basis of electrophysiological recordings, as referred to in the discussion] that were significant at a height threshold of P < 0.001 (uncorrected) or better were reported in the individual groups. This hypothesis-based approach was also applied to both patient groups, based on previous vibratory activation studies in other movement disorder conditions (Tempel and Perlmutter, 1990, 1993; Catalan et al., 1998) that revealed either local magnitude changes of vibratory-induced rCBF increases or local activation shifts within components of pre-established cortical sensory areas. Similar hypothesis-driven approaches have been applied in several other PET imaging studies for their potential of reducing false-negative findings; this is of particular relevance when less activating, i.e. passive stimulation, designs are employed, as in this study. A statistical threshold of P < 0.001 (uncorrected) was applied for activation decreases, based on previously reported activation decreases in superior parietal cortex bilaterally, in paralimbic association areas, left globus pallidus (Seitz et al., 1992) and in ipsilateral S1 (for review, see Paulesu et al., 1997).

To assess specific differences in vibration-induced activation changes between the patient groups and the control cohort, between-group subtraction analyses were performed and thresholded at P < 0.01 (uncorrected).

Results

Control group (within-group subtraction analyses)

In the control cohort, the pattern of activation was strongly lateralized to the side opposite to vibratory stimulus presentation. Significant cortical activation foci included contralateral S1 and S2. Other cortical areas within the hypothesized sensory network were below the set level of significance, for instance, caudal SMA (P = 0.008, trend only). No unpredicted activation foci outside the hypothesized network were observed. Subcortical peak activation was seen in contralateral globus pallidus, the cluster extending into adjacent left ventrolateral thalamus. Detection and separation of individual peaks, however, within this subcortical cluster was not possible. No significant rCBF decreases induced by vibration were observed in the control group, only a trend towards decreased rCBF in ipsilateral S1 (P < 0.002, trend only). All results, including Z scores, P values, pixels values per cluster and x, y, z coordinates of respective rCBF changes are summarized in Table 3. For visualization purposes, cortical activation changes are superimposed on to three orthogonal standard MRI sections (Fig. 1) and projected on a single volume rendered MRI (Fig. 2, upper section); subcortical (basal ganglia, thalamus) rCBF increases are superimposed on to three consecutive normalized MRI slices (Fig. 2, lower section); Fig. 3A demonstrates the entire SPM set by comparison with the patient group data (Fig. 3B and C) as maximum intensity projections.

Patient groups (within-group subtraction analyses)

While significant rCBF increases were observed within cortical and subcortical components of the hypothesized sensory network, contralateral S1 did not reach the significance level of P < 0.001 in either of the two patient groups (Tables 4 and 5). Moreover, the pattern of vibration-induced rCBF increases in both groups was characterized by a tendency of enhanced recruitment of ipsilateral (right) insular cortex in Huntington's disease (P < 0.001, Z = 3.33) and in Parkinson's disease (P < 0.002, Z = 2.92, trend only). Activation of basal ganglia structures was observed neither in Parkinson's disease nor in Huntington's disease. All results are summarized in Table 4 (Parkinson's disease) and Table 5 (Huntington's disease), and as corresponding SPM maps (maximum intensity projections of the entire within-group SPM set) displayed in Fig. 3B (Huntington's disease) and Fig. 3C (Parkinson's disease).

Patient groups versus controls (between-group subtraction analyses)

There were significant relative differences in vibration-evoked rCBF between patients and controls that can be summarized as follows: (i) in Huntington's disease, relatively decreased activation of contralateral S2 (P < 0.001), S1 (P ≤ 0.012, trend only), parietal areas 39 and 40 (P < 0.001), and lingual gyrus (P < 0.001), bilateral prefrontal cortical areas 8, 9, 10 and 44 (P ≤ 0.002), along with decreased activation of contralateral basal ganglia (putamen and globus pallidus, P ≤ 0.003); (ii) in Parkinson's disease, relatively decreased activation of contralateral sensorimotor cortex (S1/M1) (P < 0.001), lateral premotor cortex (P ≤ 0.003), S2 (P ≤ 0.005), contralateral posterior cingulate (P ≤ 0.001), bilateral prefrontal cortex [Brodman area (BA) 10; P ≤ 0.007] and contralateral basal ganglia (globus pallidus: P ≤ 0.008; putamen: P ≤ 0.019, trend only); (iii) in both entities, relatively enhanced activation of ipsilateral sensory cortical areas, notably caudal S1 (P ≤ 0.001), S2 (P ≤ 0.002) and insular cortex (P ≤ 0.002). The data are summarized in Table 6 (relative activation differences between Parkinson's disease patients and controls) and Table 7 (relative activation differences between Huntington's disease patients and controls).

Discussion

Activation pattern in control subjects

The pattern of brain activation induced by unilateral high-frequency passive vibratory stimulation in our control cohort is in keeping with previous PET data on elementary somatosensory function, as reviewed recently by Paulesu and colleagues (Paulesu et al., 1997). Our study confirms that this rather crude sensory stimulus produces strong activation in cortical areas S1 and S2. The pattern of normalized group rCBF increases in our study was markedly lateralized to the contralateral hemisphere, similar to previous reports (Seitz and Roland, 1992). Transcallosal connections have, nevertheless, been demonstrated in posterior S1 (BA 2) (Iwamura et al., 1994), adjoining parietal cortex and secondary sensory cortical areas (S2, insular cortex) and, likewise, previous PET (Burton et al., 1993) and functional MRI (Boecker et al., 1995) experiments have provided evidence for bilateral sensory cortical processing in humans. However, it remains an issue of further inquiry with higher temporal resolution imaging modalities, how ipsilateral sensory area recruitment is affected by habituation and/or other task-related issues. For instance, evoked potential recordings in cats indicate that habituation occurs more rapidly in S2 compared with S1 areas (Chernigovskii et al., 1979).

Medial premotor cortex activation, in this study, was only detectable as a trend in caudal SMA territory. While this is in line with monkey recording data showing that SMA neurons respond nearly exclusively to sensory cues that are relevant for motor control (Romo et al., 1993), more significant SMA activation has been observed previously on passive high frequency vibratory tasks (Seitz and Roland, 1992). Seitz and Roland attributed the co-activation of primary motor cortex (M1) and SMA to reflectory grasping of the stimulated hand (Seitz and Roland, 1992). No spillover of activation to M1 cortex was observed in our study and, therefore, task-related issues, for instance, the immobilization imposed on the stimulated hand, are to be considered when interpreting differences between these studies.

A new aspect of the `physiological' activation pattern seen in healthy control subjects was the participation of contralateral globus pallidus. That the basal ganglia, beyond well established motor-related functions, are actively involved in sensory processing is evident from neuronal recordings (from striatum and globus pallidus) in different non-human species, including rats (Schneider et al., 1982a), cats (Sedgwick and Williams, 1967; Schneider and Lidsky, 1981; Schneider et al., 1982b; Lidsky et al., 1985; Rothblat and Schneider, 1993) and monkeys (Romo et al., 1995) (for review, see Rothblat and Schneider, 1995). It has been concluded from these studies that the basal ganglia function as a `sensory analyser' (Lidsky et al., 1985; Schneider and Lidsky, 1987) which modulates motor behaviour by integrating and focusing adequate sensory impulses. Such gating and focusing properties seem to be of particular relevance for providing contextual sensory triggers for on-line guidance of movement. Sensory input to the basal ganglia takes the route via established direct projections from S1 to putamen (Flaherty and Graybiel, 1991). In turn, while the basal ganglia are thought to direct their entire output to frontal cortex (premotor and prefrontal) but not parietal cortical areas (Alexander et al., 1986), interaction with lemniscal pathways—and thereby indirectly with parietal cortex—is thought to occur at the level of the intralaminar thalamic nuclei, as discussed previously (Schwarz et al., 1992). Despite the obvious relevance of these sensory triggers for on-line motor control, basal ganglia neuronal responses have been demonstrated during passive sensory stimulation, i.e. in tasks devoid of any active motor component, supporting our findings (Schneider et al., 1982a; Rothblat and Schneider, 1993, 1995).

Previous PET studies in humans have demonstrated enhanced basal ganglia activation during somatosensory shape discrimination (Seitz and Roland, 1992), when compared with pure motor performance of similar finger sequences (counterbalance of motor component) or to high frequency vibratory stimulation (counterbalance of sensory component). Moreover, basal ganglia activation has been reported during roughness and length discrimination tasks (O'Sullivan et al., 1994) and during tasks examining tactile learning and recognition of complicated geometrical objects (Roland and Mortensen, 1987). In contrast to our findings, Seitz and Roland reported rCBF decreases in contralateral globus pallidus during a similar vibratory task (Seitz and Roland, 1992). In the context of `passive' stimulation paradigms, basal ganglia activation has been observed during 47–48°C painful heat stimulation (Coghill et al., 1994) but, so far, it was not evident in response to passive tactile stimulation of the fingertips (Burton et al., 1997), unilateral median nerve stimulation (Ibanez et al., 1995) or innocuous 110 Hz (Coghill et al., 1994) and 130 Hz (Burton et al., 1993) vibrotactile stimulation. In conclusion, our study extends previous neuroimaging work by demonstrating contralateral pallidal activation in response to a passive vibratory task. This finding may be attributed to enhanced detection sensitivity of current 3D PET scanning and provides further support to the eminent role of the basal ganglia as a sensory analyser.

Activation pattern in Parkinson's disease and Huntington's disease patients

The major finding emerging from our investigations in Parkinson's disease and Huntington's disease patients is that task-related differences in cortical and subcortical sensory-evoked activation exist by comparison with healthy control subjects and, like previous H215O-PET studies on motor processing, there was a considerable degree of congruency between activation patterns in Parkinson's disease (Jenkins et al., 1992; Samuel et al., 1997) and Huntington's disease (Bartenstein et al., 1997; Weeks et al., 1997). Among distributed areas with relative rCBF reductions, basal ganglia activation was reduced (globus pallidus > putamen) in both patient groups. This is in keeping with findings in cats rendered parkinsonian with MPTP, where marked decreases (from 31% to 12%) of neuronal responses to tactile stimuli have been demonstrated in globus pallidus (Rothblat and Schneider, 1995). Similar reductions of striatal responsiveness to sensory stimulation have been reported in MPTP treated monkeys, and were reversible after apomorphine (Aosaki et al., 1994).

In the context of the extrapyramidal pathology underlying Parkinson's disease and Huntington's disease, it is tempting to relate abnormal cortical activation, as evident in both patient groups, in the first place to processing deficits at basal ganglia level. It has to be considered, however, that the degenerative process in both conditions involves multiple systems, including cortex. Likewise, previous resting PET studies with the tracer [18F]fluorodeoxyglucose (FDG) have demonstrated frontoparietal cortical hypometabolism in Huntington's disease (Kuwert et al., 1990) and also in Parkinson's disease (Eberling et al., 1994; Eidelberg et al., 1994), which implies that cortical pathology may have contributed to our findings as well. Nevertheless, as has been discussed in the context of Huntington's disease previously, several independent arguments support the specific relevance of basal ganglia dysfunction for alterations of cortical sensory processing: (i) the characteristic frontal and parietal SSEP changes that have been observed in Huntington's disease patients with manifest disease were also evident in at-risk subjects (Noth et al., 1984; Yamada et al., 1991), at a stage where cortical involvement is less prominent; (ii) pertinent SSEP findings correlate significantly with reductions of caudate and lentiform glucose metabolism measured with FDG PET (Kuwert et al., 1993); (iii) data from the experimental Huntington's disease model in rats with excitotoxic striatal damage demonstrate that basal ganglia dysfunction alone is sufficient to induce equivalent alterations of evoked potentials (Schwarz et al., 1992). In this respect, it is of considerable interest that reductions of parietal and frontal SSEP components have also been observed in Parkinson's disease patients (Rossini et al., 1989, 1993; de Mari et al., 1995; Traversa et al., 1995) and in primates rendered parkinsonian with MPTP (Onofrj et al., 1990).

Parkinson's disease and Huntington's disease patients both showed significant, mainly contralateral, decreases of vibratory-evoked activation in parietal and frontal cortical areas. At parietal sites, decreased activation included contralateral S1 and S2, and in the Huntington's disease patient group there were additional relative activation decreases in contralateral parietal areas 39 and 40. Processing of complex multidimensional sensory stimuli, as studied here, is neither spatially nor functionally restricted to S1, but rather involves adjoining parietal cortex, where further somatosensory processing and integration occurs (for review, see Paulesu et al., 1997). Therefore, when considering the spatial extension of rCBF decreases, parietal cortex, involving multiple areas, appeared to be more extensively affected in the Huntington's disease group.

According to our a priori hypothesis, impaired premotor cortex activation was predicted in both patient groups, considering frontal amplitude decreases observed on evoked potential recordings in Huntington's disease (Abbruzzese et al., 1990; Yamada et al., 1991; Topper et al., 1993) and Parkinson's disease (Rossini et al., 1989; de Mari et al., 1995). In fact, it has been argued that the frontal P20–N30–P40 complex is generated, `at least in part, with a cortico-subcortico-cortical re-entry loop involving the supplementary motor area, the basal ganglia, the primary motor cortex, and the ventrolateral thalamic nuclei' (Rossini et al., 1993). Abnormal frontostriatal function `could impact on the decision process that operates on incoming sensory input to deliver an externally recognisable response' (Sathian et al., 1997). However, in our study no relative reductions of sensory-evoked rCBF were detectable in SMA territory. While lateral premotor cortex showed relative hypoactivity in the Parkinson's disease patient group, this was not the case in the Huntington's disease group. Clearly, future imaging studies with more elaborate paradigms are required to determine the precise role of premotor cortex for sensorimotor integration processes and the influence of subcortical pathology on pertinent functions. Significant frontal activation decreases were observed at prefrontal sites. While current evidence suggests that the basal ganglia direct their output via at least five segregated loops to different portions of the frontal lobe (Alexander and Crutcher, 1990), we cannot rule out the possibility that prefrontal activation changes have occurred as a consequence of frontal cortical dysfunction (Kuwert et al., 1990; Eberling et al., 1994; Eidelberg et al., 1994) and/or cognitive aspects of task processing.

Another remarkable observation on between-group analyses is that of relative enhanced activation of ipsilateral cortical sensory areas, notably of caudal S1, S2 and insular cortex in both patient groups. These ipsilateral activation increases result from differing hemispheric activation patterns between patients and controls. In fact, within group analyses revealed a more bilaterally distributed pattern of rCBF increases in both patient groups, compared with a very lateralized activation pattern in the control group. Moreover, there was a tendency towards ipsilateral S1 rCBF decreases in the control cohort—a phenomenon observed by other investigators as well (for review, see Paulesu et al., 1997)—which together are thought to account for our ipsilateral findings. We can only carefully speculate about the meaning of these observations, but, considering focusing and gating functions of basal ganglia (outlined before), they may be interpreted as an indication of either altered central focusing and/or enhanced compensatory recruitment of associative sensory areas, in the presence of basal ganglia dysfunction. Similar rCBF findings indicating enhanced associative area recruitment in the presence of basal ganglia disorders have been reported recently on motor tasks (Bartenstein et al., 1997; Samuel et al., 1997; Weeks et al., 1997); of particular interest, relative insular overactivity of nearly identical distribution has been shown in Huntington's disease patients performing a free-selection joystick task (Weeks et al., 1997). While relative insular overactivity has also been demonstrated on motor tasks in patients with motor neuron disease (Kew et al., 1993) following striatocapsular stroke (Weiller et al., 1992), idiopathic dystonia (Ceballos-Baumann et al., 1995b) and acquired hemidystonia (Ceballos-Baumann et al., 1995a), it is an interesting finding that similar relative activation increases occur on pure sensory processing tasks, as shown in our study. It is tempting to interpret relative insular overactivity as a form of polymodal functional adaptation occurring also in the presence of structural or functional lesions at the level of the basal ganglia, but future studies on sensory processing in other basal ganglia disorders will have to examine this issue more closely.

Methodological considerations

We can only speculate on enhanced activation at basal ganglia level in tasks demanding appropriate integration or gating of sensory impulses to ongoing motor plans, which was not studied here, but appears to be an important element of basal ganglia function (Lidsky et al., 1985; Schneider and Lidsky, 1987). Studies on sensorimotor function have, in fact, more in common with physiological behaviour where on-line integration of sensory and motor modalities is required. The advantage, however, of a passive sensory stimulation approach, as applied here, is the absence of any confounding motor component; this conduct provides a reasonable basis for between-group comparisons with patients, in particular when these are characterized by abnormal movement. This may be, however, at the expense of detection sensitivity, considering the proposed role of the basal ganglia as a sensorimotor integrator.

Conclusions

This is the first functional neuroimaging study that specifically addresses the issue of sensory processing in Parkinson's disease and Huntington's disease, by comparison with healthy controls. Our data show that sensory-evoked brain activation in both movement disorders is reduced in cortical (parietal and frontal) and subcortical (basal ganglia) areas. Our study, therefore, indicates that Parkinson's disease and Huntington's disease, beyond known deficits in central motor control, are characterized by abnormal sensory processing even on tasks devoid of any motor component.

Table 1.

Clinical data in the Parkinson's disease group

Table 1.

Clinical data in the Parkinson's disease group

Table 2.

Clinical data in the Huntington's disease group

Table 2.

Clinical data in the Huntington's disease group

Table 3

Areas with activation increases induced by right-sided vibratory stimulation compared with rest in the control group

Table 3

Areas with activation increases induced by right-sided vibratory stimulation compared with rest in the control group

Table 4

Areas with activation increases induced by right-sided vibratory stimulation compared with rest in the Parkinson's disease patient group

Table 4

Areas with activation increases induced by right-sided vibratory stimulation compared with rest in the Parkinson's disease patient group

Table 5

Areas with activation increases induced by right-sided vibratory stimulation compared with rest in the Huntington's disease patient group

Table 5

Areas with activation increases induced by right-sided vibratory stimulation compared with rest in the Huntington's disease patient group

Table 6

Areas with relative differences in vibratory-induced activation between Parkinson's disease patients and controls

Table 6

Areas with relative differences in vibratory-induced activation between Parkinson's disease patients and controls

Table 7

Areas with relative differences in vibratory-induced activation between Huntington's disease patients and controls

Table 7

Areas with relative differences in vibratory-induced activation between Huntington's disease patients and controls

Fig. 1

Superposition of rCBF increases in the control cohort (n = 8) on to three orthogonal stereotactically normalized standard MRI sections (Talairach coordinate of the cross hair: x = 50 mm, y = –20 mm, z = 52mm); according to our convention, the left side of the figure corresponds to the right hemisphere. Note vibration-induced co-activation of contralateral left S1 and S2 (P < 0.001, uncorrected).

Fig. 2

Upper section. Surface rendering of cortical activation foci in the normal control cohort (n = 8) superimposed on to a stereotactically normalized standard MRI image. According to our convention, the left side of the figure corresponds to the right hemisphere. Note that vibration-induced activation foci are strongly lateralized to the side opposite to stimulus presentation with a peak activation focus in contralateral S1 (P < 0.001, uncorrected). Lower section. Consecutive axial sections (−2, 0, +2 mm relative to the bicommissural line) of subcortical activation foci in the control cohort (n = 8) superimposed on to stereotactically normalized standard MRI images; according to our convention, the left side of the figure corresponds to the right hemisphere. Note that peak activation occurs in contralateral globus pallidus extending into adjacent ventrolateral thalamus (for illustrative purposes only, the threshold was reduced to P < 0.01, uncorrected).

Fig. 3

SPM (within-group subtraction analyses) demonstrating the entire data sets as maximum intensity projections (P < 0.001, uncorrected) from sagittal, coronal and horizontal views; according to our convention, the left side of the figure corresponds to the right hemisphere: (A) controls; (B) Huntington's disease patients; (C) Parkinson's disease patients. Note that the pattern of rCBF increases in the control group involves cortical (contralateral S1 and S2) and subcortical (contralateral globus pallidus/ventrolateral thalamus) areas, reflecting our a priori hypotheses that in both patient groups the activation of contralateral S1 was not significant at P < 0.001, uncorrected.

We wish to thank our radiochemistry group and cyclotron staff for the radiotracer supply, S. Dieckmann for methodological assistance and S. Fürst, C. Kolligs and C. Kruschke for their technical assistance at the PET camera. This study was supported by the Deutsche Forschungsgemeinschaft (SFB 462, Sensomotorik).

References

Abbruzzese G, Dall'Agata D, Morena M, Reni L, Favale E. Abnormalities of parietal and prerolandic somatosensory evoked potentials in Huntington's disease.

Electroencephalogr Clin Neurophysiol

1990

;

77

:

340

–6.

Albin RL, Young AB. Somatosensory phenomena in Huntington's disease.

Mov Disord

1988

;

3

:

343

–6.

Alexander GE, Crutcher MD. Functional architecture of basal ganglia circuits: neural substrates of parallel processing [see comments]. [Review].

Trends Neurosci

1990

;

13

:

266

–71. Comment in: Trends Neurosci 1991; 14: 55–9.

Alexander GE, DeLong MR, Strick PL. Parallel organization of functionally segregated circuits linking basal ganglia and cortex. [Review].

Annu Rev Neurosci

1986

;

9

:

357

–81.

Aosaki T, Graybiel AM, Kimura M. Effect of the nigrostriatal dopamine system on acquired neural responses in the striatum of behaving monkeys.

Science

1994

;

265

:

412

–5.

Bartenstein P, Weindl A, Spiegel S, Boecker H, Wenzel R, Ceballos-Baumann AO, et al. Central motor processing in Huntington's disease. A PET study.

Brain

1997

;

120

:

1553

–67.

Blaha L, Pater W. Stability and reliability of a brief-intelligence test (MWT-b) to long-stay psychiatric patients (author's transl). [German].

Nervenarzt

1979

;

50

:

196

–8.

Boecker H, Khorram-Sefat D, Kleinschmidt A, Merboldt KD, Hänicke W, Requardt M, et al. High-resolution functional magnetic resonance imaging of cortical activation during tactile exploration.

Hum Brain Mapp

1995

;

3

:

236

–44.

Brouwers P, Cox C, Martin A, Chase T, Fedio P. Differential perceptual-spatial impairment in Huntington's and Alzheimer's dementias.

Arch Neurol

1984

;

41

:

1073

–6.

Burton H, Videen TO, Raichle ME. Tactile-vibration-activated foci in insular and parietal-opercular cortex studied with positron emission tomography: mapping the second somatosensory area in humans.

Somatosens Mot Res

1993

;

10

:

297

–308.

Burton H, MacLeod AM, Videen TO, Raichle ME. Multiple foci in parietal and frontal cortex activated by rubbing embossed grating patterns across fingerpads: a positron emission tomography study in humans.

Cereb Cortex

1997

;

7

:

3

–17.

Bylsma FW, Rothlind J, Hall MR, Folstein SE, Brandt J. Assessment of adaptive functioning in Huntington's disease.

Mov Disord

1993

;

8

:

183

–90.

Catalan MJ, Ishii K, Bara-Jiminez W, Honda M, Karp B, Hallett M. Plastic reorganization of the human somatosensory cortex (S1) in hand dystonia. A PET study [abstract].

Mov Disord

1988

;

13 (Suppl 2)

:

32

.

Ceballos-Baumann AO, Passingham RE, Marsden CD, Brooks DJ. Motor reorganization in acquired hemidystonia.

Ann Neurol

1995

;

37

:

746

–57.

Ceballos-Baumann AO, Passingham RE, Warner T, Playford ED, Marsden CD, Brooks DJ. Overactive prefrontal and underactive motor cortical areas in idiopathic dystonia.

Ann Neurol

1995

;

37

:

363

–72.

Chernigovskii VN, Musyashchikova SS, Mokrushin AA. Dynamics of habituation in different cortical regions of the cat brain.

Biol Bull Acad Sci USSR

1979

;

6

:

1

–7.

Coghill RC, Talbot JD, Evans AC, Meyer E, Gjedde A, Bushnell MC, et al. Distributed processing of pain and vibration by the human brain.

J Neurosci

1994

;

14

:

4095

–108.

de Mari M, Margari L, Lamberti P, Iliceto G, Ferrari E. Changes in the amplitude of the N30 frontal component of SEPs during apomorphine test in parkinsonian patients.

J Neural Transm Suppl

1995

;

45

:

171

–6.

Demirci M, Grill S, McShane L, Hallett M. A mismatch between kinesthetic and visual perception in Parkinson's disease.

Ann Neurol

1997

;

41

:

781

–8.

Drory VE, Inzelberg R, Groozman GB, Korczyn AD. N30 somatosensory evoked potentials in patients with unilateral Parkinson's disease.

Acta Neurol Scand

1998

;

97

:

73

–6.

Duyao M, Ambrose C, Myers R, Novelletto A, Persichetti F, Frontali M, et al. Trinucleotide repeat length instability and age of onset in Huntington's disease [see comments].

Nat Genet

1993

;

4

:

387

–92. Comment in: Nat Genet 1993; 4: 329–30.

Eberling JL, Richardson BC, Reed BR, Wolfe N, Jagust WJ. Cortical glucose metabolism in Parkinson's disease without dementia.

Neurobiol Aging

1994

;

15

:

329

–35.

Eidelberg D, Moeller JR, Dhawan V, Spetsieris P, Takikawa S, Ishikawa T, et al. The metabolic topography of parkinsonism.

J Cereb Blood Flow Metab

1994

;

14

:

783

–801.

Fahn S, Elton RL, Committee and Members of the UPDRS Development Committee. Unified Parkinson's disease rating scale. In: Fahn S, Marsden CD, Goldstein M, Calne DB, editors. Recent developments in Parkinson's Disease. Florham Park, NJ: Macmillan; 1987. p. 153–63; 293–304.

Fellows S, Schwarz M, Schaffrath C, Domges F, Noth J. Disturbances of precision grip in Huntington's disease.

Neurosci Lett

1997

;

226

:

103

–6.

Flaherty AW, Graybiel AM. Corticostriatal transformations in the primate somatosensory system. Projections from physiologically mapped body-part representations.

J Neurophysiol

1991

;

66

:

1249

–63.

Friston KJ. Analysing brain images: principles and overview. In: Frackowiak RSJ, Friston KJ, Frith CD, Dolan RJ, Mazziotta JC, editors. Human brain function. San Diego (CA): Academic Press; 1997. p. 25–41.

Friston KJ, Frith CD, Liddle PF, Dolan RJ, Lammertsma AA, Frackowiak RSJ. The relationship between global and local changes in PET scans [see comments].

J Cereb Blood Flow Metab

1990

;

10

:

458

–66. Comment in: J Cereb Blood Flow Metab 1993; 13: 1038–40.

Friston KJ, Ashburner J, Frith CD, Poline J-B, Heather JD, Frackowiak RSJ. Spatial registration and normalization of images.

Hum Brain Mapp

1995

;

3

:

165

–89.

Friston KJ, Holmes AP, Worsley KJ, Poline J-B, Frith CD, Frackowiak RSJ. Statistical parametric maps in functional imaging: a general linear approach.

Hum Brain Mapp

1995

;

2

:

189

–210.

Harris GJ, Pearlson GD, Peyser CE, Aylward EH, Roberts J, Barta PE, et al. Putamen volume reduction on magnetic resonance imaging exceeds caudate changes in mild Huntington's disease.

Ann Neurol

1992

;

31

:

69

–75.

Huttunen J, Teravainen H. Pre- and postcentral cortical somatosensory evoked potentials in hemiparkinsonism.

Mov Disord

1993

;

8

:

430

–6.

Ibanez V, Deiber MP, Sadato N, Toro C, Grissom J, Woods RP, et al. Effects of stimulus rate on regional cerebral blood flow after median nerve stimulation.

Brain

1995

;

118

:

1339

–51.

Iwamura Y, Iriki A, Tanaka M. Bilateral hand representation in the postcentral somatosensory cortex.

Nature

1994

;

369

:

554

–6.

Jenkins IH, Fernandez W, Playford ED, Lees AJ, Frackowiak RS, Passingham RE, et al. Impaired activation of the supplementary motor area in Parkinson's disease is reversed when akinesia is treated with apomorphine.

Ann Neurol

1992

;

32

:

749

–57.

Jobst EE, Melnick ME, Byl NN, Dowling GA, Aminoff MJ. Sensory perception in Parkinson disease.

Arch Neurol

1997

;

54

:

450

–4.

Kew JJ, Leigh PN, Playford ED, Passingham RE, Goldstein LH, Frackowiak RS, et al. Cortical function in amyotrophic lateral sclerosis. A positron emission tomography study.

Brain

1993

;

116

:

655

–80.

Klockgether T, Borutta M, Rapp H, Spieker S, Dichgans J. A defect of kinesthesia in Parkinson's disease.

Mov Disord

1995

;

10

:

460

–5.

Koller WC. Sensory symptoms in Parkinson's disease.

Neurology

1984

;

34

:

957

–9.

Kuwert T, Lange HW, Langen KJ, Herzog H, Aulich A, Feinendegen LE. Cortical and subcortical glucose consumption measured by PET in patients with Huntington's disease.

Brain

1990

;

113

:

1405

–23.

Kuwert T, Noth J, Scholz D, Schwarz M, Lange HW, Topper R, et al. Comparison of somatosensory evoked potentials with striatal glucose consumption measured by positron emission tomography in the early diagnosis of Huntington's disease.

Mov Disord

1993

;

8

:

98

–106.

Lane RD, Glazer WM, Hansen TE, Berman WH, Kramer SI. Assessment of tardive dyskinesia using the Abnormal Involuntary Movement Scale.

J Nerv Ment Dis

1985

;

173

:

353

–7.

Lidsky TI, Manetto C, Schneider JS. A consideration of sensory factors involved in motor functions of the basal ganglia. [Review].

Brain Res

1985

;

356

:

133

–46.

Nakashima K, Nitta T, Takahashi K. Recovery functions of somatosensory evoked potentials in parkinsonian patients.

J Neurol Sci

1992

;

108

:

24

–31.

Noth J, Engel L, Friedemann HH, Lange HW. Evoked potentials in patients with Huntington's disease and their offspring. I. Somatosensory evoked potentials.

Electroencephalogr Clin Neurophysiol

1984

;

59

:

134

–41.

Oldfield RC. The assessment and analysis of handedness: the Edinburgh inventory.

Neuropsychologia

1971

;

9

:

97

–113.

Onofrj M, Ghilardi MF, Basciani M, Martinez-Tica J, Glover A. Attenuation of the early anterior negativity of median nerve somatosensory evoked potential in the MPTP-treated monkey.

Neurophysiol Clin

1990

;

20

:

283

–93.

O'Sullivan BT, Roland PE, Kawashima R. A PET study of somatosensory discrimination in man. Microgeometry versus macrogeometry.

Eur J Neurosci

1994

;

6

:

137

–48.

Paulesu E, Frackowiak RSJ, Bottini G. Maps of somatosensory systems. In: Frackowiak RSJ, Friston KJ, Frith CD, Dolan RJ, Mazziotta JC, editors. Human brain function. San Diego (CA): Academic Press; 1997. p. 183–242.

Rickards C, Cody FW. Proprioceptive control of wrist movements in Parkinson's disease. Reduced muscle vibration-induced errors.

Brain

1997

;

120

:

977

–90.

Roland PE, Mortensen E. Somatosensory detection of microgeometry, macrogeometry and kinesthesia in man [published erratum appears in Brain Res 1987; 434: 241. [Review].

Brain Res

1987

;

434

:

1

–42.

Romo R, Ruiz S, Crespo P, Zainos A, Merchant H. Representation of tactile signals in primate supplementary motor area.

J Neurophysiol

1993

;

70

:

2690

–4.

Romo R, Merchant H, Ruiz S, Crespo P, Zainos A. Neuronal activity of primate putamen during categorical perception of somaesthetic stimuli.

Neuroreport

1995

;

6

:

1013

–7.

Rossini PM, Babiloni F, Bernardi G, Cecchi L, Johnson PB, Malentacca A, et al. Abnormalities of short-latency somatosensory evoked potentials in parkinsonian patients.

Electroencephalogr Clin Neurophysiol

1989

;

74

:

277

–89.

Rossini PM, Traversa R, Boccasena P, Martino G, Passarelli F, Pacifici L, et al. Parkinson's disease and somatosensory evoked potentials: apomorphine-induced transient potentiation of frontal components.

Neurology

1993

;

43

:

2495

–500.

Rothblat DS, Schneider JS. Response of caudate neurons to stimulation of intrinsic and peripheral afferents in normal, symptomatic, and recovered MPTP-treated cats.

J Neurosci

1993

;

13

:

4372

–8.

Rothblat DS, Schneider JS. Alterations in pallidal neuronal responses to peripheral sensory and striatal stimulation in symptomatic and recovered parkinsonian cats.

Brain Res

1995

;

705

:

1

–14.

Samuel M, Ceballos-Baumann AO, Blin J, Uema T, Boecker H, Passingham RE, et al. Evidence for lateral premotor and parietal overactivity in Parkinson's disease during sequential and bimanual movements. A PET study. [see comments].

Brain

1997

;

120

:

963

–76. Comment in: Brain 1998; 121: 769–72.

Sathian K, Zangaladze A, Green J, Vitek JL, DeLong MR. Tactile spatial acuity and roughness discrimination: impairments due to aging and Parkinson's disease.

Neurology

1997

;

49

:

168

–77.

Schneider JS, Lidsky TI. Processing of somatosensory information in striatum of behaving cats.

J Neurophysiol

1981

;

45

:

841

–51.

Schneider J, Lidsky T. Basal ganglia and behavior: sensory aspects of motor functioning. Toronto: Hans Huber Publishers; 1987.

Schneider JS, Denaro FJ, Lidsky TI. Basal ganglia: motor influences mediated by sensory interactions.

Exp Neurol

1982

;

77

:

534

–43.

Schneider JS, Morse JR, Lidsky TI. Somatosensory properties of globus pallidus neurons in awake cats.

Exp Brain Res

1982

;

46

:

311

–4.

Schneider JS, Diamond SG, Markham CH. Deficits in orofacial sensorimotor function in Parkinson's disease.

Ann Neurol

1986

;

19

:

275

–82.

Schneider JS, Diamond SG, Markham CH. Parkinson's disease: sensory and motor problems in arms and hands.

Neurology

1987

;

37

:

951

–6.

Schwarz M, Block F, Topper R, Sontag KH, Noth J. Abnormalities of somatosensory evoked potentials in the quinolinic acid model of Huntington's disease: evidence that basal ganglia modulate sensory cortical input.

Ann Neurol

1992

;

32

:

358

–64.

Sedgwick EM, Williams TD. The response of single units in the caudate nucleus to peripheral stimulation.

J Physiol (Lond)

1967

;

189

:

281

–98.

Seitz RJ, Roland PE. Vibratory stimulation increases and decreases the regional cerebral blood flow and oxidative metabolism: a positron emission tomography (PET) study.

Acta Neurol Scand

1992

;

86

:

60

–7.

Siesling S, Zwinderman AH, van Vugt JP, Kieburtz K, Roos RA. A shortened version of the motor section of the Unified Huntington's Disease Rating Scale.

Mov Disord

1997

;

12

:

229

–34.

Talairach J, Tournoux P. A co-planar stereotaxic atlas of the human brain. Stuttgart: Thieme; 1988.

Tempel LW, Perlmutter JS. Abnormal vibration-induced cerebral blood flow responses in idiopathic dystonia.

Brain

1990

;

113

:

691

–707.

Tempel LW, Perlmutter JS. Abnormal cortical responses in patients with writer's cramp [published erratum appears in Neurology 1994; 44: 2411].

Neurology

1993

;

43

:

2252

–7.

Topper R, Schwarz M, Podoll K, Domges F, Noth J. Absence of frontal somatosensory evoked potentials in Huntington's disease.

Brain

1993

;

116

:

87

–101.

Traversa R, Pierantozzi M, Semprini R, Loberti M, Cicardi MC, Bassi A, et al. N30 wave amplitude of somatosensory evoked potentials from median nerve in Parkinson's disease: a pharmacological study.

J Neural Transm Suppl

1995

;

45

:

177

–85.

Weeks RA, Ceballos-Baumann A, Piccini P, Boecker H, Harding AE, Brooks DJ. Cortical control of movement in Huntington's disease. A PET activation study.

Brain

1997

;

120

:

1569

–78.

Weiller C, Chollet F, Friston KJ, Wise RJ, Frackowiak RS. Functional reorganization of the brain in recovery from striatocapsular infarction in man.

Ann Neurol

1992

;

31

:

463

–72.

Yamada T, Rodnitzky RL, Kameyama S, Matsuoka H, Kimura J. Alteration of SEP topography in Huntington's patients and their relatives at risk.

Electroencephalogr Clin Neurophysiol

1991

;

80

:

251

–61.

© Oxford University Press 1999

© Oxford University Press 1999

Topic:

• second heart sound, s2
• parkinson disease
• basal ganglia
• huntington's disease
• basal ganglia diseases
• globus pallidus
• thalamus
• vibration
• premotor cortex
• insula of reil
• subcortical
• sensory processing

What is the main differences between Alzheimer's Parkinson's and Huntington's disease?

Can Huntington's be misdiagnosed as Parkinson's?

What Can Huntington's disease be mistaken for?

What disease has the same symptoms as Parkinson's disease?