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Determining the position and size of the subthalamic nucleus based on magnetic resonance imaging results in patients with advanced Parkinson disease

Erich O. Richter, Tasnuva Hoque, William Halliday, Andres M. Lozano, and Jean A. Saint-Cyr

Object. The subthalamic nucleus (STN) is a target in surgery for Parkinson disease, but its location according to brain atlases compared with its position on an individual patient's magnetic resonance (MR) images is incompletely understood. In this study both the size and location of the STN based on MR images were compared with those on the Talairach and Tournoux, and Schaltenbrand and Wahren atlases.

Methods. The position of the STN relative to the midcommissural point was evaluated on 18 T2-weighted MR images (2-mm slices). Of 35 evaluable STNs, the most anterior, posterior, medial, and lateral borders were determined from axial images, dorsal and ventral borders from coronal images. These methods were validated using histological measurements in one case in which a postmortem examination was performed.

The mean length of the anterior commissure—posterior commissure was 25.8 mm. Subthalamic nucleus borders derived from MR imaging were highly variable: anterior, 4.1 to −3.7 mm relative to the midcommissural point; posterior, 4.2 to 10 mm behind the midcommissural point; medial, 7.9 to 12.1 mm from the midline; lateral, 12.3 to 15.4 mm from the midline; dorsal, 0.2 to 4.2 mm below the intercommissural plane; and ventral, 5.7 to 9.9 mm below the intercommissural plane.

The position of the anterior border on MR images was more posterior, and the medial border more lateral, than its position in the brain atlases. The STN was smaller on MR images compared with its size in atlases in the anteroposterior (mean 5.9 mm), mediolateral (3.7 mm), and dorsoventral (5 mm) dimensions.

Conclusions. The size and position of the STN are highly variable, appearing to be smaller and situated more posterior and lateral on MR images than in atlases. Care must be taken in relying on coordinates relative to the commissures for targeting of the STN.

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The regulation of adult rodent hippocampal neurogenesis by deep brain stimulation

Laboratory investigation

Hiroki Toda, Clement Hamani, Adrian P. Fawcett, William D. Hutchison, and Andres M. Lozano

Object

To examine the influence of deep brain stimulation on hippocampal neurogenesis in an adult rodent model.

Methods

Rats were anesthetized and treated for 1 hour with electrical stimulation of the anterior nucleus of the thalamus (AN) or sham surgery. The animals were injected with 5′-bromo-2′-deoxyuridine (BrdU) 1–7 days after surgery and killed 24 hours or 28 days later. The authors counted the BrdU-positive cells in the dentate gyrus (DG) of the hippocampus. To investigate the fate of these cells, they also stained sections for doublecortin, NeuN, and GFAP and analyzed the results with confocal microscopy. In a second set of experiments they assessed the number of DG BrdU-positive cells in animals treated with corticosterone (a known suppressor of hippocampal neurogenesis) and sham surgery, corticosterone and AN stimulation, or vehicle and sham surgery.

Results

Animals receiving AN high-frequency stimulation (2.5 V, 90 μsec, 130 Hz) had a 2- to 3-fold increase in the number of DG BrdU-positive cells compared with nonstimulated controls. This increase was not seen with stimulation at 10 Hz. Most BrdU-positive cells assumed a neuronal cell fate. As expected, treatment with corticosterone significantly reduced the number of DG BrdU-positive cells. This steroid-induced reduction of neurogenesis was reversed by AN stimulation.

Conclusions

High-frequency stimulation of the AN increases the hippocampal neurogenesis and restores experimentally suppressed neurogenesis. Interventions that increase hippocampal neurogenesis have been associated with enhanced behavioral performance. In this context, it may be possible to use electrical stimulation to treat conditions associated with impairment of hippocampal function.

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Absence of collagen deficiency in familial cerebral aneurysms

Richard Leblanc, Andrés M. Lozano, Michel van der Rest, and Ronald David Guttmann

✓ It has been suggested that a deficiency in the expression of type III collagen may play a role in the pathogenesis of cerebral aneurysms. To test this hypothesis in cases of familial cerebral aneurysms, fibroblast cell cultures were established and the expression of collagen types I and III was studied in a patient with three cerebral aneurysms whose mother and sister also had cerebral aneurysms. Cultured skin fibroblasts were labeled with tritiated proline. The collagens and procollagens were precipitated and run on sodium dodecyl sulfate-polyacrylamide gel electrophoresis after reduction to analyze procollagen chains. Control cell lines were analyzed simultaneously. Quantitation of the ratios of type III to type I procollagen synthesis was achieved by integration of the intensities of the pro-α1 (III), pro-α1(I), and pro-α2(I) bands on fluorograms of electrophoretic gels of medium proteins.

There was no difference in type I and III procollagen levels observed between the cells from the aneurysm patient and those from the control cell lines. These data do not support the hypothesis that familial cerebral aneurysms are caused by a deficiency of type III collagen.

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Letter to the Editor: Bibliometrics

Paul Klimo Jr., L. Madison Michael II, Garrett T. Venable, and Douglas R. Taylor

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Microstimulation-induced inhibition as a tool to aid targeting the ventral border of the subthalamic nucleus

Clinical article

Myriam Lafreniere-Roula, William D. Hutchison, Andres M. Lozano, Mojgan Hodaie, and Jonathan O. Dostrovsky

Object

The aim of the current study was to examine and compare the aftereffects of local high-frequency microstimulation through the recording electrode on the firing of neurons in the subthalamic nucleus (STN) and the substantia nigra pars reticulata (SNr) in patients undergoing surgery for deep brain stimulation. Deep brain stimulation has been playing an increasing role in the treatment of Parkinson disease, with the subthalamic nucleus (STN) being the preferred implantation target. Changes in cellular activity indicative of the borders of the STN are typically used during surgery to determine the extent of the STN and locate the optimal target, but in some cases borders may be difficult to identify. In this study the authors compared the effects of microstimulation in the SNr and STN. In previous studies they have shown that microstimulation in the internal globus pallidus, which is functionally similar to the SNr, inhibits firing, whereas similar microstimulation in the STN has minimal effect. The presence of inhibition in the SNr but not in the STN could be used as an additional criterion to help identify the location of the border between the STN and SNr.

Methods

Dual microelectrode recordings were performed during stereotactic surgery in 4 patients. Well-isolated high-amplitude units were stimulated extracellularly through the recording microelectrode with 0.5-second trains of high frequency (200 Hz) and low current (≤ 5 μA).

Results

In the majority (92%) of SNr neurons, this type of stimulation led to a period of inhibition lasting several hundreds of milliseconds following the end of the train. In contrast, only 1 neuron of 70 judged to be in the STN by other criteria was inhibited by this type of microstimulation, and this neuron was located at the ventral border of the STN.

Conclusions

These findings indicate that prolonged inhibition of firing following low-amplitude high-frequency microstimulation via the recording electrode is a consistent feature of almost all SNr neurons and rarely if ever occurs in STN neurons. This feature therefore provides a useful additional finding that can be used to help identify the border between the STN and SNr.

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Movement-related neurons of the subthalamic nucleus in patients with Parkinson disease

Aviva Abosch, William D. Hutchison, Jean A. Saint-Cyr, Jonathan O. Dostrovsky, and Andres M. Lozano

Object. The subthalamic nucleus (STN) is a target in the surgical treatment of Parkinson disease (PD). Little is known about the neurons within the human STN that modulate movement. The authors' goal was to examine the distribution of movement-related neurons within the STN of humans by using microelectrode recording to identify neuronal receptive fields.

Methods. Data were retrospectively collected from microelectrode recordings that had been obtained in 38 patients with PD during surgery for placement of STN deep brain stimulation electrodes. The recordings had been obtained in awake, nonsedated patients. Antiparkinsonian medications were withheld the night before surgery. Neuronal discharges were amplified, filtered, and displayed on an oscilloscope and fed to an audio monitor. The receptive fields were identified by the presence of reproducible, audible changes in the firing rate that were time-locked to the movement of specific joint(s).

The median number of electrode tracks per patient was six (range two–nine). The receptive fields were identified in 278 (55%) of 510 STN neurons studied. One hundred one tracks yielded receptive field data. Fourteen percent of 64 cells tested positive for face receptive fields, 32% of 687 cells tested positive for upper-extremity receptive fields, and 21% of 242 cells tested positive for lower-extremity receptive fields. Sixty-eight cells (24%) demonstrated multiple-joint receptive fields. Ninety-three cells (65%) with movement-related receptive fields were located in the dorsal half of the STN, and 96.8% of these were located in the rostral two thirds of the STN. Analysis of receptive field locations from pooled data and along individual electrode tracks failed to reveal a consistent somatotopic organization.

Conclusions. Data from this study demonstrate a regional compartmentalization of neurons with movement-related receptive fields within the STN, supporting the existence of specific motor territories within the STN in patients suffering from PD.

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Editorial. Deep brain stimulation for tinnitus: exploring the frontier between sensory perception and awareness

Martin Jakobs and Andres M. Lozano

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Methods for microelectrode-guided posteroventral pallidotomy

Andres Lozano, William Hutchison, Zelma Kiss, Ronald Tasker, Karen Davis, and Jonathan Dostrovsky

✓ Methods for localizing the posteroventral globus pallidus internus are described. The authors' techniques include the use of microelectrodes to record single-unit activity and to microstimulate in human pallidum and its surrounding structures. This technique allows a precise determination of the locations of characteristic cell types in sequential trajectories through the external and internal segments of the pallidum. The location of the optic tract can be determined from microstimulation-evoked visual sensations and recordings of flash-evoked potentials. In addition, microstimulation-evoked motor and sensory responses allow the internal capsule to be identified. The data collected using this technique are an important adjunct to selecting optimum sites to place electrocoagulation lesions for stereotactic posteroventral pallidotomy for refractory Parkinson's disease.

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Editorial

Functional neurosurgery and hemorrhage

Tejas Sankar and Andres M. Lozano

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Deep brain stimulation electrodes used for staged lesion within the basal ganglia: experimental studies for parameter validation

Laboratory investigation

Sylvie Raoul, Dominique Leduc, Thomas Vegas, Paul Sauleau, Andres M. Lozano, Marc Vérin, Philippe Damier, and Youenn Lajat

Object

Deep brain stimulation (DBS) has been shown to be an effective treatment for various types of movement disorders. High-frequency stimulation is applied to specific brain targets through an implanted quadripolar lead connected to a pulse generator. These leads can be used for creating lesions in the brain. The experimental study reported here was designed to examine the electrical parameters that could be used to create reproducible therapeutic lesions in the brain.

Methods

Egg whites were used to measure the relationship between the electrical parameters (current and voltage) applied through the DBS electrode and the size of coagulum. The authors measured current spread from the electrode contact used for lesioning to the adjacent contact. Similar studies were performed in the pallidum or the thalamus of human cadavers. Modeling of the lesion size was performed with simulation of current density and temperature. The ultrastructure of the electrodes after lesioning was verified by electron microscopy.

Results

Coagulation size increased with time but reached a plateau after 30 seconds. For a given set of electrical parameters, reproducibility of the size of lesions was high. Using constant voltage, lesions were larger in egg whites than in cadaveric brains with a mean length of 5 ± 0.6 mm in egg whites at 40 V, 125 mA, impedance 233 Ω; and 4.0 ± 0.8 mm in cadavers at 40 V, 38 mA, impedance 1333 Ω. Computer modeling indicated negligible current flow to the adjacent, unused electrodes. The electrodes showed no structural alterations on scanning electron microscopy after more than 200 lesions.

Conclusions

Results of this study demonstrate that DBS electrodes can be used to generate lesions reproducibly in the brain. The choice of lesioning parameters must take into account differences in impedance between the test medium (egg whites) and the human brain parenchyma.