Dissociation between upper and lower neck N13 potentials following paired median nerve stimuli

Electroencephalography and clinical Neurophysiology 104 (1997) 68–73

Dissociation between upper and lower neck N13 potentials following paired median nerve stimuli Atsushi Araki, Thoru Yamada*, Takashi Ito, Nobuo Urushibara, Ryutaro Kohira, Shih-Pin Hsu, Malcolm Yeh Division of Clinical Electrophysiology, Department of Neurology, University of Iowa, College of Medicine, Iowa City, IA 52242, USA Accepted for publication: 12 August 1996

Abstract Cervical N13 potential in response to the median nerve stimulation can be recorded either from upper (Cv2) or lower (Cv6) neck with almost equal amplitudes and latencies. It has long been debated whether they represent the same or different generator sources. Using a conditioning-test paired stimuli paradigm, we examined the differences of recovery function of Cv2- and Cv6-N13, anterior neck (AN)P13, and scalp recorded P13/P14 in 6 healthy subjects. All cervical electrodes were referenced to the non-cephalic site. Scalp response was recorded with linked ear reference. The inter-stimulus intervals ranged from 4 to 20 ms with 2 ms increments. Throughout 4 to 18 ms ISI, Cv6-N13, AN-P13 and scalp P13/P14 were suppressed, whereas Cv2-N13 was facilitated. All but scalp P13/P14 returned close to the control at 20 ms ISI. The findings indicate that Cv2-N13, Cv6-N13 and scalp P13/P14 are independent each other and arise from different generator sources. The suppression of Cv6-N13 is consistent with a postsynaptic nature of this potential and may indeed be mediated through dorsal horn interneurons creating a current field orientation in the posterior-anterior direction. The facilitation of Cv2N13 suggests that this is a presynaptic potential and may travel through the dorsal column with vertical orientation. The longer period of suppression of scalp P13/P14 suggests it to be of polysynaptic origin and to arise at least rostral to the cuneate nucleus.  1997 Elsevier Science Ireland Ltd. All rights reserved Keywords: Recovery function; Cervical N13; Somatosensory evoked potential; Cuneate nucleus; Dorsal column

1. Introduction The negative potential with latency of 13 ms (N13) recorded from the posterior portion of the neck is an obligate potential of the median nerve SEP. It has been reported that the cervical N13 originates from dorsal horn interneurons yielding a horizontally oriented dipole with positivity at the anterior neck and negativity at the posterior neck (Desmedt and Cheron, 1980; Desmedt and Cheron, 1981; Mauguie`re et al., 1983; Emerson et al., 1984; Jeanmonod et al., 1989). If cervical N13 from median nerve stimulation is generated segmentally, this should have a maximum amplitude at C5 to C6 spine level. Contrary to this expectation, cervical N13 can be recorded either from upper neck (Cv2) or lower neck (Cv6) with almost equal amplitude and latencies (Desmedt and * Corresponding author. Tel.: +1 319 3568770; fax: +1 319 3564505.

0168-5597/97/$17.00  1997 Elsevier Science Ireland Ltd. All rights reserved PII S0921-884X(96)9604 5-2

Cheron, 1981; Lu¨ders et al., 1983; Mauguie`re et al., 1983; Emerson et al., 1984; Sonoo et al., 1990). In fact, high cervical N13 (Cv2-N13) and low cervical N13 (Cv6N13) have been used arbitarily in clinical application, and the recording location depends on simply the laboratory’s preference. Recently Sonoo et al. (1990) claimed that Cv2-N13 and Cv6-N13 have distinct origins based on the observation of clinical cases. Kaji and Sumner (1987) also found that cervical N13 has two components, N13a and N13b, and that the N13a vector is directed horizontally while the N13b vector is directed vertically. Assessing the ulnar nerve SEP which has a segmentally lower entrance to the cervical cord than the median nerve, Zannette et al. (1995) proposed separate generators for Cv2-N13 and Cv6-N13 potentials. Using conditioning-test paradigm in this study, we evaluated the recovery functions of Cv2-N13 and Cv6-N13 to

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A. Araki et al. / Electroencephalography and clinical Neurophysiology 104 (1997) 68–73

confirm the existence of separate generators for these two components. The recovery function of scalp P13/P14 potential was also examined for comparison with cervical potentials. 2. Materials and methods The subjects included 6 healthy males, aged 29-40, with a mean age of 35 years; each with provided informed consent. The subject lay supine on a bed and was instructed to relax with eyes closed. One series of test required 8–10 h for one subject and the subject was allowed to have several rest periods for 5–10 min in between testing sessions. A pair of stimulating electrodes (silver-silver chloride cups) filled with EKG gel were attached to the skin with collodion. The median nerve was stimulated at the left wrist with the cathode 2 cm proximal to the anode. Consistent stimulus delivery to the median nerve was assured by carefully positioning the arm and stimulating electrodes. The stimulus was a square-wave pulse of 0.2 ms duration delivered via a stimulus isolation unit. Each test consisted of a single pulse stimulus and a paired pulse stimulus with a repetition rate of 4.3 Hz. The inter-stimulus intervals (ISIs) for the paired stimuli ranged from 4 to 20 ms with 2 ms increments. The stimulus pulse intensity for single and paired stimuli was the same and was 2.5–3 times sensory threshold. A block of 800 averaged responses to single and paired stimuli each was recorded alternately. This was repeated 4–5 times until a total of 3200–4000 averaged responses for each condition was obtained. The recording electrodes were silver-silver chloride cups filled with EKG gel attached to the skin with collodion. Electrode impedance was less than 5 kQ. The recording scalp electrode was C4′ (2 cm posterior to C4) in accordance to the 10–20 international system and referenced to linked ear electrodes (A1 + A2). The cervical potentials were recorded from the cervical spine at Cv2, Cv3, Cv4, Cv5, Cv6 in addition to the anterior neck (AN) while using a reference at the right shoulder. The AN electrode was placed on the midline at the midpoint of the rostral-caudal length of the neck. Erb’s potential was also monitored. The SEPs were recorded with a Nicolet pathfinder I. The input was amplified 20 000 times, with a filter band pass of 15–1500 Hz (−6dB). To analyze the test response affected by the preceding conditioning stimulus, the test response was extracted by subtracting the control response to single (S1) stimulation from the response to the paired (S1 + S2) stimuli. We then compared the subtracted wave form (test response = (S1 + S2) − S1) with the S1 only (control) response. The amplitude of N13 was measured from the onset (positive peak) to the negative peak. The amplitude of P13 recorded from anterior neck was measured from the

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preceding negative peak. A distinction of scalp recorded P13 and P14 potentials was not always possible especially in derived test responses. The amplitudes of P13 and P14 peaks were then measured as a complex and measured from the onset of positive deflection to the maximum positive peak. The amplitude of the test response was expressed as a percent of the control response. The Wilcoxon rank-sign test was used for statistical analysis. 3. Results 3.1. Recovery function of cervical N13 N13 amplitude of the test response at Cv6 was slightly but consistently smaller than the control response at ISIs of 4–18 ms. In contrast, the Cv2-N13 amplitude of the test response was consistently larger than the control response. The control and test responses were almost the same at the Cv4 spine level. Fig. 1 shows example of the above features at 6 ms in one subject and the grand mean responses from 6 subjects. The shaded areas indicate the difference between test and control responses. The vertically lined shaded areas indicate facilitation of the test response at Cv2 and Cv3, whereas dark shaded areas indicate suppression of the test response at Cv5 and Cv6. Although the amplitude recovery showed considerable individual variation with a non-linear, zig-zag pattern from ISIs of 4–20 ms, there was a clear distinction between

Fig. 1. The left colmn of tracings show representative example of cervical N13 at different cervical levels at an ISI of 6 ms in one subject. Superimposition of control and test responses shows the difference; the Cv6-N13 amplitude is depressed and the Cv2-N13 amplitude is facilitated when compared to the control response. (The dark shadow represents suppression and the vertical shadow represents facilitation.) There is no significant difference between control and test responses at Cv3, Cv4 or Cv5 spinal levels. Also note the suppression of scalp P13/P14.

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trol amplitude, though not all subjects recovered completely at this ISI. In contrast to facilitation of CV2N13 and suppression of CV6-N16, Erb’s potential fully recovered at 4 ms ISI but in some subjects showed minimal facilitation (less than 5% at most) at ISI of 4–18 ms. 3.2. Recovery function of the anterior neck AN-N13 potential AN-P13 potential also showed significant amplitude suppression at ISIs 4, 8, 10, 12, 14 and 20 ms ranging from 80 to 90% of the control (Fig. 3; Table 1; Fig. 1) but showed greater inconsistency across the individuals when compared to the Cv6-N13 amplitude suppression. Although mean amplitude from 6 subjects was about 80% of the control at ISIs of 6 and 16 ms, these did not reach statistical significance due to greater individual variations (Fig. 3). 3.3. Recovery function of scalp recorded P13/P14

Fig. 2. The recovery functions of all subjects. The facilitation of the Cv2 amplitude response ranged from 104 to 125% and suppression at the Cv6 potential ranged from 66 to 98%.

Cv2-N13 and Cv6-N13. Facilitation for Cv2-N13 ranged from 104 to 125% of control amplitude in contrast to amplitude suppression for Cv6-N13 which ranged from 66 to 98% (Fig. 2). Table 1 shows mean amplitude of control and test responses, and percentage of test response relative to the control at each ISI. The mean test response recovery functions were statistically significant for amplitude facilitation of Cv2-N13 and amplitude suppression of Cv6-N13 as compared to the control at ISIs between 4 and 18 ms (Fig. 3). At 20 ms ISI the mean test response amplitude of both Cv2-N13 and Cv6-N13 approached the con-

Scalp recorded P13/P14 potentials showed significant amplitude suppression throughout all ISIs and remained suppressed at ISI of 20 ms (Fig. 3; Table 1; Fig. 1). The degree of suppression was more than was noted for Cv6N13 or AN-P13 ranging from 60 to 80% of the control. 4. Discussion A number of investigators have studied the recovery functions of SEPs by using the conditioning-test paired stimulus paradigm on the median nerve (Allison, 1962; Shagass and Schwartz, 1964; Luders et al., 1983; MeyerHardting et al., 1983; Iragui, 1984; Greenwood and Goff, 1987; Emori et al., 1991). The recovery function of cervical N13 was studied by Iragui (1984), who observed the attenuation of cervical N13 lasting for 8 ms after the preceding conditioning stimulus. This recovery cycle was

Table 1 Recovery functions (mean ± S.D.) for CV2-N13, CV6-N13 and scalp P13-14 (n = 6) ISI (ms)

CV2-N13 Control (mV) Test (mV) % Recovery CV6-N13 Control (mV) Test (mV) % Recovery Scalp P13-14 Control (mV) Test (mV) % Recovery

4

6

8

10

12

14

16

18

20

1.04 ± 0.27 1.07 ± 0.32 109 ± 6

1 ± 0.28 1.18 ± 0.36 114 ± 4

1.04 ± 0.39 1.06 ± 0.28 108 ± 12

1.01 ± 0.24 1.11 ± 0.28 110 ± 11

1.08 ± 0.39 1.13 ± 0.34 108 ± 11

0.91 ± 0.34 0.98 ± 0.31 111 ± 9

0.84 ± 0.29 1.07 ± 0.27 116 ± 10

1.04 ± 0.29 1.16 ± 0.27 110 ± 9

1.26 ± 0.38 1.21 ± 0.41 99 ± 6

1.1 ± 0.32 0.88 ± 0.28 80 ± 7

1.02 ± 0.32 0.91 ± 0.26 90 ± 9

0.96 ± 0.26 0.83 ± 0.27 84 ± 10

1.03 ± 0.4 0.88 ± 0.22 84 ± 6

1.07 ± 0.31 0.86 ± 0.39 81 ± 8

0.94 ± 0.39 0.77 ± 0.37 82 ± 14

0.89 ± 0.35 0.80 ± 0.3 92 ± 14

1.03 ± 0.3 0.95 ± 0.29 92 ± 4

1.04 ± 0.33 0.95 ± 0.31 7±8

0.76 ± 0.11 1.41 ± 0.38 58 ± 22

0.93 ± 0.34 1.48 ± 0.47 64 ± 17

0.93 ± 0.23 1.39 ± 0.36 68 ± 13

0.99 ± 0.33 1.4 ± 0.43 73 ± 17

1.02 ± 0.26 1.64 ± 0.38 64 ± 17

0.82 ± 0.16 1.36 ± 0.38 64 ± 12

0.94 ± 0.24 1.45 ± 0.34 65 ± 16

1.1 ± 0.34 1.48 ± 0.47 79 ± 15

1.33 ± 0.37 1.7 ± 0.52 78 ± 12

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Fig. 3. The mean amplitude recovery functions (6 subjects) of Cv2-N13, Cv6-N13, AN-P13 and scalp P13/P14. Cv6-N13 and AN-P13 showed significant suppression (from 4 to 18 ms ISI) while Cv2-N13 showed facilitation when compared to the control. The scalp P13/P14 suppression was greater than Cv6-N13 or AN-P13.

consistent with a postsynaptic origin for the N13 potential. He recorded N13 at both the Cv2 and Cv6 spinal levels but no special attention was paid to the difference of recording sites. Because the facilitation at Cv2 and suppression at Cv6 observed in our study were relatively subtle, it required ‘cleaner’ response with greater number of averaging than usual to assess the difference. Desmedt and Cheron (1981) found that a prevertebral P13 recorded from an esophageal electrode had a phase reversal relationship with N13 recorded from a lower posterior neck electrode. They interpreted this N13-P13 relationship to represent a horizontally oriented dipole originating from a postsynaptic potential of the dorsal horn interneurons. Later Desmedt and Huy (1984) found that the prevertebral P13 can also be recorded from the surface of the anterior neck region. Our study also showed a phase reversal relationship between AN-P13 and Cv6N13, and both showed suppression when preceded by a conditioning stimulus. Both suppressions persisted between 4 and 18 ms ISI, though the degree of suppression and recovery function were not necessarily parallel nor did the suppression progress linearly from 4 to 18 ms ISI. One possible explanation for this is the measurement error due to a relatively poor signal to noise ratio for a small amplitude potential. To compensate, we used 3–4 times the number of averages than conventionally used for the

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SEP recording. Another inaccuracy may be compounded by the overlapping influence of opposite effects between facilitated Cv2-N13 and depressed Cv6-N13. The facilitation or suppression was cancelled at the Cv3 or Cv4 spinal level. It is, therefore, possible that the suppression or facilitation may be greater than actually measured. Despite these potential errors, the suppression of AN-P13 and Cv6-N13 suggests that they are generated postsynaptically and supports the notion that they are mediated through dorsal horn interneurons with a posterior-anterior transverse orientation (Desmedt and Cheron, 1981; Jeanmonod et al., 1989; Kaji and Sumner, 1990). In contrast to suppression of AN-P13 and Cv6-N13, Cv2-N13 amplitude was facilitated. This suggests separate generators for Cv6-N13 and Cv2-N13 despite the fact that they have almost the same latency and amplitude. In patients having lesions at the high cervical cord, Sonoo et al. (1990) observed dissociated changes between upper and lower neck N13; the absence of upper cervical N13 in association with normal lower cervical N13 in these patients lead them to propose the upper cervical N13 to be the postsynaptic potential of the cuneate nucleus. Several authors reported the negative wave at the dorsal medulla recorded intraoperatively in human subjects (Lesser et al., 1981; Suzuki and Mayanagi, 1984; Urasaki et al., 1984; Yasue et al., 1985; Møller et al., 1986; Jacobson and Tew, 1988). Of these investigators, Suzuki and Mayanagi (1984), and Urasaki et al. (1984) interpreted it as the postsynaptic activity of cuneate nucleus, while others thought it to be presynaptic activity of the dorsal column. Recently, Zannette et al. (1995) demonstrated a longer latency for the rostrally (Cv2) recorded N13 compared to the caudally (Cv6) recorded N13 when the ulnar nerve was stimulated. This latency dissociation seen in ulnar but absent in median nerve stimulation was interpreted to be due to a longer distance between the root entry zone and the cuneate nucleus for the ulnar nerve than for median nerve. They have proposed that rostral and caudal cervical N13 have separate generators and that rostral N13 reflects the presynaptic activity of dorsal column entering the cuneate nucleus. Emerson et al. (1984) also have found that dorsal column volley increases its latency as it ascends the cervical spine and matches with Cv2-N13. If Cv2-N13 represent postsynaptic activity, it would have been expected to show suppression with a conditioning-test stimulus paradigm. The facilitation of Cv2-N13 supports that this is of presynaptic origin and may have similar characteristics with peripheral nerve in which ’supernormality’ occurs at ISI of 5–15 ms (Gilliatt et al., 1963). Degree of facilitation was, however, greater in Cv2-N13 than peripheral nerve facilitation, which may vary depending on the stimulus intensity. The precise origin of the scalp recorded P13/P14 complex is still unclear. Most authors claimed that the generator of P13/P14 is located in the caudal brainstem (Desmedt and Cheron, 1980; Mauguie`re et al., 1983; Hashimoto,

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1984; Suzuki and Mayanagi, 1984; Mauguie`re and Ibanez, 1985; Yamada et al., 1986; Jacobson and Tew, 1988). Others suggested that it originates from presynaptic activity of dorsal column terminations in the cunate nucleus (Lesser et al., 1981; Lu¨ders et al., 1983; Møller et al., 1986; Morioka et al., 1991). In the present study, we observed suppression of P13/P14 which persisted for ISIs longer than 20 ms, implying that they are of postsynaptic origin. Zannette et al. (1995) suggested that P13/ P14 complex may receive a contribution from the generator at the rostral cervical N13. Our findings are not consistent with their view since recovery functions between rostral cervical N13 (Cv2-N13) and scalp P13/P14 were opposite. It is thus conceivable that scalp recorded P13/ P14 potentials reflect postsynaptic activity at or after the cuneate nucleus. Although P13 and P14 may have separate origins (Delestre et al., 1986; Mavroudakis et al., 1993), our present data was not sufficient to delineate the separate functions for P13 and P14. In summary, our results indicate that the cervical N13 has two separate components: (1) a postsynaptic potential recorded at Cv6, and (2) a presynaptic potential recorded at Cv2. The former may indeed be mediated through dorsal horn interneurons as has been suggested by others and the latter may be generated by a presynaptic volley through dorsal column before reaching the cuneate nucleus. Scalp recorded P13/P14 are also postsynaptic potentials and arise at least after the activation of the cuneate nucleus. From a clinical standpoint, it is important to evaluate Cv2and Cv6-N13 separately. The recording derivation for Cv6 may be referenced to the anterior neck. However, Cv2 must be referenced to a non-cephalic site. References Allison, T. Recovery functions of somatosensory evoked responses in man. Electroenceph. clin. Neurophysiol., 1962, 14: 331–343. Delestre, F., Lonchampt, P. and Dubas, F. Neural generators of P14 farfield somatosensory evoked potential studied in a patient with pontine lesion. Electroenceph. clin. Neurophysiol., 1986, 65: 227–230. Desmedt, J.E. and Cheron, G. Central somatosensory conduction in man: neural generators and interpeak latencies of the far-field components recorded from neck and right or left scalp and earlobes. Electroenceph. clin. Neurophysiol., 1980, 50: 382–403. Desmedt, J.E. and Cheron, G. Prevertebral recording of subcortical somatosensory evoked potentials in man: the spinal P13 component and the dual nature of the spinal generators. Electroenceph. clin. Neurophysiol., 1981, 52: 257–275. Desmedt, J.E. and Huy, N.T. Bit–mapping color imaging of the potential fields of propagated and segmental subcortical components of somatosensory evoked potentials in man. Electroenceph. clin. Neurophysiol., 1984, 58: 481–497. Emerson, R.G., Seyal, M. and Pedley, T.A. Somatosensory evoked potentials following median nerve stimulation. Brain, 1984, 107: 169-182. Emori, T., Yamada, T., Seki, Y., Yasuhara, A., Ando, K., Honda, Y., Leis, A.A. and Vachotimanont, P. Recovery functions of fast frequency potentials in the initial negative wave of median SEP. Electroenceph. clin. Neurophysiol., 1991, 78: 116–123. Gilliatt, R.W., Hopf, H.C., Rudge, P. and Baraitsh, M. The refractory and

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