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Neuromagnetic localization of cortical activity evoked by painful dental stimulation in man
Neuroscience Letters, 42 (1983) 77-82
77
Elsevier Scientific Publishers Ireland Ltd.
NEUROMAGNETIC LOCALIZATION OF CORTICAL ACTIVITY EVOKED BY PAINFUL DENTAL STIMULATION IN MAN
R. HARI l, E. KAUKORANTA l, K. REINIKAINEN l, T. HUOPANIEMIF- z and J. MAUNO z
~Low Temperature Laboratory, Helsinki University of Technology, 02150 Espoo 15 and ZDepartment of Physiology, University of Heisinki, 00290 Helsinki 29 (Finland) (Received July 29th, 1983; Revised version received August 29th, 1983; Accepted August 31st, 1983)
Key words: dental pain - magnetoencephalography - evoked responses - somatosensory cortex - Sll human brain
We have recorded cerebral magnetic fields evoked by painful dental stimulation. The field pattern indicates a current source at the upper bank of the anterior Sylvian fissure, corresponding to the anterior end of the secondary somatosensory cortex. Thi'o finding suggests cortical representation of tooth pulp in man. The neuromagnetic technique, allowing the investigation of this cortical area, thus provides a new non-invasive tool for pain research.
Cortical mechanisms of pain are poorly understood in man. Available information derives from clinical reports of neurosurgical and neurological patients. This scarcity arises from the lack of non-invasive means to study cortical representation of pain in healthy subjects. For example, electrical evoked potentials elicited by dental pulp stimulation [1, 2] reflect arousal of the subject rather than activation of a certain cortical projection area. In comparison to electroencephalography, the neuromagnetic techniques (for reviews, see refs. 14 and 19) provides better spatial resolution and better detection of signals originating in fissural cortex. With this technique it is possible, for example, to differentiate between activities at the primary and secondary somatosensory cortices [4, 5, 16]. In the present work we show that the neuromagnetic technique also allows us to localize cortical areas activated by painful dental pulp stimulation in man. The recordings were made in a magnetically shielded room [8]. The component of the magnetic field perpendicular to the skull was measured with a first order gradiometer, whose pickup coil was about 12 mm above the skull. The pickup coil radius was 7.5 mm, and the intercoil distance 57.5 mm. The noise of the gradiometer was 30 ft/~-Hz. Six adult subjects were studied. In one subject, the right side of the head was extensively mapped in consecutive measurements. In 3 other subjects the qualitative findings of the first subject were confirmed with less numerous 0304-3940/83/$ 03.00 © 1983 Elsevier Scientific Publishers Ireland Ltd.
75
measurements. Two subjects, each of them having one devitalized upper central incisor, served as controls. The upper central incisor was stimulated electrically with non-invasive electrodes. The stimuli were monophasic constant current square wave pulses of 10 ms duration. The cathode, made of conducting rubber (diameter 4.5 mm), was manually pressed by the subject against the crown of the intact upper central incisor. The tooth was isolated by cotton wool from the lip and dried carefully before each measurement. The anode was on the skin beneath the nose. In mapping studies, stimulus intensity was adjusted to produce a clearly painful sensation. The effect of stimulus intensity was studied separately. During the measurement the subject was lying and was instructed to fixate on a point on the opposite wall. The interstimulus interval of 4 s allowed blinking and swallowing between the stimuli. The measurement bandwidth was 0.05-50 Hz. All single responses were visually checked before averaging to eliminate artefacts. For each measurement location, 40-56 responses were averaged. The analysis period of 1024 ms included a prestimulus period of at least 250 ms. At many measurement locations, dental stimulation elicited clear responses within the first 200 ms after the stimulation onset. The main deflections reaching in amplitude up to 0.45 pT, occurred at latencies of 90-100 ms. As Fig. 1
il-
! 0,2 pT
i 0,2 pT i.
i A i
B i I
C v ...................... l
0
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i
l
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Fig. I (Left). Averaged magnetic responses of one subject to stimuli of 3 different intensities: A, just above the sensory threshold (average stimulation current ! = 20 cA); B, painful (l = 28 #A); C, very painful (i = 69 #A). Contralateral central incisor was stimulated, and the responses were measured at the right centrotemporal area. The number of averaged responses is about 50 for each curve. Curves from two separate measurements are superposed. Downward deflection indicates flux out of the skull. Note the stimulus artefact at the beginning of each trace. Fig. 2 (Right). Averaged magnetic responses from another subject at two measurement locations (A, posterior frontotemporal area; B, anterior frontotemporal area) on the right hemisphere.
79
demonstrates, the reproducibifity of the responses in consecutive measurements was rather good. Stimulation of ,psi- and contralateral central incisors elicited similar responses. Responses were obtained already at stimulus intensities slightly above the sensory threshold (Fig. IA). With increasing stimulus intensity the form of the responses changed slightly: there was an additional small deflection at 200 ms and a longer slow shift after the stimulus; simultaneously the peak latency o f the dominant deflection decreased by about 15 ms (Fig. I B , C). The main deflection changed in polarity between the anterior and posterior front,temporal areas (Fig. 2). This change of polarity is clearly demonstrated by the is, field contour map (Fig. 3), which shows dipolar field pattern at a latency of 100 ms: on the right hemisphere the flux came out of the skull from the posterior part of t~te measurement grid and re-entered the skull at the anterior part. On the left the polarities of the deflections were opposite. The field pattern agrees with a dipolar current source parallel to the polarity reversal line in a depth of 2.5 cm from the scalp (for determination of the depth of the source, see ref. 5). The dipole - in-
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Fig. 3. Is,field contour map at a latency of 100 ms after the stimulus onset. The map was calculated using a weighted least squares approximation and bicubic spline interpolation [ 1i ]. The mean amplitlJde during the 250 ms before the stimulus served as baseline for the amplitude measurements. The solid lines indicate flux into the skull and the dashed lines flux out of the skull, the dotted lines show the zero lines. The curves are separated by 0,03 pT. The measurement grid is shown in the schematic head. The interpoint distance is 2 cm and the black dot shows the location of T4 of the International 10-20 system.
80
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Fig. 4. Responses of one subject to the stimulation of a healthy (A) and devitalized (B) upper incisor, Measurement from the right frontotemporai area. Other details as in Fig. I.
dicating the direction of the main current flow - points upwards at this latency. According to the available information about the relationship between the skull and the fissures, the source is at the upper lip of the anterior part of the Sylvian fissure. Although the field distribution strongly suggests a cerebral source within the Sylvian fissure, a special effort was made to rule out extracerebral artefacts as sources of the responses. Eye artefacts can be e~ +:luded: (1) the location of the source - as estimated on the basis of the measured field extrema - is clearly posterior to the eyes; (2) the eye movements - neither horizontal nor ¢ertical - do not generate magnetic signals which change in polarity at the measurement area [7]; (3) the eye blink, which might be caused by a sudden painful stimulus, causes at the frontotemporal area a magnetic artefact which has opposite polarity to the main deflections of the present responses. These artefacts do not change in polarity at the measurement area (own unpublished results). Muscle artefacts can be excluded: (l) increased tension of the temporalis muscle by biting the teeth together did not increase the amplitude of the response; (2) the dependence of the signal on the distance between the magnetometer and the skull fitted better with a deep (cerebral) than with a superficial (muscular) source; (3) the form of the field pattern - with steepest slopes near the polarity reversal line - does not suggest activation of a broad superficial dipolar layer (like the temporalis muscle); (4) electric stimulation of ipsilateral median and peroneal nerves also elicits dipolar field patterns at the frontotemporal area, evidently due to activation of the secondary somatosensory cortex SII [4, 5]. The sources of these responses are slightly posterior to those observed in the present study. These somatotopic features suggest cerebral rather than muscular origin.
81
It seems improbable that fibers other than dental pulp afferents have been stimulated: (1) the subjects always localized the sensation only to the tooth; (2) even at low intensities Oust exceeding the sensory threshold), electric stimulation of the lips (cutaneous branches II and III of the trigeminal nerve) elicited blink artefacts contaminating the responses at the frontal area. The polarity o f these artefacts was opposite to that of our magnetic responses at the same area, and the artefacts did not reverse polarity at the measurement area; (3) stimulation of the devitalized (pulpotomized) tooth in two subjects did not elicit any evoked response with the same stimulation as used for intact teeth (Fig. 4). So the responses could not be due to activation of cutaneous, gingival or periodontal fibers. We evidently recorded activity transmitted by the A-delta tooth pulp afferents [18], although C-fibers might have been activated at high stimulus intensities, which resulted to responses of different waveforms. In monkeys, the first afferent impulses reach the cerebral cortex about 20 ms after dental stimulation [6]. Stimulus artefacts prevented us from paying attention to the magnetic counterparts of these early deflections. The opinions about cortical representation of pain in humans have been controversial. In some patients, partial removal of the primary somatosensory cortex SI ~t the postcentral gyrus has relieved pre-existing pain [9]. In cats and monkeys, tooth pulp afferents reach SI in addition to SII and the anterior orbital cortex [6, 10, 12]. In the present study, the location and direction of the estimated current source suggest activation of the rostral and of SII [13, 21], rather than activation of the postcentral SI. The results thus support those of Chatrian et al. [2] who by recording electric evoked potentials to painful dental stimuli, suggested that the nociceptive stimuli might activate SII at latencies of 80-90 ms. Because pain is a primitive sensation, its possible representation at the phylogenetically old SII [15] seems understandable. However, one should be cautious in interpreting evoked responses in terms of activation of a certain brain area, because both the electrical scalp recordings and the neuromagnetic recordings reveal the neural sources only in reference to the skull. Unfortunately, the external landmarks do not allow exact localization of the underlying brain areas. For two of our subjects, whose field patterns on the left and right hemispheres were compared, the sources on the left were significantly posterior to those on the right (difference of at least 3 cm). This finding agrees with anatomical evidence of hemispheric asymmetry: the planum temporale is larger on the left than on the right, and also the slope of Sylvian fissure is different [3, 17, 20]. Further experiments are needed to determine whether the studied fissural cortex is also activated by nociceprive stimuli from other parts of the body, or whether it is specific to dental stimulation. This study has been supported by the Academy of Finland. The gradiometer was constructed by Mr. R. Ilmoniemi and the dental stimulator by Mr. P. Vikberg. The computer programs were written by Mr. M. H~m~il~iinen and Mr. J. Salminen. We thank Dr. L. Leinonen for helpful comments.
82
1 Chapman, C.R., Chen, A.C.N. and Harkins, S.W., Brain evoked potentials as correlates of laboratory pain: a review and perspective. In J.J. Bonica, J.C. Liebeskind and D. Albe-Fessard (Eds.), Advances in Pain REsearch and Therapy, Vol. 3, Raven Press, New York, 1979, pp. 791-803. 2 Chatrian, G.E., Canfield, R.C., Knauss, T.A. and Lettich, E., Cerebral responses to electrical tooth pulp stimulation in man, Neurology, 25 (1975) 745-757. 3 Geschwind, N. and Levitsky, W., Human brain: left right asymmetries in temporal speech region, Science, 161 (1968) 186-187. 4 Hari, R., H~im~l~iinen, M., Kaukoranta, E., Reinikainen, K. and Teszner, D., Neuromagnetic responses from the second somatosensory cortex in man, Acta neurol, scand., in press. 5 Hari, R., Reinikainen, K., Kaukoranta, E., H~im~il~iinen, M., llmoniemi, R., Penttinen, A., Salminen, J. and Teszner, D., Somatosensory evoked cerebral magnetic fields from SI and Sll in man, Electroenceph. din. Neurophysiol., in press. 6 van Hassel, H.J., Biedenback, M.A. and Brown, A.C., Cortical potentials evoked by tooth pulp stimulation in rhesus monkeys, Arch. Oral. Biol., 17 (1972) 1059-1066. 7 Katila, T., Maniewski, R., Poutanen, T., Varpula, T. and Karp, P., Magnetic fields produced by the human eye, J. appl. Physiol., 52 (1981) 2565-2571. 8 Kelh/i, V.O., Pukki, J.M., Peltonen, R.S., Penttinen, A.A., llmoniemi, R.J. and Heino, J.J., Design, construction and performance of a large-volume magnetic shield, IEEE Trans Magn., MAG-18 (1982) 260-270. 9 Lewin, W. and Phillips, C.G., Observations on partial removal of the post-central gyrus for pain, J. Neurol. Neurosurg. Psychiat., 15 (1952) 143-147. 10 Lund, J.P. and Sessle, B.J., Oral-facial and jaw muscle afferent projections to neurons in cat frontal cortex, Exp. Neurol., 45 (1974) 314-331. 1! McLain, D.H., Drawing contours from arbitrary data points, The Computer J., 17 (1971) 318-324. 12 Melzack, R. and Haugen, F.P., Responses evoked at the cortex by tooth stimulation, Amer. J. Physiol., 190 (1957) 570-574. 13 Penfield, W. and Rasmussen, T., The Cerebral Cortex of Man. A Clinical Study of Localization of Function, Macmillian, New York, 1950. 14 Reite, M. and Zimmerman, J., Magnetic phenomena of the central nervous system, Ann. Rev. Biophys. Bioengng., 7 (1978) 167-188. 15 Sanides, F., Comparative architectonics of the neocortex of mammals and their evolutionary interpre'.ation, Ann. N.Y. Acad. Sci. 167 (1969) 404-423. 16 Teszner, D., Hari, R., Nicolas, P. and Varpula, T., Somatosensory evoked magnetic fields: mappings and the influence of stimulus repetition. 11 Nuovo Cimento, 2D (1983) 429-437. 17 Teszner, D., Tzavaras, A., Gruner, J. and H6caen, H., L'asym6trie droite-gauche du planum temporale; apropos de l'~tude anatomique de 100 cervaux, Rev. Neurol., 126 (1972) 444-449. 18 Virtanen, A., N~irhi, M., Huopaniemi, T. and Hirvonen, T., Thresholds of intradental A- and Cnerve fibres in the cat to electrical current pulses of different duration, Acta physiol, scand., in press. 19 Williamson, S.J. and Kaufman, L., Biomagnetism, J~ Magn. Magn. Mat., 22 (1981) 129-202. 20 Witelson, S.F., Anatomic asymmetry in the temporal lobes: its documentation, phylogenesis, and relationship to functional asymmetry, Ann~ N.Y. Acad. Sci., 299 (1977) 328-354. 21 Woolsey, C.N., Erickson, T.C. and Gilson, W.E., Localization in somatic and motor areas of human cerebral cortex as determined by direct recording of evoked potentials and electric stimulation, J. Neurosurg., 51 (1979)476-506.
77
Elsevier Scientific Publishers Ireland Ltd.
NEUROMAGNETIC LOCALIZATION OF CORTICAL ACTIVITY EVOKED BY PAINFUL DENTAL STIMULATION IN MAN
R. HARI l, E. KAUKORANTA l, K. REINIKAINEN l, T. HUOPANIEMIF- z and J. MAUNO z
~Low Temperature Laboratory, Helsinki University of Technology, 02150 Espoo 15 and ZDepartment of Physiology, University of Heisinki, 00290 Helsinki 29 (Finland) (Received July 29th, 1983; Revised version received August 29th, 1983; Accepted August 31st, 1983)
Key words: dental pain - magnetoencephalography - evoked responses - somatosensory cortex - Sll human brain
We have recorded cerebral magnetic fields evoked by painful dental stimulation. The field pattern indicates a current source at the upper bank of the anterior Sylvian fissure, corresponding to the anterior end of the secondary somatosensory cortex. Thi'o finding suggests cortical representation of tooth pulp in man. The neuromagnetic technique, allowing the investigation of this cortical area, thus provides a new non-invasive tool for pain research.
Cortical mechanisms of pain are poorly understood in man. Available information derives from clinical reports of neurosurgical and neurological patients. This scarcity arises from the lack of non-invasive means to study cortical representation of pain in healthy subjects. For example, electrical evoked potentials elicited by dental pulp stimulation [1, 2] reflect arousal of the subject rather than activation of a certain cortical projection area. In comparison to electroencephalography, the neuromagnetic techniques (for reviews, see refs. 14 and 19) provides better spatial resolution and better detection of signals originating in fissural cortex. With this technique it is possible, for example, to differentiate between activities at the primary and secondary somatosensory cortices [4, 5, 16]. In the present work we show that the neuromagnetic technique also allows us to localize cortical areas activated by painful dental pulp stimulation in man. The recordings were made in a magnetically shielded room [8]. The component of the magnetic field perpendicular to the skull was measured with a first order gradiometer, whose pickup coil was about 12 mm above the skull. The pickup coil radius was 7.5 mm, and the intercoil distance 57.5 mm. The noise of the gradiometer was 30 ft/~-Hz. Six adult subjects were studied. In one subject, the right side of the head was extensively mapped in consecutive measurements. In 3 other subjects the qualitative findings of the first subject were confirmed with less numerous 0304-3940/83/$ 03.00 © 1983 Elsevier Scientific Publishers Ireland Ltd.
75
measurements. Two subjects, each of them having one devitalized upper central incisor, served as controls. The upper central incisor was stimulated electrically with non-invasive electrodes. The stimuli were monophasic constant current square wave pulses of 10 ms duration. The cathode, made of conducting rubber (diameter 4.5 mm), was manually pressed by the subject against the crown of the intact upper central incisor. The tooth was isolated by cotton wool from the lip and dried carefully before each measurement. The anode was on the skin beneath the nose. In mapping studies, stimulus intensity was adjusted to produce a clearly painful sensation. The effect of stimulus intensity was studied separately. During the measurement the subject was lying and was instructed to fixate on a point on the opposite wall. The interstimulus interval of 4 s allowed blinking and swallowing between the stimuli. The measurement bandwidth was 0.05-50 Hz. All single responses were visually checked before averaging to eliminate artefacts. For each measurement location, 40-56 responses were averaged. The analysis period of 1024 ms included a prestimulus period of at least 250 ms. At many measurement locations, dental stimulation elicited clear responses within the first 200 ms after the stimulation onset. The main deflections reaching in amplitude up to 0.45 pT, occurred at latencies of 90-100 ms. As Fig. 1
il-
! 0,2 pT
i 0,2 pT i.
i A i
B i I
C v ...................... l
0
V-v................
100 ms
i
l
I
d
L
0
.....
100 ms
Fig. I (Left). Averaged magnetic responses of one subject to stimuli of 3 different intensities: A, just above the sensory threshold (average stimulation current ! = 20 cA); B, painful (l = 28 #A); C, very painful (i = 69 #A). Contralateral central incisor was stimulated, and the responses were measured at the right centrotemporal area. The number of averaged responses is about 50 for each curve. Curves from two separate measurements are superposed. Downward deflection indicates flux out of the skull. Note the stimulus artefact at the beginning of each trace. Fig. 2 (Right). Averaged magnetic responses from another subject at two measurement locations (A, posterior frontotemporal area; B, anterior frontotemporal area) on the right hemisphere.
79
demonstrates, the reproducibifity of the responses in consecutive measurements was rather good. Stimulation of ,psi- and contralateral central incisors elicited similar responses. Responses were obtained already at stimulus intensities slightly above the sensory threshold (Fig. IA). With increasing stimulus intensity the form of the responses changed slightly: there was an additional small deflection at 200 ms and a longer slow shift after the stimulus; simultaneously the peak latency o f the dominant deflection decreased by about 15 ms (Fig. I B , C). The main deflection changed in polarity between the anterior and posterior front,temporal areas (Fig. 2). This change of polarity is clearly demonstrated by the is, field contour map (Fig. 3), which shows dipolar field pattern at a latency of 100 ms: on the right hemisphere the flux came out of the skull from the posterior part of t~te measurement grid and re-entered the skull at the anterior part. On the left the polarities of the deflections were opposite. The field pattern agrees with a dipolar current source parallel to the polarity reversal line in a depth of 2.5 cm from the scalp (for determination of the depth of the source, see ref. 5). The dipole - in-
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Fig. 3. Is,field contour map at a latency of 100 ms after the stimulus onset. The map was calculated using a weighted least squares approximation and bicubic spline interpolation [ 1i ]. The mean amplitlJde during the 250 ms before the stimulus served as baseline for the amplitude measurements. The solid lines indicate flux into the skull and the dashed lines flux out of the skull, the dotted lines show the zero lines. The curves are separated by 0,03 pT. The measurement grid is shown in the schematic head. The interpoint distance is 2 cm and the black dot shows the location of T4 of the International 10-20 system.
80
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Fig. 4. Responses of one subject to the stimulation of a healthy (A) and devitalized (B) upper incisor, Measurement from the right frontotemporai area. Other details as in Fig. I.
dicating the direction of the main current flow - points upwards at this latency. According to the available information about the relationship between the skull and the fissures, the source is at the upper lip of the anterior part of the Sylvian fissure. Although the field distribution strongly suggests a cerebral source within the Sylvian fissure, a special effort was made to rule out extracerebral artefacts as sources of the responses. Eye artefacts can be e~ +:luded: (1) the location of the source - as estimated on the basis of the measured field extrema - is clearly posterior to the eyes; (2) the eye movements - neither horizontal nor ¢ertical - do not generate magnetic signals which change in polarity at the measurement area [7]; (3) the eye blink, which might be caused by a sudden painful stimulus, causes at the frontotemporal area a magnetic artefact which has opposite polarity to the main deflections of the present responses. These artefacts do not change in polarity at the measurement area (own unpublished results). Muscle artefacts can be excluded: (l) increased tension of the temporalis muscle by biting the teeth together did not increase the amplitude of the response; (2) the dependence of the signal on the distance between the magnetometer and the skull fitted better with a deep (cerebral) than with a superficial (muscular) source; (3) the form of the field pattern - with steepest slopes near the polarity reversal line - does not suggest activation of a broad superficial dipolar layer (like the temporalis muscle); (4) electric stimulation of ipsilateral median and peroneal nerves also elicits dipolar field patterns at the frontotemporal area, evidently due to activation of the secondary somatosensory cortex SII [4, 5]. The sources of these responses are slightly posterior to those observed in the present study. These somatotopic features suggest cerebral rather than muscular origin.
81
It seems improbable that fibers other than dental pulp afferents have been stimulated: (1) the subjects always localized the sensation only to the tooth; (2) even at low intensities Oust exceeding the sensory threshold), electric stimulation of the lips (cutaneous branches II and III of the trigeminal nerve) elicited blink artefacts contaminating the responses at the frontal area. The polarity o f these artefacts was opposite to that of our magnetic responses at the same area, and the artefacts did not reverse polarity at the measurement area; (3) stimulation of the devitalized (pulpotomized) tooth in two subjects did not elicit any evoked response with the same stimulation as used for intact teeth (Fig. 4). So the responses could not be due to activation of cutaneous, gingival or periodontal fibers. We evidently recorded activity transmitted by the A-delta tooth pulp afferents [18], although C-fibers might have been activated at high stimulus intensities, which resulted to responses of different waveforms. In monkeys, the first afferent impulses reach the cerebral cortex about 20 ms after dental stimulation [6]. Stimulus artefacts prevented us from paying attention to the magnetic counterparts of these early deflections. The opinions about cortical representation of pain in humans have been controversial. In some patients, partial removal of the primary somatosensory cortex SI ~t the postcentral gyrus has relieved pre-existing pain [9]. In cats and monkeys, tooth pulp afferents reach SI in addition to SII and the anterior orbital cortex [6, 10, 12]. In the present study, the location and direction of the estimated current source suggest activation of the rostral and of SII [13, 21], rather than activation of the postcentral SI. The results thus support those of Chatrian et al. [2] who by recording electric evoked potentials to painful dental stimuli, suggested that the nociceptive stimuli might activate SII at latencies of 80-90 ms. Because pain is a primitive sensation, its possible representation at the phylogenetically old SII [15] seems understandable. However, one should be cautious in interpreting evoked responses in terms of activation of a certain brain area, because both the electrical scalp recordings and the neuromagnetic recordings reveal the neural sources only in reference to the skull. Unfortunately, the external landmarks do not allow exact localization of the underlying brain areas. For two of our subjects, whose field patterns on the left and right hemispheres were compared, the sources on the left were significantly posterior to those on the right (difference of at least 3 cm). This finding agrees with anatomical evidence of hemispheric asymmetry: the planum temporale is larger on the left than on the right, and also the slope of Sylvian fissure is different [3, 17, 20]. Further experiments are needed to determine whether the studied fissural cortex is also activated by nociceprive stimuli from other parts of the body, or whether it is specific to dental stimulation. This study has been supported by the Academy of Finland. The gradiometer was constructed by Mr. R. Ilmoniemi and the dental stimulator by Mr. P. Vikberg. The computer programs were written by Mr. M. H~m~il~iinen and Mr. J. Salminen. We thank Dr. L. Leinonen for helpful comments.
82
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