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J. Richard Toleikis, Leo Verhagen Metman, Julie G. Pilitsis, Andrei Barborica, Sandra C. Toleikis and Roy A. E. Bakay

Object

Insight may be gained into the physiological mechanisms of deep brain stimulation (DBS) by analyzing local and contralateral subthalamic nucleus (STN) single-unit activity during activation of previously placed DBS electrodes. Special techniques are required to perform such analysis due to the presence of a large stimulus artifact. The purpose of this study was to determine the effects of DBS stimulation on single unit activity acquired from patients undergoing new or revised DBS placements.

Methods

Subthalamic nucleus single unit activity was acquired from awake patients during activation of a previously implanted STN DBS electrode. Stimulation was contralateral to the recording site in 4 cases and ipsilateral in 3. Data were acquired at stimulation frequencies of 30, 60, and 130 Hz and with other stimulation parameters at clinically effective settings. Cells were included if they showed kinesthetic activity before and after the stimulation paradigm and if their action potential morphology was maintained throughout the experiment. Analysis of single-unit activity acquired before, during, and after stimulation was performed employing a time-domain algorithm to overcome the stimulus artifact.

Results

Both ipsilateral and contralateral acute stimulation resulted in reversible STN firing rate suppression. The degree of suppression became greater as stimulus frequency increased and was significant at 60 Hz (t-test, p < 0.05) and 130 Hz (p < 0.01). Suppression with ipsilateral 130-Hz stimulation ranged between 52.8% and 99.8%, whereas with similar contralateral STN stimulation, the range was lower (1.9%–50.3%). Return to baseline activity levels typically occurred within seconds after stimulation ended.

Conclusions

Stimulation of the STN at clinically effective frequencies has an acute suppressive rather than an excitatory effect on STN single-unit activity. The effect is bilateral, even though the degree of suppression is greater on the ipsilateral than the contralateral STN. The authors' algorithm helps reveal this effect in human patients.

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Roy A. E. Bakay and Prasad S. S. V. Vannemreddy

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Roy A. E. Bakay and Prasad S. S. V. Vannemreddy

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Adam P. Smith and Roy A. E. Bakay

Object

Correct lead location in the desired target has been proven to be a strong influential factor for good clinical outcome in deep brain stimulation (DBS) surgery. Commonly, a surgeon's first reliable assessment of such location is made on postoperative imaging. While intraoperative CT (iCT) and intraoperative MR imaging have been previously described, the authors present a series of frameless DBS procedures using O-arm iCT.

Methods

Twelve consecutive patients with 15 leads underwent frameless DBS placement using electrophysiological testing and O-arm iCT. Initial target coordinates were made using standard indirect and direct assessment. Microelectrode recording (MER) with kinesthetic responses was performed, followed by microstimulation to evaluate the side-effect profile. Intraoperative 3D CT acquisitions obtained between each MER pass and after final lead placement were fused with the preoperative MR image to verify intended MER movements around the target area and to identify the final lead location. Tip coordinates from the initial plan, final intended target, and actual lead location on iCT were later compared with the lead location on postoperative MR imaging, and euclidean distances were calculated. The amount of radiation exposure during each procedure was calculated and compared with the estimated radiation exposure if iCT was not performed.

Results

The mean euclidean distances between the coordinates for the initial plan, final intended target, and actual lead on iCT compared with the lead coordinates on postoperative MR imaging were 3.04 ± 1.45 mm (p = 0.0001), 2.62 ± 1.50 mm (p = 0.0001), and 1.52 ± 1.78 mm (p = 0.0052), respectively. The authors obtained good merging error during image fusion, and postoperative brain shift was minimal. The actual radiation exposure from iCT was invariably less than estimates of exposure using standard lateral fluoroscopy and anteroposterior radiographs (p < 0.0001).

Conclusions

O-arm iCT may be useful in frameless DBS surgery to approximate microelectrode or lead locations intraoperatively. Intraoperative CT, however, may not replace fundamental DBS surgical techniques such as electrophysiological testing in movement disorder surgery. Despite the lack of evidence for brain shift from the procedure, iCT-measured coordinates were statistically different from those obtained postoperatively, probably indicating image merging inaccuracy and the difficulties in accurately denoting lead location. Therefore, electrophysiological testing may truly be the only means of precisely knowing the location in 3D space intraoperatively. While iCT may provide clues to electrode or lead location during the procedure, its true utility may be in DBS procedures targeting areas where electrophysiology is less useful. The use of iCT appears to reduce radiation exposure compared with the authors' traditional frameless technique.

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Vaninder Chhabra, Edward Sung, Klaus Mewes, Roy A. E. Bakay, Aviva Abosch and Robert E. Gross

Object

With the expanding indications and increasing number of patients undergoing deep brain stimulation (DBS), postoperative MR imaging is becoming even more important in guiding clinical care and practice-based learning; important safety concerns have recently emerged, however. Although phantom model studies have driven conservative recommendations regarding imaging parameters, highlighted by 2 recent reports describing adverse neurological events associated with MR imaging in patients with implanted DBS systems, the risks of MR imaging in such patients in clinical practice has not been well addressed. In this study, the authors capitalized on their large experience with serial MR imaging (3 times per patient) to use MR imaging itself and clinical outcomes to examine the safety of MR imaging in patients who underwent staged implantation of DBS electrodes for Parkinson disease, tremor, and dystonia.

Methods

Sixty-four patients underwent staged bilateral lead implantations between 1997 and 2006, and each patient underwent 3 separate MR imaging sessions subsequent to DBS placement. The first of these was performed after the first DBS placement, the second occurred prior to the second DBS placement, and third was after the second DBS placement. Follow-up was conducted to examine adverse events related either to MR imaging or to DBS-induced injury.

Results

One hundred and ninety-two MR images were obtained, and the mean follow-up time was 3.67 years. The average time between the first and second, and second and third MR imaging sessions was 19.4 months and 14.7 hours, respectively. Twenty-two MR imaging–detected new findings of hemorrhage were documented. However, all new findings were related to acute DBS insertion, whereas there were no new findings after imaging of the chronically implanted electrode.

Conclusions

Although potential risks of MR imaging in patients undergoing DBS may be linked to excessive heating, induced electrical currents, disruption of the normal operation of the device, and/or magnetic field interactions, MR imaging can be performed safely in these patients and provides useful information on DBS lead location to inform patient-specific programming and practice-based learning.

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Editorial

Mesial temporal lobe epilepsy

Kim J. Burchiel

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László Seress, Hajnalka Ábrahám, Zsolt Horváth, Tamás Dóczi, József Janszky, Joyce Klemm, Richard Byrne and Roy A. E. Bakay

Object

Hippocampal sclerosis can be identified in most patients with mesial temporal lobe epilepsy (TLE). Surgical removal of the sclerotic hippocampus is widely performed to treat patients with drug-resistant mesial TLE. In general, both epilepsy-prone and epilepsy-resistant neurons are believed to be in the hippocampal formation. The hilar mossy cells of the hippocampal dentate gyrus are usually considered one of the most vulnerable types of neurons. The aim of this study was to clarify the fate of mossy cells in the hippocampus in epileptic humans.

Methods

Of the 19 patients included in this study, 15 underwent temporal lobe resection because of drug-resistant TLE. Four patients were used as controls because they harbored tumors that had not invaded the hippocampus and they had experienced no seizures. Histological evaluation of resected hippocampal tissues was performed using immunohistochemistry.

Results

Mossy cells were identified in the control as well as the epileptic hippocampi by using cocaine- and amphetamine-regulated transcript peptide immunohistochemistry. In most cases the number of mossy cells was reduced and thorny excrescences were smaller in the epileptic hippocampi than in controls; however, there was a significant loss of pyramidal cells and a partial loss of granule cells in the same epileptic hippocampi in which mossy cell loss was apparent. The loss of mossy cells could be correlated with the extent of hippocampal sclerosis, patient age at seizure onset, duration of epilepsy, and frequency of seizures.

Conclusions

In many cases large numbers of mossy cells were present in the hilus of the dentate gyrus when most pyramidal neurons of the CA1 and CA3 areas of the Ammon's horn were lost, suggesting that mossy cells may not be more vulnerable to epileptic seizures than the hippocampal pyramidal neurons.

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S. Elizabeth Zauber, Nidhi Watson, Cynthia L. Comella, Roy A. E. Bakay and Leo Verhagen Metman

The authors report on a patient with craniocervical dystonia who was treated with bilateral GPi stimulation, with excellent improvement in dystonia but at the cost of stimulation-induced, reversible parkinsonism. Stimulation through ventral contacts resulted in maximal relief of craniocervical dystonia but induced considerable hypophonia, bradykinesia, rigidity, freezing, and impaired postural reflexes. Stimulation through dorsal contacts alleviated parkinsonism, but resulted in the return of dystonia. No stimulation parameters could alleviate the dystonia without inducing parkinsonism over the course of his 4-year follow-up.

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Julie G. Pilitsis, Leo Verhagen Metman, John R. Toleikis, Lindsay E. Hughes, Sepehr B. Sani and Roy A. E. Bakay

Object

Although nucleus ventralis intermedius stimulation has been shown to be safe and efficacious in the treatment of essential tremor, there is a subset of patients who eventually lose benefit from their stimulation. Proposed causes for this phenomenon include tolerance, disease progression, and suboptimal location. The goal of this study was to assess the factors that may lead to both stimulation failure, defined as loss of meaningful tremor relief, and less satisfactory outcomes, defined as leads requiring voltages > 3.6 V for effective tremor control.

Methods

The authors present their clinical outcomes from 31 leads in 27 patients who had effective tremor control for > 1 year following nucleus ventralis intermedius stimulation. All patients postoperatively had a mean decrease in both the writing and drawing subscales of the Fahn-Tolosa-Marin Tremor Rating Scale (p < 0.001).

Results

After a mean follow-up of 40 months, 22 patients continued to have tremor control with stimulation. Four patients eventually lost efficacy of their stimulation at a mean of 39 months. There was no difference in age, duration of disease, or disease severity between the groups. Examination of perioperative factors revealed that suboptimal anteroposterior positioning as evidenced on intraoperative fluoroscopy occurred significantly more frequently in patients with stimulation failure (p = 0.018). In patients with less satisfactory outcomes, no difference was seen between group demographics. Fluoroscopy again revealed suboptimal positioning more frequently in these patients (p = 0.005).

Conclusions

This study provides further evidence that suboptimal lead position in combination with disease progression or tolerance may result in less satisfactory long-term outcomes.

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Sepehr Sani, Kirk Jobe, Adam Smith, Jeffrey H. Kordower and Roy A. E. Bakay

Object

Given the success of deep brain stimulation (DBS) in a variety of applications (for example, Parkinson disease and essential tremor), other indications for which there is currently little effective therapy are being evaluated for clinical use of DBS. Obesity may be one such indication. Studies of the control of feeding and appetite by neurosurgical lesioning have been completed previously. This study was conducted to test the authors' hypothesis that continuous bilateral stimulatory inhibition of the rat lateral hypothalamic nucleus (LH) would lead to significant and sustained decrease in food intake and subsequent weight loss.

Methods

Sixteen Sprague–Dawley rats were maintained on a high-fat diet. Daily food intake and weight gain were measured for 7 days, at which time the animals underwent stereotactic placement of 0.25-mm-diameter bipolar stimulating electrodes bilaterally in the LH. On postoperative Day 7, eight animals began to receive continuous stimulation of the LH. The remaining eight animals were left unstimulated as the control group. Individual animal weight, food intake, and water intake were monitored daily and continuously throughout the experiment until postoperative Day 24.

Results

There was a decreased rate of weight gain after surgery in all animals, but the unstimulated group recovered and resumed a linear weight gain curve. The stimulated group, however, failed to show weight gain and remained below the mean baseline for body mass. There was a significant weight loss between the stimulated and unstimulated groups. On postoperative Day 24, compared with the day of surgery (Day 0), the unstimulated group had a mean weight gain of 13.8%, whereas the stimulated group had a 2.3% weight loss on average (p = 0.001), yielding a 16.1% weight difference between the two groups.

Conclusions

Bilateral electrical stimulatory inhibition of the LH is effective in causing significant and sustained weight loss in rats.