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PubMed2005

Disease progression continues in patients with advanced Parkinson's disease and effective subthalamic nucleus stimulation.

OBJECTIVES: Glutamate mediated excitotoxicity of the hyperactive subthalamic nucleus (STN) has been reported to contribute to nigral degeneration in Parkinson's disease (PD). Deep brain stimulation of the STN (STN DBS), in its role as a highly effective treatment of severe PD motor complications, has been thought to inhibit STN hyperactivity and therefore decrease progression of PD. METHODS: In a prospective two centre study, disease progression was determined by means of serial (18)F-fluorodopa (F-dopa) positron emission tomography (PET) in 30 patients with successful STN DBS over the first 16 (SD 6) months after surgery. RESULTS: Depending on the method of PET data analysis used in the two centres, annual progression rates relative to baseline were 9.5-12.4% in the caudate and 10.7-12.9% in the putamen. CONCLUSIONS: This functional imaging study is the first to demonstrate a continuous decline of dopaminergic function in patients with advanced PD under clinically effective bilateral STN stimulation. The rates of progression in patients with STN DBS were within the range of previously reported data from longitudinal imaging studies in PD. Therefore this study could not confirm the neuroprotective properties of DBS in the STN target.

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PubMed2001

Deep brain stimulation of the subthalamic nucleus: clinical effectiveness and safety.

The authors report the data relative to the clinical effectiveness of bilateral deep brain stimulation of the subthalamic nucleus in 16 patients with PD 3 months after the surgery. The comparison of the Unified PD Rating Scale scores in the different conditions of medication and stimulation, and the lack of significant surgical complications, confirm the effectiveness and the safety of the subthalamic nucleus deep brain stimulation for the treatment of advanced PD.

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PubMed2003

Temporal changes in movement time during the switch of the stimulators in Parkinson's disease patients treated by subthalamic nucleus stimulation.

OBJECTIVE: Deep brain stimulation (DBS) of the subthalamic nucleus (STN) is a very effective therapy for the advanced phase of Parkinson's disease (PD). The functional inhibition of this nucleus is responsible for a significant improvement of cardinal motor symptoms of PD. The aim of the study was the assessment of the effectiveness of STN DBS on bradykinesia by the analysis of movement time (MT) in 2 conditions: with the stimulators turned on ('stim-on') or off ('stim-off'). METHODS: After pharmacological wash-out, 10 patients submitted to bilateral STN DBS were studied with an MT analyser in 3 phases: stim-on, stim-off and stim-on again, in order to establish the time course of MT lengthening, the posteffect duration and the latency of the effect of STN DBS. MT data were then compared with the UPDRS motor scores. RESULTS: After turning off the stimulators, MT progressively increases, reaching a plateau after about 30 min, which then lasts for the subsequent observation time (2 h). A significant elongation is achieved after the first 5 min. Upon pulse generator activation, MT shows a dramatic shortening, already significant after 2 min. Moreover, we observed a significant correlation between MT and the severity of PD, higher with bradykinesia than with rigidity or tremor. CONCLUSION: Our findings show a relevant effect of STN DBS on MT, a parameter strongly related to bradykinesia. This study confirms the effectiveness of STN inhibition on the whole parkinsonian triad, suggesting that this target can be considered a proper choice for the surgical treatment of advanced PD.

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PubMed1986

Interconnections between the subthalamic nucleus and the cerebral cortex of the cat.

The corticosubthalamic and subthalamocortical projections were examined in the cat by anterograde and retrograde axonal transport of horseradish peroxidase (HRP). Injections of HRP into the gyrus proreus, gyrus sigmoideus anterior and the part lateral to the sulcus cruciatus gave rise to anterogradely labelled terminals in all parts of the ipsilateral subthalamic nucleus in a topographical manner. Injections of HRP into these cerebral cortices as well as the gyrus sigmoideus posterior, the posterior part of the gyrus coronalis and the middle part of the gyrus ectosylvius produced retrogradely labelled neurons in the medial half of the ipsilateral subthalamic nucleus in a topographical manner. These findings suggest that the subthalamic nucleus acts as a link not only in the pallido-subthalamo-pallidal loop but also in the corticosubthalamo-cortical pathways.

Animals↗

PubMed2005

Anatomical alterations of the subthalamic nucleus in relation to age: a postmortem study.

The subthalamic nucleus (STN) is currently the preferred target for chronic electrical high-frequency stimulation in Parkinson's disease. Anatomical determination of the exact position of the STN in the individual patient, using magnetic resonance imaging, remains cumbersome, whereas calculation of the target using a stereotactic atlas bypasses patient interindividual variations in the exact delineation of the STN. The aim of this study was to demonstrate variations in shape and position of the STN during life. In this anatomopathological study, a method was applied to localize the STN in reference to the anterior commissure-posterior commissure line (AC-PC line) in 12 postmortem brains of patients who died of non-neurological diseases. Their age varied from 29 to 84 years. Centers and borders of the STN were macroscopically measured in three spatial orthogonal planes in relation to the AC-PC line, and verified by light microscopy. The AC-PC distance remains almost constant during life (24.4 mm; SD 3.58). With increasing age, the center of the STN tends to move 3.9 mm cranially, 2.6 mm laterally, and 0.2 mm anteriorly. This last result also differs from the position mentioned in the stereotactic brain atlases. The form of the STN also changes. During life, the STN becomes wider in the mediolateral direction and smaller in the superior-inferior and anterior-posterior direction. The shape and spatial position of the STN also change during life. These changes should be taken into account during target determination in deep brain stimulation procedures in Parkinson's disease.

Adult↗

PubMed2006

Does subthalamic nucleus stimulation induce apathy in Parkinson's disease?

BACKGROUND: Subthalamic Nucleus Deep Brain Stimulation (STN-DBS) has been shown to significantly improve motor symptoms in advanced Parkinson's disease (PD). Only few studies, however, have focused on the non-motor effects of DBS. METHODS: A consecutive series of 15 patients was assessed three months before (M-3), then three months (M3) and six months (M6) after surgery. Mean (+/- SD) age at surgery was 59.7 (7.6). Mean disease duration at surgery was 12.2 (2.8) years. The Mini International Neuropsychiatric Inventory was used to assess psychiatric disorders three months before surgery. Depression was evaluated using Montgomery and Asberg Rating Scale (MADRS). Anxiety was evaluated using the AMDP system (Association for Methodology and Documentation in Psychiatry). Apathy was particularly evaluated using the Apathy Evaluation Scale (AES) and the Starkstein Scale. All these scales were performed at every evaluation. RESULTS: Apathy worsened at M3 and M6 after STN-DBS in comparison with the preoperative evaluation: the AES mean score was significantly impaired between the preoperative (38.4+/-7.1) and both the postoperative M3 (44.6+/-9.5, p = 0.003) and M6 scores (46.0+/-10.9, p = 0.013). Significant worsening of apathy was confirmed using the Starkstein scale. There was no evidence of depression: the mean MADRS score did not differ before surgery (9.1+/-7.4) and at both M3 (8.6+/-8.2) and M6 (9.9+/-7.7) after STN-DBS. The anxiety level did not change between preoperative (9.4+/-9.2) and both M3 (5.5+/-4.5) and M6 (6.6+/-4.6) postoperative states. CONCLUSION: Although STN-DBS constitutes a therapeutic advance for severely disabled patients with Parkinson's disease, we should keep in mind that this surgical procedure may contribute to the inducing of apathy. Our observation raises the issue of the direct influence of STN- DBS on the limbic system by diffusion of stimulus to the medial limbic compartment of STN.

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PubMed2001

Lidocaine and muscimol microinjections in subthalamic nucleus reverse Parkinsonian symptoms.

Inactivation of neurones in the subthalamic nucleus (STN) of the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine treated monkey model of Parkinson's disease has been shown to relieve parkinsonian motor symptoms. In patients with Parkinson's disease, neurones in the STN display hyperactive firing rates and rhythmic discharge activity such as tremor-related oscillations (3-8 Hz) and synchronous high-frequency oscillations (15-30 Hz). In this study, microinjections of lidocaine (n = 4) and muscimol, a GABA(A) receptor agonist (n = 2), were performed in the STN of six patients with Parkinson's disease to determine whether the focal suppression of STN neuronal activity can lead to an improvement in tremor, bradykinesia and rigidity. We also report the first use of microelectrode recording of the effects of microinjections on neuronal activity in the human brain (n = 2). Microinjections of 10-23 microl of lidocaine produced striking improvements in bradykinesia, limb tremor and rigidity in three out of three patients. These improvements were correlated with good therapeutic effects of subsequent STN deep brain stimulation performed in the same microelectrode trajectories as these injections. The most dramatic observation following lidocaine injections was the appearance of dyskinetic limb movements. In one patient, simultaneous microelectrode recording during an injection of 3.5 microl of lidocaine demonstrated a suppression of neuronal activity at distances of < 0.9 mm from the injection site, but no suppression was observed at > or = 1.2 mm from the injection site. Microinjections of 5-10 microl of muscimol in a region with tremor-related activity resulted in suppression of limb tremor in two out of two patients. Interestingly, in one of these patients, 4 Hz oscillatory activity was diminished in a neurone recorded 1.3 mm from the injection site, but there was no reduction in the mean firing rate or 20 Hz oscillatory activity. These results demonstrate that inactivation of neuronal activity in the STN of patients with Parkinson's disease improves motor symptoms. These findings also suggest that a focal block of the STN might alter the oscillatory activity of neurones located beyond the inhibited region.

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PubMed2005

Fracture of subthalamic nucleus deep brain stimulation hardware as a result of compulsive manipulation: case report.

OBJECTIVE AND IMPORTANCE: Trichotillomania (TTM) is an impulse control disorder characterized by the recurrent pulling of one's hair resulting in noticeable hair loss. There has been no definite association drawn between Parkinson's disease (PD) and TTM, although there is a suggestion that obsessive-compulsive symptomatology may be more prevalent in left-side predominant PD. We believe that it is important to be aware of psychiatric comorbidities in the surgical treatment of PD, as they may significantly impact the postoperative course. CLINICAL PRESENTATION: We describe the case of a 58-year-old woman with an eleven-year history of left-side predominant PD who also suffered from TTM. She underwent subthalamic nucleus deep brain stimulation (STN-DBS) and subsequently developed significant wound complications of her left-sided deep brain stimulation leads. It was noted during the postoperative period that the patient was picking her left-sided, but not right-sided, incision-a behavior that was felt to be a part of this patient's impulse control disorder. INTERVENTION: Multiple wound revisions and eventual replacement of her left-sided deep brain stimulation lead was performed as a result of hardware malfunction secondary to wound manipulation by the patient. CONCLUSION: Before surgery, this patient's TTM was right-sided, but after subthalamic nucleus deep brain stimulation, her wound picking was only left-sided. This case suggests that subthalamic nucleus deep brain stimulation may have a role in unleashing the symptomatology of TTM through an as yet poorly understood mechanism. Furthermore, there is also an implication that the pathophysiology of PD and TTM may be intertwined.

Deep Brain Stimulation↗

PubMed1994

Subthalamic nucleus modulates burst firing of nigral dopamine neurones via NMDA receptors.

The role of the subthalamic nucleus in the burst firing of dopamine neurones of the substantia nigra was investigated using extracellular single unit recordings combined with pressure or iontophoretic micro-injections in anaesthetized rats. Inhibition of subthalamic neurones by pressure injection of gamma-aminobutyric acid (GABA) regularized the burst firing pattern in eight out of 17 dopamine neurones. Bicuculline injection near subthalamic neurones increased their firing rate and increased burst discharge in a subpopulation of dopamine neurones tested (34 out of 102). The increase was depressed by iontophoresis of the N-methyl-D-aspartate (NMDA) antagonist (+-)2-amino,5-phosphonopentanoic acid (AP-5), but not of the non-NMDA antagonist, 6-cyano,7-nitroquinoxaline-2,3-dione (CNQX). These data suggest that the subthalamic nucleus promotes burst discharge in a subpopulation of substantia nigra dopamine neurones via NMDA receptors.

2-Amino-5-phosphonovalerate↗

PubMed2003

Correlated multisecond oscillations in firing rate in the basal ganglia: modulation by dopamine and the subthalamic nucleus.

Previous studies from this laboratory have shown that many neurons in the basal ganglia have multisecond (<0.5 Hz) periodicities in firing rate in awake rats. The frequency and regularity of these oscillations are significantly increased by systemically injected dopamine (DA) agonists. Because oscillatory activity should have greater functional impact if shared by many neurons, the level of correlation of multisecond oscillations was assessed by recording pairs of neurons in the globus pallidus and substantia nigra pars reticulata in the same hemisphere, or pairs of globus pallidus neurons in opposite hemispheres in awake, immobilized rats. Cross-correlation (90-180 s lags) and spectral analysis were used to characterize correlated oscillations. Thirty-eight percent of pairs recorded in baseline (n=50) demonstrated correlated multisecond oscillations. Phase relationships were near 0 or 180 degrees. DA agonist injection significantly increased the incidence of correlation (intra- and interhemispheric) to 94% (n=17). After DA agonist injection, phase relationships of globus pallidus/substantia nigra neuron pairs were exclusively concentrated near 180 degrees, and phases of interhemispheric pairs of globus pallidus neurons were concentrated near 0 degrees. After subthalamic nucleus lesion (n=8), the incidence of correlated multisecond oscillations (or of multisecond oscillations per se) was not changed, although the consistent phase relationship between the globus pallidus and substantia nigra pars reticulata was disrupted. Subthalamic lesion also blocked apomorphine-induced decreases in oscillatory period and increases in oscillation amplitude, and significantly attenuated apomorphine-induced changes in mean firing rate. The data demonstrate that multisecond oscillations in the basal ganglia can be correlated between nuclei, and that DA receptor activation increases the level of correlation and organizes internuclear phase relationships at these multisecond time scales. While the subthalamic nucleus is not necessary for generating or transmitting these slow oscillations, it is involved in DA agonist-induced modulation of mean firing rate, oscillatory period, and internuclear phase relationship. These data further support a role for DA in modulating coherent oscillatory activity in the basal ganglia, and for the subthalamic nucleus in shaping the effects of DA receptor stimulation on basal ganglia output.

Animals↗

PubMed2006

Subthalamic nucleus influences spatial orientation in extra-personal space.

While the role of frontal and parietal cortex in spatial orientation has been studied extensively, the contribution of the basal ganglia and especially the subthalamic nucleus to spatial orientation remains less clear. Here we use subthalamic nucleus (STN) deep brain stimulation (DBS) in Parkinson's disease (PD) as a reversible model of functional lesioning to evaluate the influence of the STN in extra-personal space orientation. To this end, 12 PD patients were examined 1 year after implantation of DBS electrodes in the STN after overnight withdrawal of L-dopa. Patients were tested in a pseudo-randomized order while both stimulators, the right only, the left only, or no stimulator, were switched on. Patients performed line bisection and a reaction time task responding to stimuli of the middle, the left, and the right extra-personal space. A separate assessment of the right and left hand responding to visual stimuli in each hemispace made it possible to distinguish hemi-spatial and hemi-motor impairments. No asymmetries in space orientation were found when both stimulators were switched OFF, when both stimulators were switched ON, and when only the right stimulator was switched ON. When only the left subthalamic stimulation was switched ON, the reaction times of both hands to visual stimuli in the left extra-personal hemispace increased significantly and the line bisection test showed a significant orientation to the right. These results lead to the conclusion that the STN and its cortical projections influence the network involved in visuospatial orientation. These patterns of symptoms of neglect demonstrate the influence of the STN on the attentional system of the nondominant hemisphere.

Attention↗

PubMed2006

Elevations in local gamma activity are accompanied by changes in the firing rate and information coding capacity of neurons in the region of the subthalamic nucleus in Parkinson's disease.

Local field potential (LFP) gamma (55-95 Hz) activity has been recorded in the vicinity of the subthalamic nucleus with both microelectrodes and macroelectrodes in patients with Parkinson's disease undergoing functional neurosurgery. Although this activity increases with movement its functional significance remains unknown. We hypothesised that elevations in local gamma activity might be associated with an increase in the capacity of individual spike trains to code information. Changes in the median firing frequency, entropy and baud were determined during spontaneous variations in the level of simultaneously recorded LFP gamma activity in a sample of 31 neurons. The latter were recorded from the zona incerta (n = 5) and subthalamic nucleus (n = 26) in 10 parkinsonian patients. Although 19% of neurons showed a decrease in firing rate, overall there was a net increase in spike frequency and baud of 18.0+/-5.5% and 16.9+/-5.3%, when periods of high gamma were compared to periods of low gamma LFP activity. In contrast, entropy dropped by only 0.8+/-0.2% across the sampled neuronal population during periods of high gamma. All net changes were significant. We conclude that overall there was a net elevation in firing rate and potential information coding capacity, assessed in terms of baud, amongst neurons during periods of elevated gamma LFP activity in the subthalamic region.

Action Potentials↗

PubMed1994

Subthalamic nucleus and globus pallidus lesions alter activity in nigrothalamic neurons in rats.

Lesions of the subthalamic nucleus or the globus pallidus altered the response of substantia nigra pars reticulata neurons (antidromically identified as projecting to the thalamus) to electrical stimulation of the frontal agranular cortex. In intact animals, cortical stimulation evokes three independent responses (excitation, inhibition, excitation) that may occur singly or in various combinations. The independence of the various responses, especially the temporally coincident excitatory and inhibitory responses, suggests that the net inhibitory and excitatory pathways carrying these signals from the cortex may converge to varying degrees on individual nigrothalamic neurons. Subthalamic lesions increased total response duration (from 28.4 to 39.7 ms), increased the duration of inhibition (from 18 to 30 ms), decreased the occurrence of excitatory responses, and decreased the intensity of the second excitation (from 1.1 to 0.6 spikes/s). Lesion of the globus pallidus also increased total response duration (up to 38 ms), but by increasing the duration of the second excitation (from 15.1 up to 23.8 ms). The intensity of the second excitation (from 1.1 to 1.5 spikes/stimulus) and the number of cells showing the first and second excitations also increased. The incidence, but not the duration, of the inhibition increased. The mean firing rate increased after subthalamic nucleus lesion (34.2 spikes/s) as compared to intact (27.0) or globus pallidus lesion (25.6). These changes may reflect changes in the relative contribution of the five different pathways transmitting information from the cortex to the substantia nigra. In all cases the cortico-striato-nigral pathway is largely intact.(ABSTRACT TRUNCATED AT 250 WORDS)

Animals↗

PubMed1995

Turning behavior in rats with unilateral lesions of the subthalamic nucleus: synergism between D1 and D2 receptors.

Rats with unilateral kainic acid lesion of the subthalamic nucleus showed a dose dependent rotational response to the lesioned side (ipsilateral) after systemic administration of the non-selective dopaminergic agonist apomorphine. Both D2 and D1 selective antagonists ((-)sulpiride and SCH23390) inhibited the response to apomorphine in these rats. Selective D2 and D1 agonists (quinpirole and SKF38393) were unable to induce turning behavior. However, an ipsilateral circling response was obtained after the simultaneous application of both agonists. The interaction mechanism between dopaminergic receptor subtypes seems to be similar to that of other normosensitive models of turning previously studied (Barone et al., 1986; Robertson and Robertson, 1986; Arnt and Perregard, 1987; Asim et al., 1990; Pazo et al., 1993). It is proposed that the ipsilateral turning response to dopaminergic agonists in rats with subthalamic nucleus lesion results from an impaired behavioral expression of the action of dopaminergic agonists on one side, leading the rats to turn away from the intact hemisphere.

Animals↗

PubMed2003

Estimating the costs of surgical innovations: the case for subthalamic nucleus stimulation in the treatment of advanced Parkinson's disease.

We estimated the current cost of deep brain stimulation surgery targeted on the subthalamic nucleus. The method used was a cost analysis using typical resource use patterns and unit costs from a leading surgical centre, detailed equipment costs from the manufacturer, and sensitivity analysis. Resource use was based on patients with advanced Parkinson's disease. The main outcome measure was the likely total health service costs per patient, including preoperative assessment, surgery, and postoperative management over a 5-year period. The preoperative assessment, surgery, and discounted follow-up costs associated with subthalamic nucleus surgery were estimated at approximately UK Pounds 32,526 per patient over 5 years. Almost 70% of these costs are attributable to the initial costs of the equipment and the likely follow-up and replacement costs of the equipment. These costs will be affected mainly by future equipment costs and their replacement period and are relatively insensitive to preoperative assessment staff costs, length of hospital stay after surgery, and imaging costs. This cost estimate should be of use to researchers, health care managers, policy makers, and surgeons working in this area. Providing an estimate of the cost of this new procedure will provide a baseline for tracking future changes in costs and will assist the production of cost-effectiveness estimates.

Data Collection↗

PubMed1999

Deep brain stimulation of the subthalamic nucleus for control of extrapyramidal features in advanced idiopathic parkinson's disease: one year follow-up.

UNLABELLED: Deep brain stimulation (DBS) of the subthalamic nucleus (STN) with a quadripolar electrode was carried out in 9 patients with advanced idiopathic Parkinson's disease (PD) affected with severe diurnal motor fluctuations. The effect of bilateral STN stimulation was evaluated by clinical methods in all patients after 3 and 12 months. Assessment was based on the Unified Parkinson's Disease Rating Scale (UPDRS), timed motor tests, the Schwab and England Activities of Daily Living and a diary chart to document motor fluctuations. Alterations in parkinsonian signs, motor performance and functional outcome were recorded postoperatively (1) under temporary complete withdrawal of both STN stimulation and medication; (2) in the presence of STN stimulation only; and (3) in the presence of both STN stimulation and medication. The results were compared with the preoperative data assessed in defined on-phase and defined off-phase. STN stimulation on (compared to STN stimulation off) results in a significant improvement in UPDRS motor scores: after 3 months from 50.5 +/- 14.3 to 27.8 +/- 5.8, and after 12 months from 49.4 +/- 14.1 to 27.1 +/- 7.1 (p < 0.01). There was a significant decrease in the average duration of off-periods from 8.82 +/- 2.47 hours to 1.00 +/- 1.06 hours (p < 0.001), a marked increase in on-periods without dyskinesia from 4.62 +/- 2.72 to 14.62 +/- 1.51 hours (p < 0.01), and a sharp drop in on-periods with dyskinesia from 2.87 (+/- 4.18) to 0.25 (+/- 0.97) hours (p < 0.05), which remained stable up to 12 months (off-periods: 1.25 +/- 1.58 hours, p < 0.001; on-periods without: 13.87 +/- 1.95 hours, p < 0.001; and on-periods wth dyskinesia: 0.37 +/- 1.06 hours, p < 0.05). However, our first PD patient with an implanted DBS electrode within the STN died from cardiac infarction two days after surgery. This sudden death was not linked either to surgery nor to stimulation - and happened by chance. Our findings confirm that STN stimulation is a suitable functional neurosurgical procedure for the modulation and control of PD signs associated with severe motor fluctuations, in that they demonstrate a beneficial effect which was fully sustained over a one year follow-up period. KEYWORDS: Subthalamic nucleus, deep brain stimulation, Parkinson's disease.

Activities of Daily Living↗

PubMed1995

Bilateral subthalamic nucleus stimulation for severe Parkinson's disease.

Subthalamic nucleus (STN) lesions or high-frequency stimulations could improve parkinsonian symptoms in monkeys treated by MPTP. We have applied the procedure of chronic stimulation to the STN in severely disabled parkinsonian patients. This article presents the case of the first patient operated on bilaterally. Bilateral STN stimulation has greatly improved akinesia and rigidity. The benefit was maintained < or = 15 months after surgery. Unilateral stimulation induced motor effects mainly in contralateral limbs. Further studies are needed to evaluate the value of this procedure in the treatment of Parkinson's disease.

Antiparkinson Agents↗

PubMed1996

Abnormal involuntary movements induced by subthalamic nucleus stimulation in parkinsonian patients.

Chronic electrical subthalamic nucleus (STN) stimulation is under investigation for alleviating parkinsonian symptoms. STN alterations may carry the risk of provoking abnormal involuntary movements (AIMs). We took advantage of the reversibility of the stimulation technique to assess the possibility of inducing AIMs, using different electrical variables with or without concomitant levodopa intake. Above a given threshold voltage, stimulation could induce contralateral distal mobile AIMs or hemiballism in the off-drug condition in two patients. AIMs occurred after a latency that varied from a few minutes up to several hours after switching on the stimulator. Hemiballism immediately disappeared upon switching off the stimulator. In these patients, levodopa had never provoked that type of AIMs before surgery. Levodopa-induced AIMs were not modified by electrical stimulation, but off-phase dystonia disappeared in one patient. Stimulation of the STN induced AIMs that resembled both those observed following spontaneous lesions of the STN and levodopa-induced diphasic AIMs in parkinsonian patients. As electrical stimulation provoked AIMs and antiparkinsonian benefit occurred with different electrical variables and different timing, the mechanisms responsible for these two effects could be distinct.

Antiparkinson Agents↗