Methods for microstimulation and recording of single neurons and evoked potentials in the human central nervous system

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✓ An apparatus and technique are described for microstimulation and recording of both slow wave and single neuron (single unit) activities during functional stereotaxic procedures. This method facilitates microstimulation and evoked potential and single unit analysis which, in combination, provide optimum definition of stereotaxic targets in the treatment of functional disorders of the human central nervous system.

Abstract

✓ An apparatus and technique are described for microstimulation and recording of both slow wave and single neuron (single unit) activities during functional stereotaxic procedures. This method facilitates microstimulation and evoked potential and single unit analysis which, in combination, provide optimum definition of stereotaxic targets in the treatment of functional disorders of the human central nervous system.

During stereotaxic surgery, knowledge of the physiological properties of fiber tracts and neurons, defined by stimulation and recording, is essential to confirm the actual location of targets whose approximate position has been determined by radiological imaging studies. Electrical stimulation of subcortical structures has usually been applied through bipolar electrodes,2,7,13,27,31 whereas cellular activity has been recorded through fine bipolar electrodes (impedance < 0.1 Mohm),3,7,10,26,27,32 low-impedance microelectrodes (0.1 to 1.0 Mohm),8,9,15,23,25,28 or high-impedance microelectrodes (> 2 Mohm).11,17,24 Recording the activity of single neurons (single units) provides physiological data of the highest resolution possible using extracellular techniques. However, these recordings have been reported to be more time-consuming than localization by either electrical stimulation or recording of multiple unit and field potential activity evoked by somatosensory stimulation.4,25 The necessary balance between speed and precision can best be achieved by using a single electrode for all modalities of physiological testing.

The high-impedance electrodes required to record single unit activity16 are particularly sensitive to noise, especially when they are long enough for human subcortical recording.25 Furthermore, stimulation through high-impedance electrodes produces high current density at the electrode tip which, by causing electrolysis and breakdown of insulation at the tip, interferes with subsequent recordings through the same microelectrode (FA Lenz, et al., unpublished data). For these reasons, recording and stimulation are often performed by using a single low-impedance electrode2,25 which is not capable of discriminating the activity of single units.

A microelectrode is described which has tougher insulation, relatively low impedance, and a fine tip, and which can be used repeatedly for stimulation and reliable recordings of both evoked potentials and single unit activity during stereotaxic operations. A simple method for on-line histogram analysis of single unit activity is also outlined.

Description of Microelectrode and Technique
Microelectrode

The microelectrode was made by electrolytically etching a platinum-iridium (70%–30%) wire, 200 µin diameter, to a tip of 3 to 4 µby passing current (12 V, 60 Hz) through the wire into a solution of sodium hydroxide (30%) and sodium cyanide (50%) using a graphite rod as the other electrode.33 The taper of the microelectrode was achieved during the etching procedure by attaching the wire eccentrically to the armature of an electric motor (6 rpm), oriented so that the wire entered the etching solution at an oblique angle. Thus, as the motor rotated, the distal part of the electrode was etched for longer than the proximal part during each pass through the solution, producing a uniform and reproducible taper. A platinum-iridium alloy was used for the microelectrode since it proved particularly resistant to electrolysis during microstimulation.

The electrode was then coated with solder glass under microscopic control,* leaving only the distal 5 to 10 µ of the tip exposed. At this point, the impedance of the electrode was 2 to 8 Mohms (1000-Hz signal). The distal 1 cm of this electrode was then sheared off and inserted into the end of a 20-cm length of No. 26 stainless steel tubing insulated with a Kapton polyimide sleeve. The junction of the microelectrode and stainless steel-Kapton tubing was secured with silver solder before being coated with a resin (Epoxylite), and baked at 100°C for 1 hour. Insulation consisting of glass, resin, and plastic was used because electrodes insulated exclusively with resin have been subject to fracture of the insulation during handling, and failure of insulation at the tip during stimulation. The latter effect dramatically lowered both the electrode impedance and the resolution of subsequent recordings.

Special measures were essential to protect the fine tip of the microelectrode during handling. The microelectrode was cut to an appropriate length, inserted into a thin-walled carrier tube, and secured with a set screw at the upper end. It was then fixed to a modified hydraulic microdrive§ which had been sterilized by immersion in a 2% glutaraldehyde solution. The microdrive incorporated a clamp, shield, and connectors for a high-impedance preamplifier which was inserted after the microdrive had been sterilized. Immediately prior to gas sterilization of the electrode in its carrier tube, the tip of the microelectrode was plated with platinum black to reduce its impedance to approximately 100 kohm. This was achieved by passing a 10-µA negative current through the electrode for 10 to 30 seconds with the tip immersed in a 5% platinic chloride solution. Lowering impedance by plating minimizes noise without sacrificing the high resolution of the microelectrode. We have recently employed a gold-plated glass-coated tungsten microelectrode with similar results.1,16 After use, the microelectrode, carrier tube, guide tube, and obturator were soaked in hydrogen peroxide (8% solution), rinsed, soaked in a 2% glutaraldehyde solution, rinsed again, and reassembled. The microelectrode was then plated and gas-sterilized.

Stereotaxic Technique

The stereotaxic frame coordinates of the anterior (AC) and posterior commissures (PC) were determined by high-resolution computerized tomography (CT) scanning using the scanner's own computer and a CT-compatible Leksell frame. A computer program14 then produced a set of sagittal brain diagrams with the same intercommissural distance as that of the patient by stretching or shrinking, as need be, the sagittal sections from the Schaltenbrand and Bailey Atlas.30 Figure 1 illustrates the map of the patient's thalamus (Fig. 1A, AC to PC distance 26.5 mm), and shows the microelectrode trajectory and the presumed location at which recordings (Fig. 1B and D) and microstimulation (Fig. 1E) were performed.

Fig. 1.
Fig. 1.

Microstimulation, single unit and evoked potential recording at a single site in the presumed ventrocaudal (Vc) nucleus (right side) of a patient with chronic pain. A: Map of the human thalamus in the parasagittal plane 15 mm lateral to the midline illustrating the position of the anterior commissure (AC)-posterior commissure (PC) line, a microelectrode trajectory oblique to the AC-PC line, and the presumed location (arrow) at which recordings (B and D) and microstimulation (E) were performed. Further details are given in the text. B: Oscilloscope trace (lower) showing a single unit recording at the presumed location indicated in A. The spike train shows a slowly adapting response to light touch applied at the receptive field illustrated in the figurine to the right of the trace. The approximate duration of somatosensory stimulation is indicated by the horizontal bars beneath the trace. The dots above the spike train indicate the occurrence of discriminated action potentials having the shape displayed at high sweep speed in the upper trace. Horizontal calibrations of the upper and lower traces are as marked. C: Photograph of the screen of an averager which has been used to construct a histogram of single neuron activity (upper trace) and average, rectified, inverted, wrist flexor electromyographic (EMG) activity (lower trace) related to five repetitions of the active movement of making a fist, cued by a flash of light occurring at the time indicated by the arrow. Horizontal calibration is as marked. D: Simultaneous recordings of evoked potentials at the right C4 location on the scalp (upper trace) and in the thalamus (at the arrow in A) (lower trace) resulting from stimulation of the left median nerve (6 mA). Each trace represents an average of 50 responses. The reference electrodes were located on the guide tube for thalamic recordings and on the right ear lobe for cortical recording. Calibration bars are as marked, with positive voltages down, negative up. The positive, downgoing wave occurring at approximately 15 msec is designated as the P15 wave. E: The black area shows the location of paresthesiae evoked by microstimulation in the thalamus at the site indicated by the arrow in A.

At operation, a thin-walled guide tube with obturator was stereotaxically directed toward the chosen target so that the tip was positioned 1 cm short of the target. The obturator was then replaced with the microelectrodecarrier tube-preamplifier assembly. The access burr hole and microelectrode trajectories were in the same parasagittal plane as the target, simplifying calculation of the electrode's location. Use of the guide tube, guide tube obturator, and microelectrode carrier tube was essential to protect the plated microelectrode tip during introduction into the brain. The use of a preamplifier fixed to the stereotaxic frame substantially reduced noise due to movement artifact.

The microelectrode signal was monitored by listening to an audio monitor and observing the spike train displayed on the oscilloscope screen. The activity of single units was identified by feeding the microelectrode signal into a window discriminator and displaying the shape of the discriminated action potential on an oscilloscope at high sweep speed with the aid of an analog delay-line circuit (see Fig. 1B). The constant shape of the action potential assured that all action potentials recorded at a particular site were being generated by a single neuron, which is the basic assumption of single unit analysis. The discriminator pulses were then fed into the audio monitor, allowing intraoperative analysis of single unit activity.

The activity of single units was subjected to visual and auditory examination for evidence of alteration of the firing pattern during voluntary movement, involuntary movement, and somatosensory stimulation. The lower trace in Fig. 1B shows the spike train of a cell responding to light touch applied to its receptive field on the contralateral index finger.19 The constant shape of the action potential, illustrated in the upper trace of Fig. 1B, confirmed that a single unit was being studied. Isolated single units of the type illustrated in this figure were easily recorded and held by means of the technique described. The microelectrode signal, electromyographic signals, and a descriptive voice channel were recorded on tape for postoperative off-line analysis.20–22

The activity of many cells was related to particular contralateral active movements. Since changes in firing rate were often difficult to recognize by listening to single unit activity,22 histograms of cellular activity were constructed by feeding the output of the discriminator into an averager used for recording evoked potentials in the operating room. Histograms generated in this way can only be interpreted reliably if the duration of the pulse from the discriminator to the averager equals the sampling interval of the averager and is shorter than the minimal interspike interval of the spike train. Figure 1C illustrates the histogram of the activity of a single unit and the average contralateral wrist flexor electromyogram related to the active movement of making a fist. The averager was triggered at a fixed interval before the flash from a strobe light which occurred at the time indicated by the arrow in Fig. 1C and cued the patient to perform the required active movement. The result of this analysis is a peristimulus time-histogram which provides an accurate on-line visual picture of cellular activity related to active movement.

The microelectrode output could be filtered to record both evoked potentials (0 to 250 Hz) and single unit responses (300 to 10,000 Hz) to peripheral nerve stimulation. Figure 1D illustrates the evoked potentials recorded from a surface electrode located at C4 on the scalp (upper trace) and from the thalamus (lower trace) at the presumed site indicated by the arrow in Fig. 1A.

Along each trajectory, recordings were made immediately after extrusion of the electrode into the brain, in order to confirm the integrity of the microelectrode. The microelectrode was then connected in the microstimulation mode (see below) and threshold microstimulation was carried out at 0.5-mm intervals and at thresholds of up to 120 µA as the electrode was advanced. When contralateral sensory effect, movement, or alteration of involuntary movement occurred with a threshold of 40 µA or less, single unit activity recording was begun. Recording and stimulation were then alternated at sites where neurons were identified, while potentials evoked by peripheral nerve stimulation were recorded only at selected sites. The stimulation applied through the microelectrode was monopolar at microampere current levels, a technique termed “microstimulation.”6,18,29 Microstimulation was accomplished by disconnecting the microelectrode from the preamplifier and connecting it to the negative output of a constant-current, optically isolated stimulator. The positive lead was connected to the guide tube. Manually changing between stimulation and recording modes eliminated capacitative losses inherent in the use of a switch. Current was monitored by measuring the voltage drop across a 1-kohm resistor connected in series between the positive output of the isolator and the connection to the guide tube. This voltage drop was amplified by an optically isolated direct-current preamplifier and displayed on an oscilloscope.

Responses related to microstimulation included sensations, movement, and modulation of tremor or other dyskinesia. A 0.5- to 2.0-second stimulus train (consisting of 0.1- to 0.3-msec negative 120-µA pulses, delivered at 300 Hz) was used for routine stimulation when searching for stimulus-related responses. When sensations or motor responses were evoked by stimulation, the threshold current was determined; this was typically less than 10 µA for sensations evoked by stimulation in the ventrocaudal nucleus. For example, microstimulation at 8 µA in the presumed site displayed in Fig. 1A produced paresthesiae in the distribution illustrated in the figurine shown in Fig. 1E. Stimulation at frequencies in the range of 60 to 500 Hz were about equally effective in generating responses, while thresholds were higher at frequencies outside this range. In a few cases short stimulus trains (< 0.5 sec) were delivered and were found to produce identical sensations, although single pulses never did.

Clinical Results

These techniques have now been applied during localization of subcortical targets in 38 patients suffering from chronic pain, Parkinson's disease, dystonia, and cerebellar and essential tremor using a single electrode in up to 10 patients without failure. The stereotaxic target was identified physiologically in all but two of these patients, one with a previous lesion of the target (the thalamic nucleus ventralis intermedius),12 and the other with the Dejerine-Roussy syndrome and infarction of the target (the nucleus ventralis caudalis).12 None of the patients operated on suffered any complication related to the microelectrode exploration, suggesting that the risks associated with thalamic exploration may be similar whether a microelectrode or a larger bipolar electrode is used.4,25

Discussion

Microstimulation has been widely used to explore the central nervous system of laboratory animals since the demonstration that its use minimized the spread of current and stimulation effects.6,18,29 The physiological effect of the stimulation is better localized to the anatomical site defined by the electrode position, resulting in a more precise anatomical-physiological correlation than is the case with stimulation using larger electrodes. For example, microstimulation at 25 µA induces stimulation effects over distances of less than 100 to 300 µ, depending upon whether cell somata or axons are being stimulated.29 In explorations of the human central nervous system during stereotaxic surgery, stimulation has usually been applied through bipolar macroelectrodes13,31 at current levels of 0.1 to 1.5 mA or through fine bipolar electrodes at current levels of less than 0.5 mA.2,7,27 While such stimulation increases the likelihood of evoking a response at a given site, it spreads stimulation effects over distances of up to 2 mm.7,31 Since the entire lemniscal thalamic homunculus is represented within a cube of a side of approximately 5 mm,19 the advantage of microstimulation over macrostimulation for localization is considerable.

The combination of both recording and stimulation can be used to facilitate thalamic explorations. Microstimulation may evoke sensations at sites where no somatosensory units are recorded, such as in sensory tracts afferent from, efferent to, or adjacent to the sensory nucleus. It may also evoke vestibular responses where related neurons cannot be documented since there is no practical method of activating them in the operating room. Finally, responses to stimulation at low threshold often identify sites where single units can be recorded. Thus, stimulation can be used to select optimal sites for recording, a technique which is both more accurate and slower than stimulation.

Single unit recording, slow wave recording, and stimulation results at one site can be compared to provide information regarding normal and abnormal neuronal function. When strong responses to sensory stimulation are obtained, the single unit response to a single presentation of the stimulus can be recorded for study (Fig. 1B). Weaker responses to sensory stimulation can be defined by averaging single unit activity to produce peristimulus time-histograms (Fig. 1C) or by averaging slow wave activity to produce evoked potentials (Fig. 1D). Evoked potentials at different sites can be compared with one another (Fig. 1D), with single unit activity (Fig. 1B), or with peristimulus time-histograms of single unit activity (Fig. 1C). Such correlations allow analysis of cell types involved in the generation of evoked potentials. For example, the fact that the P15 wave recorded from the scalp has lower amplitude but the same time course as the P15 wave recorded in the thalamus (Fig. 1D) suggests that the generator for this potential may be located in the thalamus.5 Finally, because of the ability to communicate with the patient, microstimulation and single unit recording at the same site (Fig. 1) can provide a unique perspective on the functional significance of neuronal activity in the central nervous system.

Acknowledgments

We thank M. Teofilo, A. Suran, and H. H. Nguyen-Huu for technical assistance.

References

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    Ainsworth ADostrovsky JOMerrill EGet al: An improved method for insulating tungsten micro-electrodes with glass. J Physiol (Lond) 269:4P5P1977 (Abstract)J Physiol (Lond) 269:

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    Albe-Fessard D: Electrophysiological methods for the identification of thalamic nuclei. Z Neurol 205:15281973Albe-Fessard D: Electrophysiological methods for the identification of thalamic nuclei. Z Neurol 205:

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    Albe-Fessard DArfel GGuiot G: Activités électriques charactéristiques de quelques structures cérébrales chez l'homme. Ann Chir 17:118512141963Ann Chir 17:

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    Albe-Fessard DArfel GGuiot Get al: Thalamic unit activity in man. Electroencephalogr Clin Neurophysiol Suppl 25:1321431967Electroencephalogr Clin Neurophysiol Suppl 25:

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    Albe-Fessard DTasker RRYamashiro Ket al: Comparison in man of short latency averaged evoked potentials recorded in thalamic and scalp hand zones of representation. Electroencephalogr Clin Neurophysiol 65:4054151986Electroencephalogr Clin Neurophysiol 65:

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    Asanuma HSakata H: Functional organization of a cortical efferent system examined with focal depth stimulation in cats. J Neurophysiol 30:35541967J Neurophysiol 30:

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    Bertrand CMartinez SNHardy Jet al: Stereotactic surgery for parkinsonism: microelectrode recording, stimulation, and oriented sections with a leucotomeKrayenbühl HMaspes PESweet WH (eds): Progress in Neurological Surgery5. Basel: S Karger197379112

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    Donaldson IML: The properties of some human thalamus units. Some new observations and a critical review of the localization of thalamic nuclei. Brain 96:4194401973Donaldson IML: The properties of some human thalamus units. Some new observations and a critical review of the localization of thalamic nuclei. Brain 96:

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    Gaze RMGillingham FJKalyanaraman Set al: Microelectrode recordings from the human thalamus. Brain 87:6917061964Brain 87:

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    Hardy TLBertrand GThompson CJ: The position and organization of motor fibers in the internal capsule found during stereotactic surgery. Appl Neurophysiol 42:1601701979Appl Neurophysiol 42:

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    Ohye C: Depth microelectrode studiesSchaltenbrand GWalker AE (eds): Stuttgart: Georg Thieme1982372389

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    Ohye CFukamachi ANarabayashi H: Spontaneous and evoked activity of sensory neurons and their organization in the human thalamus. Z Neurol 203:2192341972Z Neurol 203:

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    Ohye CNarabayashi H: Physiological study of presumed ventralis intermedius neurons in the human thalamus. J Neurosurg 50:2902971979J Neurosurg 50:

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    Wolbarsht MLMacNichol EF JrWagner HG: Glass insulated platinum microelectrode. Science 132:130913101960Science 132:

Micro-forge manufactured by Technical Products International, St. Louis, Missouri.

Tubing manufactured by Vita Needle Corp., Needham, Massachusetts; Kapton poly-imide sleeve manufactured by Niemad Industries, New York, New York.

Epoxylite manufactured by Epoxylite of Canada Ltd., Fort Erie, Ontario, Canada.

Microdrive manufactured by David Kopf Instruments, Tujunga, California.

This research was supported by the PSI Foundation, Toronto, Ontario, Canada, the Parkinson's Foundation of Canada, and the Medical Research Council (Canada).

Article Information

Dr. Lenz was a Fellow of the Medical Research Council (Canada) and a Schering Scholar of the American College of Surgeons.

Address reprint requests to: Frederick A. Lenz, M.D., c/o Division of Neurosurgery, 14-216 Eaton North Wing, Toronto General Hospital, 200 Elizabeth Street, Toronto, Ontario M5G 2C4, Canada.

© AANS, except where prohibited by US copyright law.

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Figures

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    Microstimulation, single unit and evoked potential recording at a single site in the presumed ventrocaudal (Vc) nucleus (right side) of a patient with chronic pain. A: Map of the human thalamus in the parasagittal plane 15 mm lateral to the midline illustrating the position of the anterior commissure (AC)-posterior commissure (PC) line, a microelectrode trajectory oblique to the AC-PC line, and the presumed location (arrow) at which recordings (B and D) and microstimulation (E) were performed. Further details are given in the text. B: Oscilloscope trace (lower) showing a single unit recording at the presumed location indicated in A. The spike train shows a slowly adapting response to light touch applied at the receptive field illustrated in the figurine to the right of the trace. The approximate duration of somatosensory stimulation is indicated by the horizontal bars beneath the trace. The dots above the spike train indicate the occurrence of discriminated action potentials having the shape displayed at high sweep speed in the upper trace. Horizontal calibrations of the upper and lower traces are as marked. C: Photograph of the screen of an averager which has been used to construct a histogram of single neuron activity (upper trace) and average, rectified, inverted, wrist flexor electromyographic (EMG) activity (lower trace) related to five repetitions of the active movement of making a fist, cued by a flash of light occurring at the time indicated by the arrow. Horizontal calibration is as marked. D: Simultaneous recordings of evoked potentials at the right C4 location on the scalp (upper trace) and in the thalamus (at the arrow in A) (lower trace) resulting from stimulation of the left median nerve (6 mA). Each trace represents an average of 50 responses. The reference electrodes were located on the guide tube for thalamic recordings and on the right ear lobe for cortical recording. Calibration bars are as marked, with positive voltages down, negative up. The positive, downgoing wave occurring at approximately 15 msec is designated as the P15 wave. E: The black area shows the location of paresthesiae evoked by microstimulation in the thalamus at the site indicated by the arrow in A.

References

1.

Ainsworth ADostrovsky JOMerrill EGet al: An improved method for insulating tungsten micro-electrodes with glass. J Physiol (Lond) 269:4P5P1977 (Abstract)J Physiol (Lond) 269:

2.

Albe-Fessard D: Electrophysiological methods for the identification of thalamic nuclei. Z Neurol 205:15281973Albe-Fessard D: Electrophysiological methods for the identification of thalamic nuclei. Z Neurol 205:

3.

Albe-Fessard DArfel GGuiot G: Activités électriques charactéristiques de quelques structures cérébrales chez l'homme. Ann Chir 17:118512141963Ann Chir 17:

4.

Albe-Fessard DArfel GGuiot Get al: Thalamic unit activity in man. Electroencephalogr Clin Neurophysiol Suppl 25:1321431967Electroencephalogr Clin Neurophysiol Suppl 25:

5.

Albe-Fessard DTasker RRYamashiro Ket al: Comparison in man of short latency averaged evoked potentials recorded in thalamic and scalp hand zones of representation. Electroencephalogr Clin Neurophysiol 65:4054151986Electroencephalogr Clin Neurophysiol 65:

6.

Asanuma HSakata H: Functional organization of a cortical efferent system examined with focal depth stimulation in cats. J Neurophysiol 30:35541967J Neurophysiol 30:

7.

Bertrand CMartinez SNHardy Jet al: Stereotactic surgery for parkinsonism: microelectrode recording, stimulation, and oriented sections with a leucotomeKrayenbühl HMaspes PESweet WH (eds): Progress in Neurological Surgery5. Basel: S Karger197379112

8.

Donaldson IML: The properties of some human thalamus units. Some new observations and a critical review of the localization of thalamic nuclei. Brain 96:4194401973Donaldson IML: The properties of some human thalamus units. Some new observations and a critical review of the localization of thalamic nuclei. Brain 96:

9.

Gaze RMGillingham FJKalyanaraman Set al: Microelectrode recordings from the human thalamus. Brain 87:6917061964Brain 87:

10.

Guiot GHardy JAlbe-Fessard D: [Precise delimitation of the sub-cortical structures and identification of thalamic nuclei in man by stereotaxic electrophysiology.] Neurochirurgia (Stuttg) 5:1181962 (Fre)Neurochirurgia (Stuttg) 5:

11.

Hardy TLBertrand GThompson CJ: The position and organization of motor fibers in the internal capsule found during stereotactic surgery. Appl Neurophysiol 42:1601701979Appl Neurophysiol 42:

12.

Hassler R: Architectonic organization of the thalamic nucleiSchaltenbrand GWalker AE (eds): Stuttgart: Georg Thieme1982140180

13.

Hassler RMundinger FRiechert T: Stereotaxis in Parkinson Syndrome. Berlin: Springer-Verlag1979Stereotaxis in Parkinson Syndrome.

14.

Hawrylyshyn PRowe IHTasker RRet al: A computer system for stereotaxic neurosurgery. Comput Biol Med 6:87971976Comput Biol Med 6:

15.

Hongell AWallin GHagbarth KE: Unit activity connected with movement initiation and arousal situations recorded from the ventrolateral nucleus of the human thalamus. Acta Neurol Scand 49:6816981973Acta Neurol Scand 49:

16.

Hubel DH: Tungsten microelectrode for recording from single units. Science 125:5495501957Hubel DH: Tungsten microelectrode for recording from single units. Science 125:

17.

Jasper HHBertrand G: Thalamic units involved in somatic sensation and voluntary and involuntary movements in manPurpura DPYahr MD (eds): The Thalamus. New York: Columbia University Press1966365390The Thalamus.

18.

Kwan HCMacKay WAMurphy JTet al: Spatial organization of precentral cortex in awake primates. II. Motor outputs. J Neurophysiol 41:110211311978J Neurophysiol 41:

19.

Lenz FADostrovsky JOTasker RRet al: Single unit analysis of the ventral nuclear group of human thalamus: somatosensory responses. J Neurophysiol 59 (In press1988)J Neurophysiol 59

20.

Lenz FATasker RRKwan HCet al: Cross-correlation analysis of thalamic neurons and EMG activity in parkinsonian tremor. Appl Neurophysiol 48:3053081985Appl Neurophysiol 48:

21.

Lenz FATasker RRKwan HCet al: Single unit analysis of the ventral tier of lateral thalamic nuclei in patients with parkinsonian tremor of human thalamus. Soc Neurosci Abstr 11:11641985 (Abstract)Soc Neurosci Abstr 11:

22.

Lenz FATasker RRKwan HCet al: Techniques for the analysis of spike trains in the human central nervous system. Acta Neurochir Suppl 33:57611984Acta Neurochir Suppl 33:

23.

Li CLvan Buren JM: Micro-electrode recordings in the brain of man with particular reference to epilepsy and dyskinesiaSomjen GG (ed): Neurophysiology Studied in Man. Amsterdam: Excerpta Medica19724963Neurophysiology Studied in Man.

24.

Martin-Rodriguez JGBuño W JrGarcía-Austt E: Human pulvinar units, spontaneous activity and sensorymotor influences. Electroencephalogr Clin Neurophysiol 54:3883981982Electroencephalogr Clin Neurophysiol 54:

25.

Ohye C: Depth microelectrode studiesSchaltenbrand GWalker AE (eds): Stuttgart: Georg Thieme1982372389

26.

Ohye CFukamachi ANarabayashi H: Spontaneous and evoked activity of sensory neurons and their organization in the human thalamus. Z Neurol 203:2192341972Z Neurol 203:

27.

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