Abstract
Salient nociceptive and non-nociceptive stimuli elicit low-frequency local field potentials (LFPs) in the human insula. Nociceptive stimuli also elicit insular gamma-band oscillations (GBOs), possibly preferential for thermonociception, which have been suggested to reflect the intensity of perceived pain. To shed light on the functional significance of these two responses, we investigated whether they would be modulated by stimulation intensity and temporal expectation – two factors contributing to stimulus saliency. Insular activity was recorded from 8 depth electrodes (41 contacts) implanted in the left insula of 6 patients investigated for epilepsy. Thermonociceptive, vibrotactile, and auditory stimuli were delivered using two intensities. To investigate the effects of temporal expectation, the stimuli were delivered in trains of three identical stimuli (S1-S2-S3) separated by a constant 1-s interval. Stimulation intensity affected intensity of perception, the magnitude of low-frequency LFPs, and the magnitude of nociceptive GBOs. Stimulus repetition did not affect perception. In contrast, both low-frequency LFPs and nociceptive GBOs showed a marked habituation of the responses to S2 and S3 as compared to S1 and, hence, a dissociation with intensity of perception. Most importantly, although insular nociceptive GBOs appear to be preferential for thermonociception, they cannot be considered as a correlate of perceived pain.
Highlights
Thermal nociceptive stimuli elicit robust low-frequency phase-locked local field potentials (LFPs) in the human insula[1,2,3,4], which are often assumed to reflect early stages of cortical processing related to nociception and to the perception of pain[2,3]
With previous studies[1,8], all three types of stimuli elicited robust low-frequency phase-locked LFPs in the insula. In addition to these low-frequency responses, nociceptive stimuli, but not non-nociceptive vibrotactile and auditory stimuli, elicited a marked enhancement of gamma-band oscillations (GBOs) at the same insular locations. This result is consistent with our recent finding that GBOs preferential for nociception can be recorded from the human insula[8], and that low-frequency phase-locked LFPs are dissociated from GBOs recorded at the same insular locations
Stimulation intensity modulated the intensity of perception, as well as the magnitude of both low-frequency phase-locked LFPs and nociceptive GBOs recorded from the human insula
Summary
Thermal nociceptive stimuli elicit robust low-frequency phase-locked local field potentials (LFPs) in the human insula[1,2,3,4], which are often assumed to reflect early stages of cortical processing related to nociception and to the perception of pain[2,3] Contrasting with this assumption, we recently observed that intense but non-nociceptive and non-painful tactile, auditory, and visual stimuli elicit similar low-frequency phase-locked LFPs at the same insular locations[1]. Because this response habituation is not necessarily paralleled by a reduction in the intensity of perception, this can lead to a marked dissociation between the magnitude of these event-related potentials and perception[13] From these phase-locked responses, GBOs elicited by thermonociceptive stimuli over the human primary somatosensory cortex (SI) have been suggested to not habituate when stimuli are presented at a constant and predictable ISI18, indicating that these high-frequency activities might reflect processes more directly related to the perception of pain and/or the strength of the eliciting sensory input. At the end of each block, participants were asked to report whether they had perceived the stimuli as painful
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