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The effect of change of stimulation frequencies on latencies, peak amplitudes and central conduction time in median somatosensory evoked potentials of normal subjects

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Corresponding author: Hande Turker, M.D.

Ondokuzmayıs University, School of Medicine, Department of Neurology 55139 Kurupelit Samsun / Turkey

E- mail: drhande@ttnet.net.tr Tel –Fax: + 90- 03624354900

Marmara Medical Journal 2004;17(1);14-21

ORIGINAL RESEARCH

THE EFFECT OF CHANGE OF STIMULATION FREQUENCIES ON LATENCIES, PEAK

AMPLITUDES AND CENTRAL CONDUCTION TIME IN MEDIAN SOMATOSENSORY

EVOKED POTENTIALS OF NORMAL SUBJECTS

Hande Türker

1

, Önder Us

2

, Gülseren Akyüz

3

, Tülin Tanrıdağ

2 1

Department of Neurology, School of Medicine, Ondokuzmayıs University, Samsun, Turkey 2Department of Neurology, School of Medicine, Marmara University, Istanbul, Turkey 3Department of Physical Medicine and Rehabilitation, School of Medicine, Marmara University, Istanbul, Turkey

ABSTRACT

Objective: The nature of somatosensory evoked potential (SEP) studies of normal subjects is obviously much different from the

patients. In this study our aim was to find out the effects of the change of stimulus frequencies on absolute latencies, amplitudes and central conduction time in median SEPs of normal subjects.

Methods: Normal values of somatosensory evoked potentials were obtained from 30 healthy subjects (14 women and 16 men).

Nerve conduction studies of each of the subjects were performed before the SEP study in order to eliminate the subclinical peripheral nerve pathologies.

Results: We found that the values of N11 peak, N13 peak, N20 peak, N11-13 complex onset and N20 onset latencies and N11-13

complex amplitudes of normal subjects were affected by changes of stimulus frequencies. As the stimulation frequency increased, the latencies showed statistically significant increases while the amplitude of N11-13 complex showed a statistically very significant decrease. On the other hand, the values of peak and onset central conduction times and the amplitude of N20 did not show any statistically significant changes from each other as the stimulation frequencies increased.

Conclusion: It is our belief that the studies on stimulus frequency changes in SEPs may play a role as a guide for SEP studies with

different patient groups and have an impact in the physiological dynamics of SEPs.

Keywords: Somatosensory evoked potentials, Median SEP, Central conduction time

NORMAL KİŞİLERDE MEDYAN SOMATOSENSORİYEL UYANDIRILMIŞ

POTANSİYELLERİN KAYDI SIRASINDA UYARIM FREKANSI DEĞİŞİKLİKLERİNİN

LATANS, AMPLİTÜD VE SANTRAL İLETİM ZAMANINA ETKİLERİ

ÖZET

Amaç: Normal kişilerde medyan somatosensoriyel uyandırılmış potansiyellerin (SUP) kaydı sırasında uyarım frekansı

değişikliklerinin, mutlak latanslar, amplitüd ve santral iletim zamanına etkilerinin araştırılması.

Metod: Medyan somatosensoriyel uyandırılmış potansiyel kayıtları 14’ü kadın, 16’sı erkek; 30 sağlıklı bireyde yapılmıştır.

Subklinik periferik sinir patolojilerini ekarte etmek için SUP kaydı öncesinde her normal bireye sinir iletim testleri yapılmıştır. Uyarım frekansı 2, 4, 6 ve 9 Hz olacak şekilde değiştirilmek suretiyle mutlak latans, amplitüd ve santral iletim zamanı parametrelerindeki değişiklikler saptanmıştır.

Bulgular: N11 pik, N13 pik, N20 pik ve N11-13 kompleksi başlangıç latansları ile N20 başlangıç latansı ve N11-13

kompleksinin amplitüdü uyarım frekansı değişikliklerinden etkilenmişlerdir. Uyarım frekansı artışı ile latanslarda istatistiksel olarak anlamlı bir gecikme izlenirken; N11-13 kompleksinin amplitüdü, istatistiksel olarak anlamlı şekilde düşüş göstermiştir. Ancak pik ve başlangıç santral iletim zamanları ile N20 amplitüdünde istatistiksel olarak anlamlı değişimler izlenmemiştir.

Sonuç: Normallerde somatosensoriyel uyandırılmış potansiyellerin kaydında uyarım frekansı değişikliklerine ilişkin

çalışmalar, farklı hasta guruplarındaki çalışmalar için bir rehber niteliği taşırken, SUP’un fizyolojik dinamiklerinin anlaşılmasında etkili olabilir.

Anahtar kelimeler: Somatosensoriyel uyandırılmış potansiyeller, Medyan SUP, Santral iletim zamanı. INTRODUCTION

Although the effects of frequency changes on somatosensory evoked potential (SEP) responses have been studied since the 1970’s, the results show many differences in various study groups. It

may be very important to find out the differences of effects of stimulation frequencies in normal subjects and patient groups in electrophysiological diagnosis. The studies on SEP recordings in normal subjects make a good basis for SEP

(2)

studies for patient groups because the increase of stimulation frequencies affect absolute latencies, amplitudes and central conduction time in different ways in various groups of patients. Studies on stimulus frequency changes in SEPs in the normal group may help explaining the physiological dynamics of SEPs .

METHODS

Normal values of somatosensory evoked potentials were obtained from 30 healthy subjects (14 women and 16 men). Their mean age was 33.46± 12.9 years (range from 12 to 56). Before

the study, the procedure was explained thoroughly to the subjects and each of them signed an informed consent. The study protocol was also approved by the ethic committee. Nerve conduction studies of each of the subjects were performed before the SEP study in order to eliminate the subclinical peripheral nerve pathologies.

Method of median SEP study

In this study, we used Medelec/Teca Sapphire II F04 / 00. Active and reference points are shown in Table I.

Table I: Active and reference points of median SEP study

Channel Active Reference

1 ( Erb Channel ) Ipsilateral Erb Contralateral Erb

2 ( Cervical channel ) Spinal process of fifth

cervical vertebra

Supraglottal region

3 ( Scalp channel ) Five centimetres behind the

point which is 7

centimetres lateral of CZ

Fz

The stimulation was made upon the median nerve on the wrist with surface electrodes and the ground was put on the ipsilateral arm. Silver electrodes were used for recordings. High and low frequency filters were 20Hz and 2kHz respectively, sweep speed was 50msec/div, sensitivity was 20microvolts. Stimulation frequency was 2/sec in four of the subjects, in 6 of them it was 2/sec, 4/sec, 6/sec and in 20 of them it was 2/sec, 4/sec, 6/sec and 9/sec. This difference occurred because ten of the subjects could not tolerate higher stimulation frequencies. Stimulus duration was 0.1 msec and the intensity stimulus was adjusted according to the minimal contraction in thenar muscles. The recordings of 750-1024 stimuli were superposed. Besides the absolute latencies of N9 obtained from the Erb channel, N11-N13 complex obtained from the spinal channel and N20 obtained from the scalp channel, the amplitudes of these potentials and the interpeak latencies which are listed as follows were taken together to form the statistical results : 1) N13-N20 interpeak latency (peak central conduction time )

2) The difference between onset latencies of N11-N13 complex and N20 onset ( onset central conduction time)

SPSS (Statistical package for social sciences) for Windows 7.0 and 10 programs were used while obtaining the results and besides mean values and standard deviations, student’s test was performed.

RESULTS

The parameters, which were studied statistically, were as follows:

1) N9 peak latency 2) N11 peak latency 3) N13 peak latency 4) N20 peak latency

5) N11-N13 complex onset latency 6) N20 onset latency

7) Peak central conduction time 8) Onset central conduction time 9) N11-13 complex amplitude (peak)

10)N20 amplitude (peak)Mean values and standard deviations of every parameter were calculated and every parameter in different stimulation frequencies (2/sec, 4/sec, 6/sec, 9/sec) was compared statistically to the others.

The statistical comparison of N9 peak latencies obtained with different stimulation frequencies in the normal group did not show any statistical differences (p>0.05).

(3)

Hande Turker, et al.

The Effect of Change of Stimulation Frequencies on Latencies, Peak Amplitudes and Central Conduction Time in Median Somatosensory Evoked Potentials of Normal Subjects

Table II: The statistical comparison of N9 peak latencies obtained with different stimulation frequencies in

the normal group

N9 Peak (msec) 1.frequency Mean±2.SD 2.frequency Mean±2.SD t+ p N9 Peak (2/s – 4/s) 9.09±1.38 9.12±1.40 -1.85 0.07 N9 Peak (2/s – 6/s) 9.09±1.38 9.12±1.48 -0.807 0.429 N9 Peak (2/s – 9/s) 8.93±1.02 9.06±1.18 -1.99 0.066 N9 Peak (4/s – 6/s) 9.12±1.40 9.12±1.48 0.071 0.944 N9 Peak (4/s – 9/s) 8.97±1.00 9.06±1.18 -1.55 0.143 N9 Peak (6/s – 9/s) 8.98±1.14 9.06±1.18 -1.77 0.09

+ t test of the difference between two

Table III: The statistical comparison of N11 peak latencies obtained with different stimulation frequencies

in the normal group

N11 Peak (msec) 1.frequency Mean±2.SD 2.frequency Mean±2.SD t+ p N11 Peak (2/s – 4/s) (n=14) 10.75±1.72 10.85±1.78 -0.870 0.400 N11 Peak (2/s – 6/s) (n=15) 10.79±1.70 10.90±1.58 -2.694 0.02* N11 Peak (2/s – 9/s) (n=12) 10.46±1.22 10.80±1.70 -2.153 0.054 N11 Peak (4/s – 6/s) (n=12) 10.90±1.86 10.92±1.66 -0.214 0.834 N11 Peak (4/s – 9/s) (n=9) 10.62±1.18 10.61±1.24 0.063 0.952 N11 Peak (6/s – 9/s) (n=11) 10.62±1.26 10.77±1.76 -0.997 0.342 * p<0.05

+ t test of the difference between two

In the statistical comparison of the values of N11 peak latency, values obtained with 6/sec stimulation frequency were significantly higher

than the values obtained with 2/sec stimulation frequency (p< 0.05).

Table IV: The statistical comparison of N13 peak latencies obtained with different stimulation frequencies

in the normal group

N13 Peak (msec) 1.frequency

Mean±2.SD 2.frequency Mean±2.SD

t+ p N13 Peak (2/s –4/s) (n=21) 12.24±2.36 12.41±2.22 -1.445 0.164 N13 Peak (2/s – 6/s) (n=21) 12.24±2.36 12.44±2.18 -1.932 0.068 N13 Peak (2/s – 9/s) (n=15) 11.93±1.66 12.47±1.68 -3.811 0.002** N13 Peak (4/s – 6/s) (n=21) 12.41±2.22 12.44±2.18 -0.346 0.733 N13 Peak (4/s – 9/s) (n=15) 12.13±1.7 12.47±1.70 -2.494 0.026* N13 Peak (6/s – 9/s) (n=15) 12.22±1.76 12.47±1.68 -1.894 0.079 **p<0.01

*p<0.05

(4)

In the statistical comparison of the values of N13 peak latency, values obtained with 9/sec stimulation frequency were significantly higher than the values obtained with 2/sec stimulation

frequency (p< 0.01) which were also significantly higher than the values obtained with 4/sec stimulation frequency (p< 0.05).

Table V: The statistical comparison of N20 peak latencies obtained with different stimulation

frequencies in the normal group

N20 Peak (msec) 1.frequency

Mean±2.SD Mean2.frequency ±2. SD

t+ p N20 Peak (2/s – 4/s) (n=21) 18.03±2.20 18.30±2.26 -3.783 0.001** N20 Peak (2/s – 6/s) (n=21) 18.03±2.20 18.34±2.10 -5.376 0.000** N20 Peak (2/s – 9/s) (n=15) 17.72±1.46 18.10±1.80 -4.647 0.000** N20 Peak (4/s – 6/s) (n=21) 18.30±2.26 18.34±2.10 -0.434 0.669 N20 Peak (4/s – 9/s) (n=15) 18.05±1.66 18.10±1.80 -0.430 0.674 N20 Peak (6/s – 9/s) (n=15) 18.08±1.48 18.10±1.80 -0.226 0.824 **p<0. 01 *p<0. 05

+ t test of the difference between two

In the statistical comparison of the values of N20 peak latency, values obtained with 4/sec 6/sec and 9/sec stimulation frequencies were significantly

higher than the values obtained with 2/sec stimulation frequency (p<0.01).

Table VI: The statistical comparison of N11-13 complex onset latencies obtained with different stimulation

frequencies in the normal group

N11-13 Onset (msec) 1.frequency

Mean±2.SD 2.frequency Mean±2.SD

t+ p N11-13 onset (2/s – 4/s) (n=21) 2.51±1.28 2.59±1.24 -1.020 0.320 N11-13 onset (2/s – 6/s) (n=21) 2.51±1.30 2.54±1.40 -2.797 0.011* N11-13 onset (2/s – 9/s) (n=15) 2.33±0.74 2.55±1.14 -2.219 0.044* N11-13 onset (4/s – 6/s) (n=21) 2.59±1.24 2.54±1.40 -1.309 0.205 N11-13 onset (4/s – 9/s) (n=15) 2.51±1.32 2.55±1.14 -1.419 0.178 N11-13 onset (6/s – 9/s) (n=15) 2.46±1.08 2.55±1.14 -0.742 0.471 *p<0.05

+ t test of the difference between two

In the statistical comparison of the values of N11-13 onset latency, values obtained with 6/sec and 9/sec stimulation frequencies were significantly

higher than the values obtained with 2/sec stimulation frequency (p< 0.05).

(5)

Hande Turker, et al.

The Effect of Change of Stimulation Frequencies on Latencies, Peak Amplitudes and Central Conduction Time in Median Somatosensory Evoked Potentials of Normal Subjects

Table VII: The statistical comparison of N20 onset latencies obtained with different stimulation frequencies

in the normal group

N20 Onset (msec) 1.frequency Mean±2.SD 2.frequency Mean±2.SD t+ p N20 Onset (2/s – 4/s) (n=21) 15.28±2.22 15.48±2.12 -2.204+ 0.039* N20 Onset (2/s – 6/s) (n=21) 15.28±2.22 15.65±2.40 -2.977+ 0.007** N20 Onset(2/s – 9/s) (n=15) 14.88±1.38 15.26±1.12 -4.055+ 0.001** N20 Onset (4/s – 6/s) (n=21) 15.48±2.12 15.65±2.40 -1.345+ 0.194 N20 Onset (4/s – 9/s) (n=15) 15.11±0.98 15.26±1.12 -1.609+ 0.130 N20 Onset (6/s – 9/s) (n=15) 15.32±1.30 15.26±1.12 0.880+ 0.394 **p<0. 01 *p<0. 05

+ t test of the difference between two

In the statistical comparison of the values of N20 onset latency, values obtained with 6/sec and 9/sec stimulation frequencies were significantly higher than the values obtained with 2/sec

stimulation frequency (p<0.01) while 4/sec values were significantly higher than the values obtained with 2/sec stimulation frequency (p<0.05).

Table VIII: The statistical comparison of Peak CCT obtained with different stimulation frequencies in the

normal group Peak CCT (msec) 1.frequency Mean±2.SD 2.frequency Mean±2.SD t+ p Peak CCT (2/s-4/s) (n=21) 5.78±0.92 5.89±1.18 -0.829 0.417 Peak CCT (2/s-6/s) (n=21) 5.78±0.92 5.89±0.92 -1.210 0.240 Peak CCT (2/s-9/s) (n=15) 5.77±1.00 5.58±1.26 1.259 0.229 Peak CCT (4/s-6/s) (n=21) 5.89±1.18 5.89±0.92 -0.037 0.971 Peak CCT (4/s-9/s) (n=15) 5.92±1.12 5.59±1.26 2.204 0.05 Peak CCT (6/s-9/s) (n=15) 5.86±0.86 5.58±1.26 1.766 0.09

+ t test of the difference between two

The statistical comparison of peak CCT obtained

(6)

Table IX: The statistical comparison of onset CCT obtained with different stimulation frequencies in the

normal group

Onset CCT (msec) 1.frequency

Mean±2.SD 2.frequency Mean±2.SD

t+ p Onset CCT (2/s-4/s) (n=21) 5.53±1.28 5.65±1.38 -1.050 0.306 Onset CCT (2/s-6/s) (n=21) 5.53±1.28 5.65±1.96 -0.659 0.517 Onset CCT (2/s-9/s) (n=15) 5.31±1.06 5.34±1.34 -0.154 0.880 Onset CCT (4/s-6/s) (n=21) 5.65±1.38 5.65±1.98 0.044 0.965 Onset CCT (4/s-9/s) (n=15) 5.48±1.24 5.34±1.34 0.690 0.501 Onset CCT (6/s-9/s) (n=15) 5.56±1.22 5.34±1.34 1.009 0.330

+ t test of the difference between two

The statistical comparison of onset CCT obtained with different stimulation frequencies in the

normal group did not show any statistical differences (p >0.05).

Table X: The statistical comparison of N11-13 amplitude obtained with different stimulation frequencies in

the normal group

N11-13 amplitude(µv) Mean ± 2SD Frequency 2-4 p Frequency 2-6 p Frequency 2-9 p Frequency 4-6 p Frequency 4-9 p Frequency 6-9 p Frequency 2 1.69 ± 1.78 Frequency 4 1.55 ± 2.22 Frequency 6 1.20 ± 1.04 Frequency 9 1.44 ± 1.62 0.365 0.007** 0.307 0.266 0.315 0.378 ** p<0. 01

In the statistical comparison of the values of N11-13 amplitude, values obtained with 6/sec frequencies were significantly lower than the

values obtained with 2/sec stimulation frequency (p<0.01) .

Table XI: The statistical comparison of N20 amplitude obtained with different stimulation frequencies in the

normal group N20 amplitude(µv) Mean ± 2SD Frequency 2-4 p Frequency 2-6 p Frequency 2-9 p Frequency 4-6 p Frequency 4-9 p Frequency 6-9 p Frequency 2 1.49 ± 1.12 Frequency 4 1.58 ± 1.52 Frequency 6 1.37 ± 1.20 Frequency 9 1.32 ± 0.94 0.793 0.231 0.195 0.143 0.125 0.300

(7)

Hande Turker, et al.

The Effect of Change of Stimulation Frequencies on Latencies, Peak Amplitudes and Central Conduction Time in Median Somatosensory Evoked Potentials of Normal Subjects

The statistical comparison of N20 amplitude obtained with different stimulation frequencies in the normal group did not show any statistical differences (p>0.05) .

DISCUSSION

In this study our aim was to find out the effects of the change of stimulus frequencies on absolute latencies, peak amplitudes and central conduction times in median SEPs of normal subjects in our laboratory. We found that the peak latencies of N11, N13, N20 and onset latencies of N11-13 complex and N20 as well as N11-13 complex amplitudes of normal subjects were affected by changes of stimulus frequencies. As the stimulation frequency increased, the latencies showed statistically significant increases while the amplitude of N11-13 complex showed a statistically very significant decrease. On the other hand, the values of peak and onset central conduction times and the amplitude of N20 did not show any significant changes from each other as the stimulation frequencies increased.

The effects of frequency changes on SEP responses have been studied since 1970’s. In 1976 Pimmel et al. studied the effects of stimulation characteristics and level of anaesthesia on SEP responses in Rhesus monkeys and found that although the latencies did not show any changes, the amplitudes were affected by stimulus intensity, duration and stimulus frequency 1 .

Manzano et al. reported in one of their studies that, increasing the stimulation frequency did not change the peak central conduction time in normals whereas absolute peak and onset latencies increased 2. Somatosensory evoked potentials were obtained by electrical stimulation of the median nerve in 10 normal subjects at 3 and 30 Hz. At the higher rate of stimulation, a reduction was observed in amplitudes and prolongation of latencies of the N9, N/P13 and N20 components as well as the increase of the interpeak latency N9-N/P13. A significant increase between the onsets of the N11 and N20 components was also seen; however, no significant increase of the N/P13-N20 interpeak latency was observed. Their analysis suggested that an important reason for this last finding was related to the fact that in some cases different fast frequency components (FFC) determined the N20 peak in the different situations 2.

Delberghe et al. and Huttunen et al. also studied the effects of stimulation frequency changes on spinal and cortical potentials of SEP 3,4. They

assessed the influence of the stimulus frequency on short-latency SEPs recorded over the parietal and frontal scalp of 26 subjects to median nerve stimulation and 16 subjects to digital nerve stimulation. When the stimulus frequency was increased from 1.6Hz to 5.7Hz, the amplitude of N13 potential decreased as the stimulation frequency increased while there was no change in the amplitude of N20 3 .We also found the same results in our study. Huttunen et al. reported the influence of varying stimulus repetition rate from 0.5 to 5 Hz on cortical SEPs up to 60-msec latency after right median nerve stimulation, separately analyzed at frontal (F3), central (C3) and parietal (P3) electrodes 4. The amplitudes of early frontal P20 and N25, central P14 and N18, and parietal N20 did not change with stimulation rate. Later deflections were significantly modified when their amplitudes were determined with respect to the baseline 4. Larrea et al. found a significant decrease in the amplitude of N20 but they did not report any changes of absolute latencies 5. They performed topographic mapping of somatosensory responses to median nerve stimulation delivered at 2, 5 and 10Hz. Parietal N20 was significantly attenuated in 10Hz somatosensory evoked potentials (SEPs), while central P22 diminished between 2 and 5 Hz, remaining stable thereafter. The single component most affected by increasing stimulus rate was N30, which abated by more than 50% in 10 Hz SEPs, as compared with basal responses. They concluded that there was no single "optimal" stimulation rate for SEP recordings and that a combination of different frequencies of stimulation should enhance the diagnostic utility of this technique5. Abbruzzese et al. 6 studied the effects of changing the stimulus presentation rate on early parietal (N20-P25) and frontal (P22-N30) somatosensory potentials, evoked by median nerve stimulation in 15 normal subjects. Stimuli were presented at 0.1, 0.4, 1.0, 4.0 and 10/sec. Only minor latency changes, mainly for the frontal P22 component, were observed when the stimulus rate was increased up to 10/sec: while the frontal P22-N30 complex was more rapidly and severely reduced in amplitude than the parietal N20-P25 complex. In their opinion, the differential effects of stimulus presentation rate on early frontal and parietal SEPs supported the hypothesis of separate neural generators and suggested that the choice of the stimulation frequency may be critical for the interpretation of diagnostic SEP studies 6. Pelosi et al. 7.found that the increase in stimulation frequency did not

(8)

affect the spinal responses but it caused a decrease of amplitude in cortical responses of SEP. The effect of variation in the stimulus frequency on spinal and cortical somatosensory evoked potentials to common peroneal nerve stimulation at the knee (CPN-K) and tibial nerve stimulation at the ankle (TN-A) were studied in 11 healthy subjects. Six stimulus frequencies, 0.7, 1.5, 3.0, 5.0, 7.0 and 10.0 Hz, were used in random order. With increasing stimulus rate spinal responses remained unchanged. By contrast, early cortical responses became significantly reduced in amplitude or undetectable for stimulation frequencies above 3.0 Hz for the CPN-K and 5.0 Hz for the TN-A. In 2 subjects the configuration and the latency of CPN-K SSEPs were affected by stimulus frequency. Similar changes were not observed in TN-A SSEPs 7.

In our study we observed changes of amplitude and latency in different parameters with different stimulation frequencies. However, we did not find any change in peak and onset central conduction times. This last finding was not assessed in the studies mentioned above. It is important because it can be used with different patient groups where central conduction time is expected to rise. The reason for differences of effects of stimulation frequencies on different SEP parameters of normal subjects was not understood very clearly and is still debated. We believe that studies on SEP recordings in normal subjects make a good basis for SEP studies for patient groups. We think that results may be different for various groups of patients and thus we can use this point for various groups of patients where we expect central conduction time changes. Increasing stimulus frequency may be practical in routine SEP studies for obtaining reliable results in various patient groups suspected of having central conduction time changes. As far as other studies are concerned, it is quite clear that the amount of increase in stimulus frequency affects the results

and this is most significant in the changes of the amplitudes. We believe this is what leads to different results in different studies. It is also our belief that the studies on stimulus frequency changes in SEPs in the normal group may be of great help in understanding the physiological dynamics of SEPs.

REFERENCES

1. Pimmel RL, Hung N, Bresnahan J. Effects of

anesthesia level and stimulus characteristics on the amplitude and latency of the somatosensory evoked response in monkeys. J Neurosci Res 1976; 2:385-293.

2. Manzano GM, De Navarro JM, Nobrega JA. Short

latency median nerve somatosensory evoked potential (SEP): Increase in stimulation frequency from 3 to 30 Hz. Electroenceph Clin Neurophysiol 1995; 96:229-235.

3. Delberghe X, Mavroudakis N, Zegers de Beyl D,

Bruriko E. The effect of stimulus frequency on post and precentral short latency somatosensory evoked potentials (SEP). Electroenceph Clin Neurophysiol 1990; 77:86-92.

4. Huttunen J, Homberg V. Influence of stimulus

repetition rate on cortical somatosensory potentials evoked by median nerve stimulation:Implication for generation mechanisms. J Neurol Sci 1991; 105:37-43.

5. Larrea GL, Bastuji H, Mauguiere F. Unmasking of

cortical SEP components by changes in stimulus rate : A topographic study. Electroenceph Clin Neurophysiol 1992; 84:71-83.

6. Abbruzzese G, Dall'Agata D, Morena M. Selective

effects of repetition rate on frontal and parietal somatosensory evoked potentials (SEPs). Electroenceph Clin Neurophysiol Suppl 1990; 41:145-148.

7. Pelosi L, Balbi P, Caruso G. The effect of stimulus

frequency on spinal and scalp somatosensory evoked potentials to stimulation of nerves in the lower limb. Electroenceph Clin Neurophysiol 1990; 41(Suppl.):149-152.

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