Imaging studies indicate that experimental pain is processed in multiple cortical areas which are often characterized as a network. However, the functional connectivity within the network and the other properties of the network is poorly understood. Substantial evidence demonstrates that synchronous oscillations between two cortical areas may indicate functional connectivity between those areas. We test the hypothesis that cortical areas with pain-related activity are functionally connected during attention to a painful stimulus. We stimulated with a painful, cutaneous, laser stimulus and recorded the response directly from the cortical surface (electrocorticography--ECoG) over primary somatosensory (SI), parasylvian (PS), and medial frontal (MF) cortex through subdural electrodes implanted for treatment of epilepsy. The results demonstrate synchrony of ECoGs between cortical structures receiving input from nociceptors, as indicated by the occurrence of laser-evoked potentials (LEPs) and/or event-related desynchronization (ERD). Prior to the stimulus, directed attention to the painful stimulus consistently increased the degree of synchrony between SI and PS regions, as the subject anticipated the stimulus. After the laser stimulus, directed attention to the painful stimulus consistently increased the degree of synchrony between SI and MF cortex, as the subject responded by counting the stimulus. Therefore, attention to painful stimuli always enhanced synchrony between cortical pain-related structures. The pattern of this synchrony changed as the patient switched tasks from anticipation of the stimulus to counting the stimulus. These results are the first compelling evidence of pain networks characterized by rapidly switching, task-specific functional connectivity.
Intensity encoding of painful stimuli in many brain regions has been suggested by imaging studies which cannot measure electrical activity of the brain directly. We have now examined the effect of laser stimulus intensity (three energy levels) on laser evoked potentials (LEPs) recorded directly from the human primary somatosensory (SI), parasylvian, and medial frontal cortical surfaces through subdural electrodes implanted for surgical treatment of medically intractable epilepsy. LEP N2* (early exogenous/stimulus-related potential) and LEP P2** (later endogenous potential) amplitudes were significantly related to the laser energy levels in all regions, although differences between regions were not significant. Both LEP peaks were also significantly correlated with the pain intensity evoked by the laser stimulus, excepting N2* over the parasylvian region. Peak latencies of both LEP peaks were independent of laser energy levels. N2* and P2** amplitudes of the maxima in all regions showed significant positive linear correlations with laser energy, excepting N2* over the parasylvian region. The lack of correlation of parasylvian cortical N2* with laser energy and pain intensity may be due to the unique anatomy of this region, or the small sample, rather than the lack of activation by the laser. Differences in thresholds of the energy correlation with amplitudes were not significant between regions. These results suggest that both exogenous in endogenous potentials evoked by painful stimuli, and recorded over SI, parasylvian, and medial frontal cortex of awake humans, encode the intensity of painful stimuli and correlate with the pain evoked by painful stimuli.
Negative and positive laser evoked potential (LEP) peaks (N2*, P2**) were simultaneously recorded from the primary somatosensory (SI), parasylvian, and medial frontal (MF: anterior cingulate and supplementary motor area) cortical surfaces through subdural electrodes implanted for the surgical treatment of intractable epilepsy. Distribution of the LEP N2* and P2** peaks was estimated to be in cortical areas (SI, parasylvian, and MF) identified by anatomic criteria, by their response to innocuous vibratory stimulation of a finger (v-SEP), and to electrical stimulation of the median nerve (e-SEP). The maximum of the LEP N2* peak was located on the CS, medial (dorsal) to the finger motor area, as determined by cortical stimulation, and to the finger somatosensory area, as determined from the e-SEP and v-SEP. This finding suggests that the generator source of the LEP N2* peak in SI was different from that of e-SEP or v-SEP in Brodmann's areas 3b or 1. In parasylvian and MF, polarity reversal was often observed, indicating tangential current sources in these regions. In contrast to e-SEP and v-SEP, the LEP N2* latency over SI was not shorter than that over the parasylvian region. The amplitude of N2* was larger over SI than over MF and the latencies of the LEP peaks in those 2 regions were different. These findings provide evidence for a significant LEP generator in the postcentral gyrus, perhaps SI cortex, that is situated outside the tactile homunculus in SI and that receives its input arising from nociceptors simultaneously with parasylvian and MF cortex.
We explored the region of human thalamic somatic sensory nucleus (ventral caudal, Vc), corresponding to monkey ventral posterior (VP), with threshold microstimulation (TMIS) during stereotactic procedures for the treatment of tremor. Of 122 sites in 116 patients (124 thalami) where mechanical (touch, pressure, and sharp) or movement [movement through the body (movement) and vibration] sensations were evoked, 72 sites were found in the core or in adjacent regions, posterior-inferior (33), inferior (4), and posterior to the core (13). Sites where TMIS evoked touch were less frequently found in the core than those where movement or pressure sensations were evoked. Pressure was more commonly (P < 0.05) evoked than vibration at sites where cells had intraoral receptive fields (RFs). Touch and vibration were more commonly (P < 0.05) evoked than pressure at sites where cells had facial RFs, consistent with the relative density of rapidly adapting (RA) receptors in the mouth and face. Sites described as deep and movement were found superior and anterior in the core, consistent with the location of cells responding to stimulation of muscle afferents. At 72 of 122 sites, TMIS evoked the same sensation at two or more sites in the same plane. Of these sites, 58 are adjacent to each other, in a cluster, consistent with studies of the localization of cells responding to different modalities. These results demonstrate that mechanical and movement sensations can be evoked by stimulation in the region of Vc. The characteristics of these sites suggest that the sensations are evoked by stimulation of pathways specific to cutaneous and deep mechanoreceptors.
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