Stimulus-evoked gamma-band oscillations recorded from the human insula may reflect early and nociceptive-specific stages of cortical processing

Abstract

Introduction. Gamma-band oscillations (GBOs, 30-100 Hz) are considered to represent a mechanism for integrating low-level cortical processing of basic stimulus features with high-level cognitive processes. Several studies have shown that nociceptive stimuli elicit a transient enhancement of GBOs in the primary somatosensory (SI) and motor (MI) cortices whose magnitude relates to perceived pain intensity. GBOs may therefore constitute a specific and clinically relevant biomarker for the perception of pain. To this date, no study has ever investigated the presence of GBOs in the insula, a region considered to have a major role in pain representation. Aims. Using direct intracerebral recordings performed in humans, we investigate whether nociceptive stimulation elicits nociceptive-specific GBOs in the anterior and posterior insula. Methods. Six patients with deep multicontact electrodes implanted for the presurgical evaluation of focal epilepsy took part in the study. Insular activity was recorded from a total of 62 insular contacts. Patients received stimuli belonging to each of the following four sensory modalities: nociceptive somatosensory, non-nociceptive somatosensory, auditory, and visual. Results. In all patients, nociceptive stimuli consistently elicited GBOs at one or more insular electrodes, but not at other cortical and subcortical locations. In contrast, non-nociceptive somatosensory, auditory, and visual stimuli did not elicit such high frequency activities at any of the recorded contacts. Conclusions. Nociceptive stimuli elicit consistent GBOs in the insula. Because non-nociceptive stimuli do not elicit a similar response, these responses could reflect activity specific for nociception, possibly involved in the integration of stimulus-driven and top-down determinants of pain perception