Short latency somatosensory evoked potentials to peroneal nerve stimulation in normal Japanese children

Short Latency Somatosensory Evoked Potentials to Peroneal Nerve Stimulation In Normal Japanese Children Toshiaki Hashimoto, MD, Masanobu Tayama, MD, Kuniaki Fukuda, MD, Shoichi Endo, MD and Masuhide Miyao, MD Short latency somatosensory evoked potentials (SSEP) were elicited by stimulation of the peroneal nerve in 68 normal children of 39 weeks to 15 years old. In all subjects, three positive potentials (PI, P2 and P3) and one negative potential (Nl) were consistently recorded. A further positive potential (P4) after Nl was not always observed. There was no change of wave form with development. PI, P2, P3 and Nl might be generated in subcortical structures; caudal cervical spine, brainstem, thalamus and thalamocortical pathway, respectively. The latency of each peak per one meter body length decreased with age until 5 or6 years of age. Moreover, the latency between peaks per one meter body length also decreased with age until 5 to 6 years of age. These findings are consistent with the development of SSEP on median nerve stimulation and with the developmental phenomenon of spinal conduction velocity, and might be related to the increase in the diameter and the progressive myelination of nerve fibers. Hashimoto T, Tayama M, Fukuda K, Endo S, Miyao M. Short latency somatosensory evoked potentials to peroneal nerve stimulation in normal Japanese children Brain Dev 1985; 7: 4 70-6

The short latency somatosensory evoked potentials (SSEP) following median nerve stimulation were studied by many workers [1-5] and their clinical usefulness has also been reported in children [6, 7]. Although in adults there are a small number of reports on far-field subcortical potentials elicited by stimulation of nerves from the lower extremities [8-14], many uncertainties remain about SSEP on

lower limb stimulation. There is no consensus on the features and labels of the early components in lower limb SSEP. Moreover, in children there are only a few reports on SSEP on nerve stimulation in the lower limbs. The aim of this investigation was to clarify the features and developmental changes of SSEP on stimulation of nerves in the lower limbs. Subjects and Methods

From the Department of Pediatrics, Tokushima University School of Medicine, Tokushima. Received for publication: October 26, 1984. Accepted for publication: June 5, 1985.

Key words: Short latency somatosensory evoked potential, peroneal nerve, development, topography. Correspondence address: Dr. Toshiaki Hashimoto, Department of Pediatrics, Tokushima University School of Medicine, Kuramoto-cho 3, Tokushima 770, Japan.

Sixty-eight normal children between 39 weeks and 15 years of age (42 males and 26 females) were studied. Informed consent was obtained from parents after the nature of the procedure had been fully explained. The studied population was drawn from both in- and out-patients, who had some illness, but without neurological problems. In order to reduce myogenic contamination, all subjects except for newborns were sedated with triclofos (50-100 mg/kg) or

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nitrazepam (2-5 mg). In the newborn SSEP was recorded during natural sleep. Square wave pulses of 200 llsec duration were generated by a stimulator. The stimulator was triggered by the R peak of each ECG. A train of stimuli consisting of 2-5 pulses with the time interval of 100 ms was delivered starting 30-100 msec after the R peak of each ECG. Somatosensory stimuli were delivered via disc electrodes filled with gel placed over the peroneal nerve with the anode 2-3 cm distal to the cathode at the knee joint. The current was adjusted to produce nonpainful and minimal dorsiflexion of the foot. Electrodes were attached to the skin over the lumbar (L3), thoracic (Th12 and Th6) and cervical locations CCv7), and the right mastoid process (RMP). Scalp electrodes were positioned according to the international 10-20 system. Electrodes over the shoulders and Cv7 were used as non cephalic references. Electrodes were filled with conductive jelly and their impedance

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Fig 2 SSEP on right peroneal nerve stimulation in a 6-yr-9-mo-old boy. Pi in Cv7-Cz recording is con· sistent with the second small upward deflection (*) in Th6-Cz. P2 latency is similar to the potential in RMP-Cv7.

was maintained at less than 3,000 n. Spinal evoked potentials were obtained by bipolar chain arrangement. The frequency response of the amplifiers was between 50 and 1,000 Hz (-3dB). Analysis times of 40.96 msec were used, and 5003,000 responses were summated. Signal was summated with a data processor (AT AC 450, Nihon Kohden Co.). Data were recorded with an XY recorder. Two or three summated responses were superimposed to ensure consistency. Results 1. The Wave Fonn of Spinal and Scalp SSEP Spinal SSEP showed tri- or quadriphasic potentials with poorly defined initial positive phases. Their amplitude was greatest in Th12-Th6 and smallest in Th6-Cv7. The latency of the response increased progressively from the lumbar to the cervical recording location. A typical scalp SSEP recorded from Cv7-Cz consisted of four upward deflections (PI, P2, P3 and P4) and one prominent downward deflection (Nl)

Hashimoto et al: SSEP on peroneal nerve stimulation

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after P3. P4 was a large upward deflection after N l. Each potential (P 1, P2, P3 and N 1) recorded at Fpz-Cz was lowered by in phase cancellation from Fpz. P4 was well defined. PI was equivalent with the initial upward deflection in Cv7-RMP (Fig 1). In Th6-Cz recording of another case, five upward deflections were observed. The second small upward deflection was consistent with PI in the Cv7-Cz recording, and the third to fifth upward deflections were consistent with P2, P3 and P4, respectively. P2 was coincident with the upward deflection in RMP-Cv7 (Fig 2). The latency of each wave was not different between 50-1,000 Hz and 160-1,000 Hz filters. The right shoulder-Cz recording showed four upward deflections and one downward one. There was no difference in wave components or latencies between Cv7-Cz and the right shoulder-Cz (Fig 3).

2. Topographic Study In a study on the scalp topography of SSEP following right peroneal nerve stimulation, four peaks (PI, P2, P3 and NI) were found to be present with a widespread distribution over the scalp in both sagittal and coronal planes. P4 appeared in Cz, C4 and T6. The amplitude of P4 was maximum at Cz. The latency of P4 at C4 and T6 was delayed. At the other record-

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472 Brain & Development, Vol 7, No 5, 1985

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Discussion

3. SSEP at Different Ages Figure 5 shows the averaged responses on the right peroneal nerve stimulation of normal subjects of various ages. In all subjects, four upward deflections (PI, P2, P3 and P4) and one downward deflection (NI) between P3 and P4 were recorded. PI was an initial potential and was followed by P2. P3 was an upward deflection preceding a downward deflection, Nl. P4 was a large upward deflection after Nl. There was no change of wave pattern with development.

Our recording showed four upward deflections and one downward deflection which we labeled PI, P2, P3, Nl and P4. With regards to the polarity of waves, it might be thought that there was a contradiction between our previous paper [15] and present paper. In our study both electrodes (Cv7 and Cz) are active. Our present results shows that the first upward deflection is picked up as a positivity from grid II (Cz) as well as a negativity from grid I (Cv7). That is to say, the first upward deflection is a far field potential recorded from Cz, which was probably originated in Cv7, and 4. Latencies of Each Wave Component equal to near field potential from Cv7. Thus the first upward deflection was labeled as PI The peak latency value of PI, P2, P3, and NI per one meter body length decreased rapidly' (positivity). The results also indicate that at from newborn to 5-6 years, and then remained Cv7-Cz, PI, P2, P3, NI and P4 are picked up constant. This change with development was respectively as positivity-positivity-positivitymost marked in N 1, and less so in the order negativity-positivity from Cz. These potentials are recorded best from Cv7-Cz. Lueders et al ofP3, P2 and PI (Fig 6). [10] described that upward deflections should 5. Latencies between Peaks per One Meter be labeled as N (negativity) if they are pikced Body Length up from grid I and P (positivity) if they are Values of PI-P3, PI-NI and P2-P3 latency per picked up from grid II. one meter body length decreased rapidly from In scalp-noncephalic reference leads, PI, P2, newborn to 5-6 years, and then remained P3 and Nl were widespread in their scalp disconstant. The value of PI-P2 latency per one tribution and similar in latency and amplitude meter body length decreased slightly from at all scalp recording sites. These potentials newborn to 5-6 years, and then remained undergo cancellation in the Fpz-Cz recording. constant (Fig 7). Thus our observations indicate the four com41 w, M

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Hashimoto et al: SSEP on peroneal nerve stimulation 473

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Fig 7 Developmental change in the interpeak latency per one meter body length. The fitted curve was as follows: PI-P2/H. y = 0.0002X2 - 0.0455x +3. 7598 (SD = 0.87); P1-P3/H. y = 0.0008X2 - 0.1753x+ 14.1459 (SD =2.62); P2-P3/H. y = 0.0006X20.1300x + 10.3938 (SD =2.14); PI-N1/H. y = 0.0009X2 - 0.2146x + 18.2797 (SD =3.47).

ponents mentioned above (PI, P2, P3 and Nl) are far-field potentials arising from subcortical structures. Our PI appears equivalent to the PI of Vas et al [8] and PIA of Rossini et al [9]. The latency of PI was similar to that of the evoked potential recorded in Cv7-RMP. PI appeared after a fast negative peak in Th6-Cz recording and was also picked up in the right shoulder-Cz recording. These findings support the hypo-

thesis that PI is recorded as a positivity from Cz and generated by the volume conducted volley in the lower cervical spine. P2 is probably the same as the P1B of Rossini et al [9]. It might also be equivalent to the P25 of Kakigi et al [11] , P27 of Yamada et al [12], P28 of Seyal et al [13] and P26 of Desmedt et al [14], although comparison with their data is difficult as they stimulated the posterior tibial nerve. The latency between PI

474 Brain & Development. Vol 7. No 5.1985

and P2 is about 2 ms after 7 years of age when the conduction velocity reaches to the adult level. The distance at 7 years of age is smaller than that in adults measured from Cv7 to dorsal column nuclei [16). Assuming that the conduction velocity of the spinal cord is about 64 m/ sec [15), it is unlikely that P2 arises from the dorsal column nuclei. It is more likely that P2 results from more rostral structures, possibly the caudal brainstem (pons). Our P3 is probably the same as the P2B of Rossini et al [9) and P2 of Vas et al [8). It might be equivalent to the P28 of Kakigi et al [II), P31 of Seyal et al [13) and P31 of Desmedt et al [14) recorded by posterior tibial nerve stimulation. Seyal et al [13) concluded that P31 resulted from the thalamus as the peak of wave generated at the nucleus ventralis posterolateralis exactly coincided with the scalp recorded P31. In the light of this finding, our P3 is likely to have a thalamic origin. Our P4 is equivalent to the P3 of Vas et al (8) , P3 of Rossini et al [9] , P36 of Kakigi et al [11), P38 of Seyal et al [13) and P32 of Lueders et al [10). P4 has the highest amplitude around the vertex , which suggests that it is generated from the cortical primary somatosensory area. Our N 1 is equivalent to the N30 of Lueders et al [10], N31 of Kakigi et al [11] , N34 of Seyal et al [13) and N34 of Desmedt et al [14]. Nl may be generated by the thalamocortical radiation. We found a completely identical SSEP wave pattern from the newborn to the teen-age group, although the amplitude of SSEP in the newborn was smaller than that of the teen-age group. However, Rossini et al [17] reported that they did not find a response morphology completely the same as the adult one. This may be due to differences of the recording method. Difficulties of their SSEP recording seem to be mainly due to the contamination by the R wave of the ECG . In order to solve this problem, we use the R wave of the ECG to trigger the stimulator [11] . In long and short latency somatosensory evoked potentials, there is a positive relationship between the peak latency and body length and/or arm length [6, 18]. In order to cancel out the effect of body length on the peak latency, we calculated the value of each peak

latency and each interpeak latency per one meter body length. These values changed with development, which was comparable to the SSEP changes on the median nerve stimulation [6). This developmental function is similar to the ones seen in the spinal cord conduction velocity [15, 19] and the maturation of brain weight. The decrease in the peak latency and interpeak latency per one meter body length is probably related to the increase in the diameter of nerve fibers [20] , as well as to the progressive myelination of nerve fibers [21].

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peak latencies of far-field components recorded from neck and righ t or left scalp and earlobes. Electroencephalogr Clin Neurophysiol 1980;50: 382-90 . Rossini PM , Pallotta R, Gambi D. Developmental anatomophysiological correlates of intermediate and short latency SEPs and their clinical perspectives in pediatric neurology. In: Chiarenza GA, Papakostopoulos D, eds. Pediatric medicine. Amsterdam·Oxford·Princeton: Excerpta Medica, 1982 :221-57 . Shagass C, Schwartz M. Age, personality and somatosensory cerebral evoked response s. Science 1965; 148 : 1359-61. Cracco RQ. Spinal evoked response : peripheral nerve stimulation in man. Electroencephalogr Clin Neurophysiol 1973 ;35: 3 79-86. Rushton WAH. A theory of the effects of fibre size in medullated nerve. J Physiol 1951;115: 101-22. Sanders FK. Whitteridge D. Conduction velocity and myelin thickness in regenerating nerve fibers. J PhysioI1946;105:152-74.