The impact of ventrolateral thalamotomy on high-frequency components of tremor

https://doi.org/10.1016/j.clinph.2005.01.012Get rights and content

Abstract

Objective

The present study assessed the impact of ventrolateral (VL) thalamotomy on the high-frequency components of tremor in patients with Parkinson's disease (PD).

Methods

Tremor was recorded prior to, and 7 days post-surgery using a laser displacement sensor. In addition, tremor was recorded in 10 age-matched patients with PD showing low amplitude tremor (named PD controls) and in 10 age-matched control subjects. Tremor recordings in patients were performed after a 12 h withdrawal from anti-Parkinsonian drugs. Tremor characteristics such as amplitude, median power frequency (MPF) and power dispersion (a measure of concentration of power in the frequency domain) were assessed for all groups (i.e. controls, PD controls, pre-surgery and post-surgery).

Results

All tremor characteristics were similar between controls and PD controls. Tremor amplitude was significantly reduced post-surgery, to become statistically similar to that of controls and PD controls. However, MPF and power dispersion remained lower post-surgery, indicating that although there was normalization of tremor amplitude, tremor showed systematically slower oscillations after the surgical procedure. In order to eliminate amplitude as a possible confounding factor, epochs of post-surgical tremor (5 s in duration) were paired for equal amplitude with 5 s tremor epochs from matched controls. Results show once again that MPF and power dispersion were lower post-surgery compared to controls. In addition, when amplitude of power was compared within specific frequency bands (0–3.5, 3.5–7.5, 7.5–12.5, 12.5–16.5, 16.5–30 and 30–45), power regained normal values at frequencies below 7.5 Hz. Power within higher frequency bands was systematically lower, indicating that the surgical procedure had an impact on high-frequency components of tremor.

Conclusions

Results from the present study showed that VL thalamotomy reduced tremor amplitude by selectively targeting centrally driven components of PD tremor. The high-frequency component of physiological tremor failed to emerge after amplitude normalization.

Significance

The thalamus should then be considered as an important component of the generation and/or propagation of high-frequency components of physiological tremor.

Introduction

Physiological tremor is defined as an oscillatory, roughly sinusoidal involuntary movement of a body part (Elble and Koller, 1990). It is now widely accepted that tremor oscillations are primarily the consequence of the interaction between mechanical characteristics of the limb in which tremor is measured (Marsden et al., 1969, Robson, 1959, Stiles and Randall, 1967, Van Buskirk et al., 1966, Yap and Boshes, 1967) and background motor-unit activity (Hagbarth and Young, 1979, Vaillancourt and Newell, 2000, Young and Hagbarth, 1980). Tremor oscillations associated with these ‘mechanical-reflex’ components are widely distributed throughout the power spectrum, up to 30 Hz for the finger (Stiles and Randall, 1967). Also to be considered are the centrally generated components of tremor, such as the one located within the 8–12 Hz band. These oscillations are believed to originate from a central oscillator located within the olivocerebellar (Lamarre et al., 1975, Llinas, 1984, Poirier et al., 1966) and/or cerebello-thalamo-cortical pathways (Duval et al., 2000, Lamarre, 1995). Centrally driven components might also exist at higher frequencies; around 25 Hz (Conway et al., 1995, Halliday et al., 1999, McAuley et al., 1997, Vaillancourt and Newell, 2000). However, others imply that these high-frequency components are produced by the muscle–spinal reflex loop, while the low frequency component of about 10 Hz originates from the central nervous system or from supraspinal reflex loop (Sakamoto et al., 1998). Whether these high-frequency components are indeed under direct central influence, and/or share similar neural pathways with the 8–12 Hz component is unknown.

Parkinson's disease (PD) tremor is usually large in amplitude and presents a well-defined frequency peak at around 4–5 Hz. Pathologically induced changes in firing patterns of neurons located within the basal ganglia (Hutchison et al., 1997, Pare et al., 1990), in combination with those in the thalamus (Hua et al., 1998, Lenz et al., 1988) and/or cortex (Volkmann et al., 1996), may be responsible for the creation of a central oscillator or oscillators, ultimately resulting in relatively high amplitude PD tremor. Here, centrally generated oscillations are large enough to overwhelm other mechanical-reflex components, and probably replace or overcome otherwise existing centrally driven components of physiological tremor. The impact of ventrolateral (VL) thalamotomy on tremor oscillations was recently examined by comparing the power spectrum of post-surgical tremor with those of age-matched control subjects, using epochs of tremor paired for equal amplitude (Duval et al., 2000). Results showed that the surgical procedure selectively eliminated the narrowly distributed Parkinsonian power peak, suggesting that the VL lesion targeted oscillations related to the centrally driven components of PD tremor. Furthermore, thalamotomy seemed to prevent the resurgence of the 8–12 Hz component of PT after amplitude normalization, suggesting that this component shared similar neural pathways with PD tremor at the level of the VL thalamus. If the VL thalamus is implicated in the generation and/or propagation of the high-frequency components of tremor, such as the ones believed to exit above 20 Hz, the surgical procedure may also have an impact on the power related to these frequencies. Accordingly, the goal of the present study was to assess the impact of VL thalamotomy on high-frequency components of tremor. Tremor from 10 patients who underwent VL thalamotomy was retrospectively examined using a proven methodology to determine the impact of the surgical procedure on high-frequency components of tremor (Duval et al., 2000). This time, the mean lesion location was confirmed using a probabilistic map methodology (Atkinson et al., 2002). Post-surgical tremor characteristics such as amplitude, median power frequency (MPF) and power dispersion were compared with those seen in age-matched control subjects. In addition, the amount of power found in post-surgical tremor, within specific frequency bands, was compared with those from matched controls using epochs of tremor paired for equal amplitude. Tremor from patients with PD showing low amplitude tremor was also examined; they served as a control group within the patient population.

Section snippets

Patients

Postural index finger tremor recordings from 10 patients with PD who underwent unilateral VL thalamotomy for tremor were analyzed (age range: 43–76, mean age: 63.7±10.3SD). Individual age, gender, handedness and UPDRS tremor scores are shown in Table 1. Tremor was recorded using a laser displacement sensor (LTS 90/45; LMI Technology, The Netherlands). The measuring range of this device was 45 mm, with a frequency response up to 20 kHz and a resolution better than 0.002 mm. This laser system is

Results

Fig. 1 shows a mid-sagittal view of the probabilistic map of lesions from the 10 surgical patients. In addition, Fig. 1 shows the results for amplitude, MPF and power distribution from all groups. Comparisons of amplitude, MPF and power dispersion between paired 5 s epochs are also shown. The map confirms that lesions were centered upon the ventral lateral (VLp) nucleus of the thalamus, the optimal target for tremor alleviation. The lesions encroached upon the most rostral shell region of the

Discussion

Results from the present study show that tremor amplitude was normalized after VL thalamotomy, from an average of 10 mm pre-surgery to less than 0.5 mm after the surgical procedure, hence attesting to the efficacy of the surgical procedure. However, several findings suggest that tremor was not normalized in the frequency domain. First, MPF and power dispersion remained lower post-surgery. After this drastic tremor amplitude reduction, one would expect to find a significant increase of MPF and

Acknowledgements

This research project was funded by an Operating Grant from the Canadian Institute for Health Research (AFS, APS), Canada Innovation Fund (CD), Ontario Innovation Trust (CD) and Parkinson Society Canada (CD).

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