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Blink reflex far fields mimicking putative cortical trigeminal evoked potentials
Electroencephalography and clinical Neurophysiology, 93 (1994) 240-242
240
© 1994 Elsevier Science Ireland Ltd. 0924-980X/94/$07.00
EEM 93744
Short communication
Blink reflex far fields mimicking putative cortical trigeminal evoked potentials M. Leandri *, R. Schizzi and E. Favale Department of Neurology and CIND (Centro Interuniversitario per la Neurofisiologia del Dolore), UniL,ersity of Genoa, Via De Toni 5, 16132 Genoa (Italy) ( A c c e p t e d for publication: 28 March 1994)
Summary The R1 component of the blink reflex was evoked by stimulation of the left supraorbital and infraorbital nerves in 10 subjects. In addition, an artificial dipole was placed over the left eyebrow, in order to simulate the occurrence of the R1 component of the blink reflex. These electrical events were recorded at scalp locations Fz, F8, F7, C6, C5, referred either to Cv7 (seventh cervical vertebra) or to Fz. It was found that the blink R1 and the field of the artificial dipole had similar behaviour across the scalp; larger amplitudes were recorded ipsilateral to the stimulus from derivations referred to Cv7, but when referred to Fz larger contralateral amplitudes were measured. In the latter condition, the scalp-recorded R1 shows similar amplitude behaviour to electrical events originating from the cortex and hence its appearance may be deceiving. Key words: Blink reflex; Trigeminal evoked potentials; Artefacts; Electrical field; Scalp record; Dipole
The origin of trigeminal evoked potentials (TEPs) with latencies over 10 msec is very much under dispute, because they take place within the same epoch as cranial reflexes, which may heavily contaminate the recording of genuine neural activity. It has already been demonstrated that dramatic changes in the scalp records occur when the subject is anaesthetized and curarized, with all muscular activity cancelled out (Leandri et al. 1987). Nevertheless, the fact that the scalp activity recorded after trigeminal stimulation is higher over the contralateral hemisphere has been considered as proof that it actually originates from the sensory cortex (Altenmiiller et al. 1990). These authors, as well as others (St6hr and Petruch 1979; Findler and Feinsod 1982; Hashimoto 1988; Soustiel et al. 1991), used a frontal electrode as reference. In such conditions it may be expected that a signal source ipsilateral to the stimulus and near the reference may be detected with largest amplitude on the contralateral scalp. To substantiate this hypothesis, we set up a series of experiments where asymmetrical signals were generated either biologically (the R1 component of the blink reflex) or artificially (half sine-wave delivered through suitably placed surface electrodes).
Material and methods
Experiments were carried out in 10 healthy volunteers, who gave informed consent and who had been selected for the constant occurrence of R1 component of the blink reflex with the 2 types of stimulation used. Electrical pulses, 0.1 msec wide, at the rate of l/sec, were delivered through needle electrodes inserted into the left supraorbital notch and the left infraorbital foramen, in order to stimulate the respective nerve trunks. The intensity of the stimuli was set between 0.30 and 0.75 mA (mean 0.28_+0.10 mA) for the
supraorbital nerve, and between 0.37 and 0.78 mA (mean 0.35 _+0.08 mA) for the infraorbital nerve, i.e., about 1.5 times the minimum intensity required to evoke the occurrence of RI component of the blink reflex after stimulation of each nerve. Recording electrodes were placed on the orbicularis oculi muscle (one connected to the non-inverting input of the amplifier on the lower lid, the other connected to the inverting input placed on the outer canthus), and at scalp locations Fz, F8, F7, C6, C5 (according to the 10-20 international system). The scalp electrodes were referred either to Cv7 (seventh cervical vertebra) or to Fz itself. In a subsequent session, an artificial dipole was created by placing two conductive strips, 2 x 4 ram, parallel and horizontally oriented, over the left eyebrow midpoint. Through them a half sine-wave current of 10 msec duration was delivered, with positive polarity applied to the upper electrode. Its intensity was adjusted between 2 and 4 mA in order to obtain a 400 /zV record from the Fz-Cv7 derivation in all subjects. The electrical signals were amplified with a gain of 100,000 when the blink reflex was elicited, and with a gain of 5000 when the artificial dipole was used. In both cases, the overall bandpass was between 10 and 10,000 Hz, 3 dB points. 250 responses were always averaged. The amplitude of the scalp far field related to the RI component of the blink reflex was quantified as a percentage of the absolute amplitude of the field recorded from derivation Fz-Cv7. Also amplitudes of the electrical fields related to the artificial dipole were expressed as percentages of the field recorded from Fz-Cv7. The 2-tailed t test was applied to analyse the amplitude differences between ipsilateral and contralateral records.
Results
Records of the R1 component after stimulation of the supraorbital nerve (Fig. 1) * Corresponding author. Tel.: 39-10-3537081; Fax: 39-10-354180.
SSDI 0 0 1 3 - 4 6 9 4 ( 9 4 ) 0 0 1 0 1 - P
When stimulating the supraorbital nerve, the R1 component bad an onset latency between 9.2 and 12.8 msec (mean 10.49_+1.02 msec). Its amplitude at the Fz-Cv7 derivation ranged from 8.38 to
BLINK REFLEX AND TEPs
241
A
B
Fz-Cv7
FB-Fz
F7-Fz
FS-Cv7 F7-Cv7 C6-Fz C6-Cv7
CS-Fz
C5-Cv7
I
I
I
l
I
i
I
I
I
I
Fig. 1. An example of recording of R1 blink component from the various scalp derivations: the left supraorbital nerve has been stimulated. Changing the reference from Cv7 fo Fz makes R1 reverse polarity and grow larger contralaterally to the stimulated side.
32.3 tzV (mean 19.54_+8.32 izV). When recorded from derivations referred to Cv7, its amplitude was larger at locations ipsilateral to the stimulus, the asymmetry being more noticeable on the frontal than on the central electrodes, but in both cases statistically significant (Table I, 1st and 2nd row). Conversely, when the Fz reference was employed, R1 was reversed in polarity and larger on the contralateral scalp, still with a larger difference between F8 and F7 than between C6 and C5, always significant. Side-to-side differences showed a rather large inter-individual variability, with both Cv7 and Fz as reference.
Records of the R1 component after stimulation of the infraorbital nerve The R1 component ranged in latency between 9.5 and 13.2 msec (mean 10.66_+ 1.14 msec), with an amplitude as recorded from Fz-Cv7
ranging from 7.4 to 28.7 izV (mean 17.41 tzV+7.42). The scalp records of R1 with Cv7 and Fz reference showed the same amplitude trend as those obtained after stimulation of the supraorbital nerve (Table I, 3rd and 4th row).
Records of the field generated by the artificial dipole (Fig. 2) When recorded with Cv7 as reference, the field from the artificial dipole was recorded with a larger amplitude on the ipsilateral side, whereas when the Fz reference was used, the field was reversed in polarity and prevailed contralaterally. In all cases the side-to-side differences were significant and more prominent at the frontal than at the central electrodes (Table I, 5th and 6th row). Thus, the behaviour of the field originating from the artificial dipole closely paralleled that of the field from the R1 component, but with a
B
A
Fz-Cv7 -
F8-Cv7
~
FB-Fz
FT-Fz
F7-Cv7
CS-Fz
C5-Cv7 C6-Cv7
-
C6-Fz
Fig. 2. A sample record of the field generated by the artificial dipole from various derivations on the scalp. The artificial dipole has been placed on the left side. Amplitude behaviour of the recorded potential is similar to that of the real blink in Fig. 1.
242
M. L E A N D R I ET AL.
TABLE I Amplitudes of R1 as percentages of amplitude at Fz-Cv7 (absolute values). The t test always detected significant differences between the F8 and F7 columns, and between the C6 and C5 columns. Fz-Cv7
F8-Cv7
F7-Cv7
C6-Cv7
C5-Cv7
Stimulation of supraorbital ner~'e Mean S.D.
100 0
51.11 14.44
73.93 14.33
16.22 5.04
Fz-Fz
F8-Fz
F7-Fz
C6-Fz
C5-Fz
11 11
59.26 17.50
31.59 17.37
101.56 6.11
88.40 5.53
24.28 4.09
Mean S.D.
27.08 4.56
Stimulation of infraorbital nL~ert~e Mean S.D.
100 0
68.70 13.31
76.59 14.84
14.45 4.49
Fz-Fz
F8-Fz
F7-Fz
C6-Fz
C5-Fz
0 0
37.93 16.14
28.37 17.99
103.70 5.45
91.79 4.96
37.90 2.31
74.92 2.23
15,67 1,63
26.17 1.27
Mean S.D.
Artificial dipole Mean S.D.
100 0 Fz-Fz
F8-Fz
F7-Fz
C6-Fz
C5-Fz
100 0
75.28 2.80
30.39 2.71
102.23 1.97
89.50 1.54
Mean S.D,
smaller inter-individual variability, obviously due to the complete control of dipole parameters.
Discussion Our results show that the R1 component of the blink reflex can be elicited by stimulation of both the first and second trigeminal division, We could detect no statistically significant difference in R1 latency or amplitude, whether it was elicited by stimulating one division or the other, whereas the necessary minimum intensity of stimulation for appearance of RI was slightly larger for the second division (the difference being only marginally significant, P = 0.09). Because our subjects had been selected, the occurrence of R1 was 100%, but it had already been reported that R1 may be evoked by stimuli in any of the 3 trigeminal divisions in unselected subjects (Gandiglio and Fra 1967). W h e t h e r R1 was elicited by stimulation of the first or second division, it was recorded from the 5 scalp electrodes in a similar way. It may be assumed that the extracranial Cv7
electrode approximates the requirements for a genuinely neutral reference with respect to scalp electrical fields. So, there is little wonder that R1, however elicited, is best recorded at frontal locations and ipsilaterally to its site of origin. However, if the Fz electrode is used as reference, dramatic changes in amplitudes and apparent behaviour of the R1 field occur, simply because Fz is an active location, in fact the most active of the others chosen by us and by many authors seeking cortical TEPs, with respect to the R1 component. Because Fz and each of the scalp electrodes ipsilateral to the stimulus, and therefore to the site generating R1, are more active than the farthest contralateral electrodes, the apparent result is a larger amplitude of R1 on the contralateral scalp, but this is an artefact due to improper use of the reference electrode. This conclusion is supported by the experiments with the artificial dipole. These offer the undeniable advantage of precisely known and controllable parameters. The electrical field thus generated spread in exactly the same way as the RI field and was detected with a larger amplitude contralaterally when the Fz reference was used. In conclusion, we have supplied evidence about the possibility that the R1 component of the blink can be elicited by stimulation of either the infraorbital and supraorbital nerves and that it generates a scalp-recordable electrical field of asymmetrical amplitude which, according to the derivation used, may prevail over the hemisphere contralateral to the stimulus. The latter characteristic makes it similar to putative cortical trigeminal evoked potentials, so that it may well be mistaken for them.
References Altenmfiller, E., Cornelius, C.P. and Buettner, U.W. Somatosensory evoked potentials following tongue stimulation in normal subjects and patients with lesions of the afferent trigeminal system. Electroenceph, clin. Neurophysiol., 1990, 77: 403-415. Findler, G. and Feinsod, M. Sensory evoked response to electrical stimulation of the trigeminal nerve in humans. J. Neurosurg., 1982, 56: 545-549. Gandiglio, G. and Fra, L. Further observations on facial reflexes. J. Neurol. Sci., 1967, 5: 273-285. Hashimoto, I. Trigeminal evoked potentials following brief air puff: enhanced signal to noise ratio. Ann. Neurol., 1988, 23: 332-338. Leandri, M., Parodi, C.I., Zattoni, J. and Favale, E. Subcortical and cortical responses following infraorbital nerve stimulation in man. Electroenceph. clin. Neurophysiol., 1987, 66: 253-262. Soustiel, J.F., Feinsod, M. and Hafner, H. Short latency trigeminal evoked potentials - normative data and clinical correlations. Electroenceph. clin. Neurophysiol., 1991, 80: 119-125. St6hr, M. and Petruch, F. Somatosensory evoked potentials following stimulation of the trigeminal nerve in man. J. Neurol., 1979, 220: 95-98.
240
© 1994 Elsevier Science Ireland Ltd. 0924-980X/94/$07.00
EEM 93744
Short communication
Blink reflex far fields mimicking putative cortical trigeminal evoked potentials M. Leandri *, R. Schizzi and E. Favale Department of Neurology and CIND (Centro Interuniversitario per la Neurofisiologia del Dolore), UniL,ersity of Genoa, Via De Toni 5, 16132 Genoa (Italy) ( A c c e p t e d for publication: 28 March 1994)
Summary The R1 component of the blink reflex was evoked by stimulation of the left supraorbital and infraorbital nerves in 10 subjects. In addition, an artificial dipole was placed over the left eyebrow, in order to simulate the occurrence of the R1 component of the blink reflex. These electrical events were recorded at scalp locations Fz, F8, F7, C6, C5, referred either to Cv7 (seventh cervical vertebra) or to Fz. It was found that the blink R1 and the field of the artificial dipole had similar behaviour across the scalp; larger amplitudes were recorded ipsilateral to the stimulus from derivations referred to Cv7, but when referred to Fz larger contralateral amplitudes were measured. In the latter condition, the scalp-recorded R1 shows similar amplitude behaviour to electrical events originating from the cortex and hence its appearance may be deceiving. Key words: Blink reflex; Trigeminal evoked potentials; Artefacts; Electrical field; Scalp record; Dipole
The origin of trigeminal evoked potentials (TEPs) with latencies over 10 msec is very much under dispute, because they take place within the same epoch as cranial reflexes, which may heavily contaminate the recording of genuine neural activity. It has already been demonstrated that dramatic changes in the scalp records occur when the subject is anaesthetized and curarized, with all muscular activity cancelled out (Leandri et al. 1987). Nevertheless, the fact that the scalp activity recorded after trigeminal stimulation is higher over the contralateral hemisphere has been considered as proof that it actually originates from the sensory cortex (Altenmiiller et al. 1990). These authors, as well as others (St6hr and Petruch 1979; Findler and Feinsod 1982; Hashimoto 1988; Soustiel et al. 1991), used a frontal electrode as reference. In such conditions it may be expected that a signal source ipsilateral to the stimulus and near the reference may be detected with largest amplitude on the contralateral scalp. To substantiate this hypothesis, we set up a series of experiments where asymmetrical signals were generated either biologically (the R1 component of the blink reflex) or artificially (half sine-wave delivered through suitably placed surface electrodes).
Material and methods
Experiments were carried out in 10 healthy volunteers, who gave informed consent and who had been selected for the constant occurrence of R1 component of the blink reflex with the 2 types of stimulation used. Electrical pulses, 0.1 msec wide, at the rate of l/sec, were delivered through needle electrodes inserted into the left supraorbital notch and the left infraorbital foramen, in order to stimulate the respective nerve trunks. The intensity of the stimuli was set between 0.30 and 0.75 mA (mean 0.28_+0.10 mA) for the
supraorbital nerve, and between 0.37 and 0.78 mA (mean 0.35 _+0.08 mA) for the infraorbital nerve, i.e., about 1.5 times the minimum intensity required to evoke the occurrence of RI component of the blink reflex after stimulation of each nerve. Recording electrodes were placed on the orbicularis oculi muscle (one connected to the non-inverting input of the amplifier on the lower lid, the other connected to the inverting input placed on the outer canthus), and at scalp locations Fz, F8, F7, C6, C5 (according to the 10-20 international system). The scalp electrodes were referred either to Cv7 (seventh cervical vertebra) or to Fz itself. In a subsequent session, an artificial dipole was created by placing two conductive strips, 2 x 4 ram, parallel and horizontally oriented, over the left eyebrow midpoint. Through them a half sine-wave current of 10 msec duration was delivered, with positive polarity applied to the upper electrode. Its intensity was adjusted between 2 and 4 mA in order to obtain a 400 /zV record from the Fz-Cv7 derivation in all subjects. The electrical signals were amplified with a gain of 100,000 when the blink reflex was elicited, and with a gain of 5000 when the artificial dipole was used. In both cases, the overall bandpass was between 10 and 10,000 Hz, 3 dB points. 250 responses were always averaged. The amplitude of the scalp far field related to the RI component of the blink reflex was quantified as a percentage of the absolute amplitude of the field recorded from derivation Fz-Cv7. Also amplitudes of the electrical fields related to the artificial dipole were expressed as percentages of the field recorded from Fz-Cv7. The 2-tailed t test was applied to analyse the amplitude differences between ipsilateral and contralateral records.
Results
Records of the R1 component after stimulation of the supraorbital nerve (Fig. 1) * Corresponding author. Tel.: 39-10-3537081; Fax: 39-10-354180.
SSDI 0 0 1 3 - 4 6 9 4 ( 9 4 ) 0 0 1 0 1 - P
When stimulating the supraorbital nerve, the R1 component bad an onset latency between 9.2 and 12.8 msec (mean 10.49_+1.02 msec). Its amplitude at the Fz-Cv7 derivation ranged from 8.38 to
BLINK REFLEX AND TEPs
241
A
B
Fz-Cv7
FB-Fz
F7-Fz
FS-Cv7 F7-Cv7 C6-Fz C6-Cv7
CS-Fz
C5-Cv7
I
I
I
l
I
i
I
I
I
I
Fig. 1. An example of recording of R1 blink component from the various scalp derivations: the left supraorbital nerve has been stimulated. Changing the reference from Cv7 fo Fz makes R1 reverse polarity and grow larger contralaterally to the stimulated side.
32.3 tzV (mean 19.54_+8.32 izV). When recorded from derivations referred to Cv7, its amplitude was larger at locations ipsilateral to the stimulus, the asymmetry being more noticeable on the frontal than on the central electrodes, but in both cases statistically significant (Table I, 1st and 2nd row). Conversely, when the Fz reference was employed, R1 was reversed in polarity and larger on the contralateral scalp, still with a larger difference between F8 and F7 than between C6 and C5, always significant. Side-to-side differences showed a rather large inter-individual variability, with both Cv7 and Fz as reference.
Records of the R1 component after stimulation of the infraorbital nerve The R1 component ranged in latency between 9.5 and 13.2 msec (mean 10.66_+ 1.14 msec), with an amplitude as recorded from Fz-Cv7
ranging from 7.4 to 28.7 izV (mean 17.41 tzV+7.42). The scalp records of R1 with Cv7 and Fz reference showed the same amplitude trend as those obtained after stimulation of the supraorbital nerve (Table I, 3rd and 4th row).
Records of the field generated by the artificial dipole (Fig. 2) When recorded with Cv7 as reference, the field from the artificial dipole was recorded with a larger amplitude on the ipsilateral side, whereas when the Fz reference was used, the field was reversed in polarity and prevailed contralaterally. In all cases the side-to-side differences were significant and more prominent at the frontal than at the central electrodes (Table I, 5th and 6th row). Thus, the behaviour of the field originating from the artificial dipole closely paralleled that of the field from the R1 component, but with a
B
A
Fz-Cv7 -
F8-Cv7
~
FB-Fz
FT-Fz
F7-Cv7
CS-Fz
C5-Cv7 C6-Cv7
-
C6-Fz
Fig. 2. A sample record of the field generated by the artificial dipole from various derivations on the scalp. The artificial dipole has been placed on the left side. Amplitude behaviour of the recorded potential is similar to that of the real blink in Fig. 1.
242
M. L E A N D R I ET AL.
TABLE I Amplitudes of R1 as percentages of amplitude at Fz-Cv7 (absolute values). The t test always detected significant differences between the F8 and F7 columns, and between the C6 and C5 columns. Fz-Cv7
F8-Cv7
F7-Cv7
C6-Cv7
C5-Cv7
Stimulation of supraorbital ner~'e Mean S.D.
100 0
51.11 14.44
73.93 14.33
16.22 5.04
Fz-Fz
F8-Fz
F7-Fz
C6-Fz
C5-Fz
11 11
59.26 17.50
31.59 17.37
101.56 6.11
88.40 5.53
24.28 4.09
Mean S.D.
27.08 4.56
Stimulation of infraorbital nL~ert~e Mean S.D.
100 0
68.70 13.31
76.59 14.84
14.45 4.49
Fz-Fz
F8-Fz
F7-Fz
C6-Fz
C5-Fz
0 0
37.93 16.14
28.37 17.99
103.70 5.45
91.79 4.96
37.90 2.31
74.92 2.23
15,67 1,63
26.17 1.27
Mean S.D.
Artificial dipole Mean S.D.
100 0 Fz-Fz
F8-Fz
F7-Fz
C6-Fz
C5-Fz
100 0
75.28 2.80
30.39 2.71
102.23 1.97
89.50 1.54
Mean S.D,
smaller inter-individual variability, obviously due to the complete control of dipole parameters.
Discussion Our results show that the R1 component of the blink reflex can be elicited by stimulation of both the first and second trigeminal division, We could detect no statistically significant difference in R1 latency or amplitude, whether it was elicited by stimulating one division or the other, whereas the necessary minimum intensity of stimulation for appearance of RI was slightly larger for the second division (the difference being only marginally significant, P = 0.09). Because our subjects had been selected, the occurrence of R1 was 100%, but it had already been reported that R1 may be evoked by stimuli in any of the 3 trigeminal divisions in unselected subjects (Gandiglio and Fra 1967). W h e t h e r R1 was elicited by stimulation of the first or second division, it was recorded from the 5 scalp electrodes in a similar way. It may be assumed that the extracranial Cv7
electrode approximates the requirements for a genuinely neutral reference with respect to scalp electrical fields. So, there is little wonder that R1, however elicited, is best recorded at frontal locations and ipsilaterally to its site of origin. However, if the Fz electrode is used as reference, dramatic changes in amplitudes and apparent behaviour of the R1 field occur, simply because Fz is an active location, in fact the most active of the others chosen by us and by many authors seeking cortical TEPs, with respect to the R1 component. Because Fz and each of the scalp electrodes ipsilateral to the stimulus, and therefore to the site generating R1, are more active than the farthest contralateral electrodes, the apparent result is a larger amplitude of R1 on the contralateral scalp, but this is an artefact due to improper use of the reference electrode. This conclusion is supported by the experiments with the artificial dipole. These offer the undeniable advantage of precisely known and controllable parameters. The electrical field thus generated spread in exactly the same way as the RI field and was detected with a larger amplitude contralaterally when the Fz reference was used. In conclusion, we have supplied evidence about the possibility that the R1 component of the blink can be elicited by stimulation of either the infraorbital and supraorbital nerves and that it generates a scalp-recordable electrical field of asymmetrical amplitude which, according to the derivation used, may prevail over the hemisphere contralateral to the stimulus. The latter characteristic makes it similar to putative cortical trigeminal evoked potentials, so that it may well be mistaken for them.
References Altenmfiller, E., Cornelius, C.P. and Buettner, U.W. Somatosensory evoked potentials following tongue stimulation in normal subjects and patients with lesions of the afferent trigeminal system. Electroenceph, clin. Neurophysiol., 1990, 77: 403-415. Findler, G. and Feinsod, M. Sensory evoked response to electrical stimulation of the trigeminal nerve in humans. J. Neurosurg., 1982, 56: 545-549. Gandiglio, G. and Fra, L. Further observations on facial reflexes. J. Neurol. Sci., 1967, 5: 273-285. Hashimoto, I. Trigeminal evoked potentials following brief air puff: enhanced signal to noise ratio. Ann. Neurol., 1988, 23: 332-338. Leandri, M., Parodi, C.I., Zattoni, J. and Favale, E. Subcortical and cortical responses following infraorbital nerve stimulation in man. Electroenceph. clin. Neurophysiol., 1987, 66: 253-262. Soustiel, J.F., Feinsod, M. and Hafner, H. Short latency trigeminal evoked potentials - normative data and clinical correlations. Electroenceph. clin. Neurophysiol., 1991, 80: 119-125. St6hr, M. and Petruch, F. Somatosensory evoked potentials following stimulation of the trigeminal nerve in man. J. Neurol., 1979, 220: 95-98.