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The Journal of Neurophysiology Vol. 80 No. 4 October 1998, pp. 2077-2088
Copyright ©1998 by the American Physiological Society
Departments of Neurosurgery and Neurology, Johns Hopkins Hospital, Baltimore, Maryland 21287-7713
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ABSTRACT |
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 Abstract
 Introduction
Methods
Results
Discussion
References
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Lenz, F. A., M. Rios, D. Chau, G. L. Krauss, T. A. Zirh, and R. P. Lesser. Painful stimuli evoke potentials recorded from the parasylvian cortex in humans. J. Neurophysiol. 80: 2077-2088, 1998. Cutaneous stimulation of the face and hand with a CO2 laser in three awake patients evoked potentials (LEPs) recorded from the dominant left parasylvian cortex. These were recorded by means of a subdural grid of electrodes implanted for evaluation of epilepsy. Stimulation of the contralateral face resulted in waveforms consisting of a negative potential (N2, 162 ± 5 ms; mean ± SE) followed by a positive potential (P2, 340 ± 18 ms). Both waves occurred at longer latency after hand than after facial stimulation. N2 and P2 potentials recorded from the grid correspond well in morphology to those recorded from the scalp in four additional patients tested with the same stimulation paradigm. The N2 waves recorded from the subdural grid occurred at significantly shorter latencies than did those recorded from the scalp (184 ± 6 ms), but the P2 waves at the grid occurred at significantly longer latencies than did those recorded at the scalp (281 ± 13 ms). The amplitudes of the potentials recorded from the grid were maximal over the parietal operculum both for contralateral stimulation of the face or hand and for ipsilateral stimulation of the face. Potentials also were recorded in this area after stimulation of the ipsilateral hand. The cortical distributions of these potentials suggest that their generators are located in the parietal operculum or in the insula, or in both, consistent with previous PET, magnetoencephalographic, and scalp LEP source analyses. These previous analyses provide indirect evidence of nociceptive input to parasylvian cortex because the interpretation of each analysis incorporates multiple assumptions. The present results are the first direct evidence of nociceptive input to the human parasylvian cortex.
Substantial indirect evidence suggests that cortex of the parietal operculum and insula are involved in pain-signaling pathways in humans. Positron emission tomographic (PET) studies demonstrate pain-related blood flow activation of contralateral primary somatosensory (SI) cortex, bilateral parietal operculum (including secondary somatosensory cortex, SII), and insula (Casey et al. 1994 Subdural electrodes were implanted over the left fronto-temporal areas (see Fig. 3) in three patients (2 men, 1 woman, ages 26-38 yr) with medically intractable seizures of temporal lobe origin. The implanted left hemisphere was dominant for language in all three, as established by intracarotid amobarbital injection (Lesser et al. 1994
Subdural electrode recordings
Waveforms from subdural recordings in patient H after bilateral facial and hand stimulation are shown in Fig. 1. Reproducible biphasic potentials were recorded from many subdural electrodes. The LEPs consisted of a prominent negative (N2) potential followed by a positive (P2) potential. The most reproducible potentials occurred after contralateral and ipsilateral facial stimulation. Maximal subdural LEPs (Fig. 1B) from facial stimulation had a mean peak N2 latency of 156 ms for contralateral and 164 ms for ipsilateral stimulation; the P2 had peak latency of 312 ms for contralateral and ipsilateral stimulation.
Scalp electrode recordings
Figure 1 shows that scalp LEPs from facial stimulation produced large potentials at Cz and C3/C4 both ipsilateral and contralateral to the side of stimulation. The N2 potential had a vertex maximum (Cz) and the scalp P2 had a maximum at electrode position Pz, located at 40% of the distance from the vertex to the inion (Jasper 1958 Topography of subdural LEPs
Figure 2 displays a set of subdural LEP waveforms in response to contralateral facial stimulation in patient H. Peak amplitudes for the N2 component are seen over the parietal operculum. A similar pattern was seen for patient C. In patient P, the distribution of LEPs was more anterior with the maximum over the central sulcus. In all patients, the largest N2 potential occurred over facial sensorimotor areas as identified by cortical stimulation mapping (indicated by shading of circles in Figs. 3-5).
Laser-evoked potentials (LEPs) were recorded from the dominant, left, parasylvian cortex in awake humans with implanted subdural electrodes. These potentials consisted of a negative (N2) wave followed by a positive (P2) wave, which occurred at longer latency after hand than after facial stimulation. The amplitude of subdural LEPs was maximal over the parietal operculum for ipsilateral stimulation of the face and contralateral stimulation of both the face and hand. The topographic distribution of LEPs in response to stimulation of the face and hand was not consistently organized in accordance with the accepted somatotopy of SI (Penfield and Rasmussen 1955 Methodologic considerations
There are latency differences for both N2 and P2 components between scalp and subdural recordings after facial stimulation. The N2 component on scalp recordings has a longer latency than that on subdural recordings, whereas the P2 component recorded from the scalp has a shorter latency peak than that from subdural recordings (Table 1). Brain electrical source analysis (BESA) predicts that the subdural latencies of the N2 and P2 potentials for a parasylvian generator should be shorter than latencies recorded at the scalp (Chen and Bromm 1995 Lesion and PET scan studies
Lesion studies have provided evidence of involvement of parasylvian cortex in pain and temperature sensation. Davison and Schick (1935) Thalamic connectivity
Thalamic connectivity links parasylvian areas to pain-signaling pathways. Cells responding to painful stimulation are recorded in human thalamic nucleusventralis caudalis (Vc) and in subnuclei of Vc parvocellularis (Vcpc) and Vc portae (Vcpor) (Lenz et al. 1993b Functional significance of parasylvian LEPs
The functional significance of pain-related activity in the parietal operculum and insula is suggested by studies demonstrating that lesions of these structures (Biemond 1956
INTRODUCTION
Abstract
Introduction
Methods
Results
Discussion
References
; Coghill et al. 1994; Talbot et al. 1991). Human lesion studies demonstrate that lesions of the parietal operculum and insula cortex modify the sensation of experimental pain (Biemond 1956; Davison and Schick 1935; Greenspan et al. 1997; Obrador et al. 1957). Although this indirect evidence suggests that parasylvian structures mediate pain sensations, there is no direct evidence of nociceptive inputs to these structures in man.
; Kunde and Treede 1993; Miyazaki et al. 1994; Tarkka and Treede 1993; Treede et al. 1988), which produces pain by activation of A
and C nociceptors (Bromm and Treede 1984; Carmon et al. 1978). The generators of these potentials are uncertain because the location of potentials recorded at the scalp depends on the complicated configuration of the generator and of the surrounding brain, cerebrospinal fluid, dura, bone, and scalp (Scherg and Picton 1991). These potentials may be explained, in part, by models that include generators in the parasylvian cortex bilaterally (Chen and Bromm 1995; Kitamura et al. 1995; Tarkka and Treede 1993). We now describe LEPs recorded from subdural electrodes over the parietal operculum; these LEPs provide the first direct evidence of nociceptive inputs to parasylvian cortex in man. Some of these results have been reported previously as an abstract (Rios et al. 1997).
METHODS
Abstract
Introduction
Methods
Results
Discussion
References
). Therefore potential differences between results recorded from the dominant and nondominant hemispheres cannot be assessed from these results (Coghill et al. 1997). Scalp LEPs were studied in four other patients (1 man, 3 women, ages 33-43 yr) during seizure monitoring. All patients had normal magnetic resonance imaging (MRI) scans and normal somatosensory testing (Lenz et al. 1993b), and none had had previous intracranial surgery. This and the lack of neurological abnormalities apart from epilepsy in patients with temporal lobe epilepsy (Adams and Victor 1984) argues that the present results may apply to normal subjects. All studies were carried out at the Johns Hopkins Hospital. The protocol was approved by the Joint Committee on Clinical Investigation of the Johns Hopkins University, and all patients signed an informed consent for these studies.
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FIG. 3.
Peak amplitude percent distribution of N2 and P2 components after contralateral facial laser stimulation in 3 patients with subdural electrodes over the left fronto-temporal areas. For each patient, the subdural electrode with the largest amplitude for each component (N2 and P2) was identified and selected as the maximum. Each circle represents electrode position over the lateral fronto-temporal cortex. Size of the circle indicates the size of the potential relative to the maximum, and shading within the circle indicates the sensory and motor effect of stimulation as listed in the figure. Pure sensory effects were not evoked by stimulation in this patient. CS, central sulcus; LS, lateral (sylvian) sulcus; STG, superior temporal gyrus.
; Carmon et al. 1978). To avoid sensitization, the laser beam was moved at random to a slightly different position for each stimulus. The stimulus was applied to the dorsum of each hand and over the V2/V3 distribution on each side of the face, at random intervals of between 5 and 7 s. During the entire recording session, continuous white noise was delivered to each ear through earphones (click-tone module, Grass Instruments, Quincy, MA).
). Laser-evoked potentials were recorded from 30 to 40 subdural electrodes, referenced to a frontal subdural electrode (Fig. 2, R), which was distant from the LEP maximum and from areas of ictal and interictal epileptiform activity on the electroencephalogram (EEG).
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FIG. 2.
Topographical representation of LEPs over the left parasylvian area (patient H) recorded from subdural electrodes. Electrodes were referenced to an electrode over the right frontal area (labeled R). Each waveform represents an average of 50 trials. Traces are of 500-ms duration; the vertical line on each trace is at 150 ms. Anatomic locations of electrodes are indicated by dots to the left of the trace (see METHODS). Large dots indicate electrodes where stimulation was carried out, and small dots indicate areas where stimulation was not carried out. Electrodes where cortical stimulation evoked motor or sensory effects are shown.
). Recordings referenced to linked ears were obtained for electrode positions Cz, which was located over the vertex (Cz), and C3/C4 at points 40% of the distance from the vertex to the preauricular point on left (C3) and the right (C4). In each patient studied, results were recorded from two hemispheres (referential recordings from C3 and C4) in response to contralateral stimulation, or from the vertex (Cz) in response to stimulation of either side of the body. EEG recordings were obtained with standard amplifiers (Grass Model 12, band-pass: 0.1-100 Hz, amplifier gain: 5,000). Electrode impedances were maintained at <20 k
for subdural electrodes and <5 k for scalp electrodes.
and - - -). Peak latencies and amplitudes of each component were measured from the maximum potential (Fig. 2). Peak amplitudes were measured from an averaged baseline (0-50 ms) to peak. Peak latencies were measured from the peak amplitude for each component. In describing LEPs in the present results and in the literature (Beydoun et al. 1993; Chen and Bromm 1995; Kitamura et al. 1995; Kunde and Treede 1993; Tarkka and Treede 1993), we will refer to the largest negative wave as N2 and to the largest positive wave as P2.
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FIG. 1.
Laser-evoked potentials (LEPs) recorded from scalp and subdural electrodes. A: LEPs recorded from scalp electrodes in response to stimulation of the right side of the face, referenced to linked ears. B: maximum subdural LEPs from stimulation of the ipsilateral and contralateral face (V2/V3 distribution). C: maximum subdural LEPs from stimulation of the dorsum of the hand. Subdural recordings (B and C) show the maximum from patient H (see Fig. 2) referenced to a subdural electrode (R in Fig. 2). Sweeps are of 500-ms duration. To establish reproducibility 2 waveforms ( and - - -), each representing an average of 15-25 trials, are shown for each potential. Negative, up.
). Briefly, pulses of duration 0.3 ms and alternating polarity at 50 pulses/s were applied across pairs of adjacent electrodes in trains of 2- to 5-s duration. This technique produced excitation beneath both of the stimulated electrodes in a pair (Ranck 1975).
RESULTS
Abstract
Introduction
Methods
Results
Discussion
References
View this table:
TABLE 1.
Scalp and subdural mean peak latencies and amplitudes of LEPS after stimulation of face (V2/V3 distribution) and dorsum of the hands
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FIG. 5.
Peak amplitude percent distribution of N2 and P2 components after contralateral hand laser stimulation in 2 patients with subdural electrodes over the left fronto-temporal areas. Other conventions as for Fig. 3.
; Woolsey et al. 1979). At this site, N2 and P2 potentials evoked by stimulation of the hand and face were 10 and 50%, respectively, of the corresponding potentials recorded at the maximum, which was located inferiorly.
). Compared with the subdural LEPs, scalp LEPs after facial stimulation showed longer latency N2 waves and shorter latency P2 waves (see preceding text). Scalp recordings were not made in the patients with grids because of the risk of infection if electrodes were applied to the scalp near the incision.
; Woolsey et al. 1979). The absence of pain evoked by cortical stimulation was consistent with the description of pain processing as a distributed cortical process (Casey et al. 1994; Coghill et al. 1994, 1997; Jones et al. 1991; Talbot et al. 1991), so that stimulation at any individual cortical site might not be expected to evoke pain. Alternatively, pain may not have been evoked because the location of cortex showing pain-related activity is deep in the sylvian fissure or interhemispheric fissure [PET studies and Lenz et al. (1998)] and thus inaccessible to stimulation from the surface (Penfield and Rasmussen 1955; Ranck 1975). Maximal amplitudes for the N2 potential from stimulation of the contralateral face occurred at precentral, postcentral, and parasylvian areas, at or adjacent to the sites where facial sensory or motor effects were evoked by stimulation (Fig. 3). In patient H, the LEP distribution was located superior and anterior to a greater extent than was the case for patient P, whereas in patient C, the LEP distribution was located inferior to that for patient P. In general, maximal amplitudes occurred over face sensorimotor areas.
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FIG. 4.
Peak amplitude percent distribution of N2 and P2 potentials evoked by ipsilateral facial stimulation in 3 patients with subdural electrodes over the left fronto-temporal areas. Other conventions as for Fig. 3.
; Woolsey et al. 1979), even given the variability of such maps (Uematsu et al. 1992).
DISCUSSION
Abstract
Introduction
Methods
Results
Discussion
References
; Woolsey et al. 1979; cf. Uematsu et al. 1992). Short-duration cutaneous stimulation with a CO2 laser has been shown to evoke cerebral potentials due to activation of cutaneous nociceptors (Bromm and Treede 1984; Carmon et al. 1978). The cortical distributions of these subdural potentials suggest that their generators are located in the parietal operculum or in the insula, or in both, consistent with previous PET, magnetoencephalographic, and scalp LEP source analyses. Because interpretation of these previous studies incorporates multiple assumptions, the present results are the first demonstration of direct nociceptive inputs to human parasylvian cortex.
; Tarkka and Treede 1993). The published literature includes a wide range of latencies for the N2 (145-181 ms) and P2 (335-390 ms) potentials recorded at the scalp (Beydoun et al. 1993; Kunde and Treede 1993; Miyazaki et al. 1994; Tarkka and Treede 1993; Treede et al. 1988). Both latency and amplitude of these potentials show a large intersubject variability (Beydoun et al. 1993; Kazarians et al. 1995). Thus intersubject variability may account for the differences between LEP latency recorded from subdural and scalp electrodes because these potentials are reported in different patients (see RESULTS, Subdural electrode recordings).
) could result in projection of the potential to a point on the cortical surface distant from the actual generator (Lesser et al. 1987) (see Fig. 4, patient C, N2). The large local gradient seen in Figs. 2 and 3 is consistent with a generator in the parietal operculum because this pattern might not be expected from the deeper (insular) generator or from generators located in both the parietal operculum and the insula. However, our current analysis cannot distinguish either the depth or the identity of the generator (Scherg and Picton 1991).
; Zaslansky et al. 1995, 1996). The P300 is a potential reflecting the "amount of attention paid to an event, in the certainty with which it is expected, the surprise which it elicits or in the clarity with which it is perceived" (Picton 1992; Sommer and Matt 1990). Previous studies demonstrate that LEPs are decreased during distraction (Becker et al. 1993; Kanda et al. 1996; Miltner et al. 1989; Seidenberg and Treede 1996; Towell and Boyd 1993; Zaslansky et al. 1995, 1996), although the attention-dependent component of LEPs may occur at a latency different from that of P2 (Lorenz 1997). Therefore the variability of the present results might arise, in part, from this variable cognitive component, which is not addressed in the present results.
reported on a patient (case 11) who developed hemi-hypesthesia and hemi-hypalgesia after an ischemic stroke involving the insula, anterior parietal operculum, and the postcentral gyrus. Biemond (1956) reported similar sensory loss after a lesion of the insula and the anterior parietal operculum (case 1) and after a lesion of the insula and the parietal operculum starting at the postcentral gyrus (case 3). Obrador (Obrador et al. 1957) described similar sensory loss in a patient with a lesion of the insula sparing all other cortical structures. In a recent report, elevated pain thresholds to mechanical, heat, and cold stimuli were described in a patient with compression of the retro-insula and the parietal operculum (Greenspan and Winfield 1992). These deficits resolved after removal of the tumor and resolution of the mass effect. The most detailed recent study reported sensory deficits occurring in six patients with parasylvian lesions, as defined by gyral analysis of the MRI scans (Greenspan et al. 1997). Patients with lesions of the parietal operculum but not those with lesions of the insula had decreased discrimination of painful stimuli (Greenspan et al. 1997). Decreased unpleasantness (Berthier et al. 1988) or motivation to escape from painful stimuli (Greenspan et al. 1997) associated with experimental pain is reported in series of parasylvian lesions identified by CT (Berthier et al. 1988) or MRI scans (Greenspan et al. 1997). These studies suggest that lesions of parietal operculum and insula are associated, respectively, with deficits of discriminative (Greenspan et al. 1997) and motivational-affective dimension of pain (Berthier et al. 1988; Greenspan et al. 1997).
), none of these structures was activated. Graded noxious stimulation is correlated with increasing blood flow activation and with increased pain ratings for anterior and posterior insula, parietal operculum, and medial temporal cortex (Coghill et al. 1997). Finally, the location of cortical generators in parasylvian structures bilaterally is suggested by magnetoencephalography (MEG), which demonstrates current flow in parasylvian cortex in response to cutaneous laser stimulation (Kakigi et al. 1995; Kitamura et al. 1995) or other noxious stimuli (Hari et al. 1983; Huttunen et al. 1986). In summary, the present results are consistent with activation of insula and parietal operculum bilaterally by painful stimuli and with disability of pain sensation after lesions of the parietal operculum and insula.
) are consistent with the suggestion that the N2 is a cortical wave evoked by direct transmission of the laser-evoked afferent volley to cortex. The cutaneous laser stimulus evokes a pure pain sensation due to selective activation of cutaneous A nociceptors (Bromm and Treede 1984; Carmon et al. 1978). Estimated latencies for the onset of the N2 (~50 ms before the peak) attributable to direct conduction from the hand (Fig. 1C) are in good agreement with measured latencies. Latency of N2 conduction from the hand can be estimated from 40-ms receptor activation time (Bromm and Treede 1984), 100-ms conduction delay in the peripheral nerve (A fibers, 8-12 m/s) (Beydoun et al. 1997; Kakigi et al. 1991; Kenton et al. 1980), and 30-ms conduction delay through the STT (8-10 m/s) (Kakigi and Shibasaki 1991). Thus the N2 of the LEP may represent the cortical response evoked by the afferent volley resulting from the laser stimulus.
; Robinson and Burton 1980a,b; Woolsey et al. 1979). LEP generators in the insula or parietal operculum are consistent with the failure of cortical stimulation to evoke pain (Erickson et al. 1952; Penfield and Rasmussen 1955; Woolsey et al. 1979). Stimulation of the surface of the hemisphere would not be expected to activate these deep structures (Penfield and Rasmussen 1955; Ranck 1975) even if electrical stimulation applied within these structures evokes pain (Price and Dubner 1977).
; Kenshalo et al. 1988), parietal operculum, and insula (Dong et al. 1978, 1989, 1994; Dostrovsky and Craig 1996a; Robinson and Burton 1980a) contain cells that respond to noxious inputs. Intracortical potentials evoked by tooth pulp stimulation (Chudler et al. 1985) are maximal over the parietal operculum just posterior to the central sulcus (see Fig. 3 in Chudler et al. 1986). Finally, lesions of SI reduce the ability of monkeys to discriminate painful stimuli (Kenshalo et al. 1991).
, 1994b) and ventral medial posterior (VMpo) (Dostrovsky et al. 1996b). Studies of patients at autopsy after lesions of the STT show that the human STT terminates in Vc (Bowsher 1957; Mehler 1962, 1966; Mehler et al. 1960; Walker 1943), Vcpor (Mehler 1966), and Vcpc (Mehler 1966). A recent study shows that thalamic nucleus Vmpo receives lamina I STT input in monkeys (Craig et al. 1994). In humans, this region displays a pattern of calcium binding protein staining similar to that found in the region of monkey thalamus where STT terminates and where many cells respond to noxious and cold stimuli (Craig et al. 1994). Stimulation in these nuclei can produce somatic pain (Dostrovsky et al. 1991, 1996b; Halliday and Logue 1972; Hassler and Reichert 1959; Lenz et al. 1993a, 1995), visceral pain (Davis et al. 1995; Lenz et al. 1994a) and memories of previously experienced pain (Davis et al. 1995; Lenz et al. 1994a, 1995). Cortical connections of Vc, Vcpor, and Vcpc have been studied using silver stain (degeneration) techniques at autopsy in patients with thalamic lesions (Van Buren and Borke 1972). This material indicates that Vc projects to SI and SII (Van Buren and Borke 1972), Vcpc projects to anterior insular cortex (Van Buren and Borke 1972), and Vcpor to the inferior parietal lobule, including the parietal operculum and SII (Van Buren and Borke 1972). In summary, anatomic studies demonstrate connections between human parasylvian cortical structures and thalamic nuclei that show pain-related activity.
). Cells in VP, VPI, pulvinar oralis, and VMpo respond to noxious stimulation (Apkarian and Shi 1994; Bushnell and Duncan 1987; Bushnell et al. 1993; Casey 1966; Casey and Morrow 1983; Chung et al. 1986; Craig et al. 1994; Kenshalo et al. 1980; Morrow and Casey 1992; Perl and Whitlock 1961). VP projects to SI and SII cortex (Burton 1986; Jones 1985; Kenshalo and Willis 1991), whereas VPI projects to SII and insular dysgranular cortex (Burton and Jones 1976; Friedman and Murray 1986). The posterior nuclear group projects widely to parasylvian structures (Burton 1986; Burton and Jones 1976). Medial and oral division of pulvinar, corresponding to human Vcpor (Hirai and Jones 1989), project to 7b (Burton 1986; Burton and Jones 1976). VMpo projects to anterior dorsal insula at the level of the central sulcus (Craig 1995). These monkey studies suggest that parasylvian cortical structures are involved in pain-related activity through input from thalamic nuclei corresponding to human Vc, Vcpc, Vcpor, and Vmpo.
; Davison and Schick 1935; Greenspan et al. 1997; Obrador et al. 1957), and specifically lesions of the parietal operculum (Greenspan et al. 1997), disable the discriminative aspect of pain. Lesions of the insula are associated with decreased unpleasantness of painful stimuli (Berthier et al. 1988) or decreased motivation to escape from painful stimuli (Greenspan et al. 1997). Stimulation of Vc, Vcpc, and Vcpor can reproduce pain associated with a strong emotional or affective dimension (Davis et al. 1995; Lenz et al. 1994a, 1995, 1997) in patients with prior experience of such pain (Lenz et al. 1997). Stimulation of parasylvian cortex can reproduce sensory experience and the affective tone associated with the original experience (Penfield and Perot 1963). These results suggest that the coupling of pain and a strong affective component is conditioned by the prior experience of pain through corticolimbic connections (Mishkin 1979). The processing of nociceptive signals in the parietal operculum and insula shares many characteristics with the inferior temporal cortex, which is involved in visual memory through corticolimbic connections (see Lenz et al. 1997; Mishkin 1979). Therefore parietal operculum may be involved in the learned component or memory of the affective dimension of pain through corticolimbic connections. The present results suggest that the involvement of human parasylvian structures in the sensory and affective dimensions of pain occurs through a mechanism including direct nociceptive input to these structures.
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ACKNOWLEDGEMENTS |
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We thank Drs. S. Breiter, N. Crone, and B. Gordon for assistance with radiological studies and D. Jackson for technical assistance.
This work was supported by grants to F. A. Lenz from the Eli Lilly Corporation and National Institute of Neurological Disorders and Stroke Grants NS-28598, K08 NS-01384, and P01 NS-32386-Proj. 1.
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FOOTNOTES |
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Address for reprint requests: F. A. Lenz, Dept. of Neurosurgery, Meyer Bldg. 7-113, Johns Hopkins Hospital, 600 N. Wolfe St., Baltimore, MD 21287-7713.
Received 5 March 1998; accepted in final form 29 June 1998.
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REFERENCES |
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Abstract
Introduction
Methods
Results
Discussion
References
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