Elsevier

Clinical Neurophysiology

Volume 110, Issue 1, January 1999, Pages 133-145
Clinical Neurophysiology

Intracortical recordings of early pain-related CO2-laser evoked potentials in the human second somatosensory (SII) area

https://doi.org/10.1016/S0168-5597(98)00054-9Get rights and content

Abstract

We studied responses of the parieto-frontal opercular cortex to CO2-laser stimulation of Aδ fiber endings, as recorded by intra-cortical electrodes during stereotactic-EEG (SEEG) presurgical assessment of patients with drug-resistant temporal lobe epilepsy. After CO2-laser stimulation of the skin at the dorsum of the hand, we consistently recorded in the upper bank of the sylvian fissure contralateral to stimulation, a negative response at a latency of 135±18 ms (N140), followed by a positivity peaking around 171±22 ms (P170). The stereotactic coordinates in the Talairach's atlas of the electrode contacts recording these early responses covered the pre- and post-rolandic part of the upper bank of the sylvian fissure (−27<y<+12 mm; 31<x<57 mm; 4<z<23 mm), corresponding to the accepted localization of the SII area in man, possibly including the upper part of the insular cortex. The spatial distribution of these early contralateral responses in the SII-insular cortex fits wit that of the modeled sources of scalp CO2-laser evoked potentials (LEPs) and with PET data from pain activation studies. Moreover, this study showed the likely existence of dipolar sources radial to the scalp surface in SII, which are overlooked in magnetic recordings. Early responses also occurred in the SII area ipsilateral to stimulation peaking 15 ms later than in contralateral SII, suggesting a callosal transmission of nociceptive inputs between the two SII areas. Other pain responsive areas such as the anterior cingulate gyrus, the amygdala and the orbitofrontal cortex did not show early LEPs in the 200 ms post-stimulus. These findings suggest that activation of SII area contralateral to stimulation, possibly through direct thalamocortical projections, represents the first step in the cortical processing of peripheral Aδ fiber pain inputs.

Introduction

Since the early work of Head and Holmes (1911)it has long been accepted that the cerebral cortex is not directly involved in the elaboration of pain sensation. This view was supported by the observation that no pain sensation could be evoked by electrical stimulation of the convexity of the human somatosensory cortex (Penfield and Boldrey, 1937). However, several papers have been published reporting on pain related cortical potentials in healthy volunteers (for a review see Chudler and Dong, 1983, using electrical tooth pulp stimuli (Chatrian et al., 1975; Chapman et al., 1979; Chen et al., 1979), electrical or mechanical skin stimuli (Johnson et al., 1975; Pratt et al., 1979; Bromm and Scharein, 1982; Bromm and Meier, 1984; Buchsbaum, 1984), or chemical stimulation of the nasal mucosa (Kobal, 1984). Moreover, during the past 20 years many studies converged on the conclusion that cortical pain-related potentials and magnetic fields, peaking in the 100–400 ms latency range, are consistently evoked by CO2-laser stimulation of the skin, via input transmission through small myelinated Aδ fibers at the periphery (Mor and Carmon, 1975; Carmon et al., 1980; Treede et al., 1988; Kakigi et al., 1989; Kakigi et al., 1995; Kakigi et al., 1996; Bromm and Treede, 1991; Beydoun et al., 1993; Kunde and Treede, 1993; Tarkka and Treede, 1993; Miyazaki et al., 1994; Bromm and Chen, 1995; Xu et al., 1995; Valeriani et al., 1996). Several studies have shown that brief heat pulses, delivered by a CO2 laser and applied to the skin, activate selectively the endings of small myelinated Aδ and of unmyelinated C fibers (Kakigi et al., 1991b; Bromm and Treede, 1984; Bromm and Treede, 1991), and there is a correlation between the decreased density of small diameter fibers at the periphery and a reduction of the cortical responses to CO2-laser stimulation in patients with peripheral neuropathies (Kakigi et al., 1991a; Kakigi et al., 1992). Moreover, the amplitude reduction of these responses in patients with syringomyelia and the selective loss of pain and temperature sensation suggests that inputs are transmitted to the cortex via the spinothalamic tract (Kakigi et al., 1991c, Treede et al., 1991; Treede et al., 1995).

The earliest scalp response recorded to CO2-laser stimulation is a N1–P1 dipolar potential field at a latency of 150–170 ms; it is followed by a N2–P2 complex in the 200–350 ms latency range. The N1 and P1 maximal voltages are recorded in the temporal region contralateral to stimulation and in the midfrontal region, respectively. N2 is maximal at Cz and spreads in temporo-frontal region ipsi and contralaterally to the stimulation, while P2 is maximal at the vertex and largely distributed over the scalp (Treede et al., 1988; Kakigi et al., 1989; Beydoun et al., 1993; Kunde and Treede, 1993; Tarkka and Treede, 1993; Miyazaki et al., 1994; Xu et al., 1995; Valeriani et al., 1996). Some of these studies attempted to localize the anatomical generators of these responses using dipolar source modeling of scalp recorded EPs, or evoked magnetic fields (EFs) (Kakigi et al., 1989; Kakigi et al., 1995; Kakigi et al., 1996; Tarkka and Treede, 1993; Bromm and Chen, 1995; Valeriani et al., 1996). These studies suggested that the first activated dipolar cortical source of CO2-laser responses is located in the second somatosensory area (SII), showing a maximal activity (dipolar moment) in the latency range of the N1–P1 potential.

In this study, we report on CO2-laser EPs (LEPs) recorded by stereotactically implanted intracortical electrodes carried out during presurgical evaluation of patients with drug refractory partial epilepsy. These recordings were included in the functional cortical mapping procedure and permitted to address the questions: (i) whether the parietal opercular cortex (SII area) responds to painful CO2-laser stimuli in the latency range of the N1–P1 scalp potentials (ii) whether the location of the cortical response is coherent with that of the SII source, as modeled from scalp recorded activity and that of pain activated areas in positron emission studies (PET) and (iii) whether other cortical areas suspected to be involved in the processing of pain sensation show CO2-laser evoked responses in the 200 ms post-stimulus interval.

Section snippets

Patients

We recorded LEPs from 11 patients (22–47 years, mean age 32 years, 6 females, 5 males). During the recording, the patients lay on a couch in a semi-dark room with the instruction to keep their eyes open and to fixate a visual target in front of them. The 11 patients included in this study presented with refractory temporal lobe epilepsy and were investigated using stereotactically implanted intracerebral electrodes before functional surgery (6–15 electrodes per patient). Various cortical

Results

As shown in Fig. 2Fig. 3, the laser stimulus consistently evoked, in the cortex of the upper bank of the sylvian fissure, a negative response at a latency of 135±18 ms (N140), followed by a positivity peaking 171±22 ms (P170) (see Table 1). The amplitude of the N140-P170 deflection was between 4.71 and 30.62 μV (see Table 1). These responses were picked up by all of the 17 electrodes implanted in the parieto-frontal operculum and upper bank of the sylvian fissure. Fig. 4 shows the coordinates

Discussion

The main conclusions of this study are as follows: (i) the earliest response recorded contralaterally to the stimulus, after a CO2-laser stimulation of the dorsum of the hand, is a negative potential at a latency of 140 ms (N140) followed by a positivity at 170 ms (P170) (ii) this early contralateral response is recorded in the cortex of the superior bank of the sylvian fissure, corresponding to the accepted localization of area SII in man and at the upper border between SII and the insular

Acknowledgements

This work was presented at the 14th International Congress of EEG and Clinical Neurophysiology (Florence, August 1997) with the support of an IFCN fellowship (M. Frot) and has been supported by the Programme thématique Neurosciences Region Rhône-Alpes 1997–2000.

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