Neurophysiologie clinique = Clinical neurophysiology
2025 Jan 30;55(3):103056. doi: 10.1016/j.neucli.2025.103056. Online ahead of print.

Raíssa Benocci ThibesPedro Henrique Martins da CunhaJorge Dornellys da Silva LapaLiu DongyangDenise Spinola PinheiroRicardo Ferrareto IglesioKleber Paiva DuarteValquiria Aparecida SilvaGabriel Taricani KubotaManoel Jacobsen TeixeiraLuis Garcia-LarreaHélène BastijiJoão Ricardo SatoDaniel Ciampi de Andrade

Abstract

Background and objectives: The activity profile of the posterior insula in neuropathic pain (NeP) remains largely unexplored. To address this and examine its modulation by somatosensory stimulation, we recorded local field potentials (LFP) in awake patients with NeP undergoing deep brain stimulation (DBS) electrode implantation to the posterior-superior insula (PSI) for analgesic purposes.

Materials and methods: Six patients (one woman; 32-45 years), experiencing refractory peripheral NeP and having previously responded to non-invasive stimulation of the PSI underwent stereotactic implantation of DBS electrodes to the PSI as part of a phase II clinical trial. The averaged power of frequencies of LFP and their peaks were calculated during rest and under thermal painful and mechanical non-painful stimulation.

Results: At rest, amplitude peaks within the delta (average min-max.: 2.2 Hz; 1.3-3.7) and theta (6.1 Hz, varying between 5.7 and 6.8 Hz) bands were identified. Compared to rest, both tonic thermal painful, and mechanical non-painful stimulation led to similar mean decreases in gamma power (-24.46 ± 70.56, and -19.56 ± 3.08; respectively). Painful stimuli caused an increase in all the other frequency bands, mainly in alpha and beta ranges, while non-painful stimulation led to decreases in power in all frequencies above 4Hz. Painful tonic stimulation was associated with a significantly greater power variability, both in amplitude and frequency, compared to nonpainful mechanical stimulation.

Conclusion: The posterior insula resting state activity in awake patients with chronic NeP was characterized by predominant theta oscillations. Painful and innocuous stimulation led to opposite spectral changes, with a much larger variability across the whole frequency spectrum for painful stimuli, relative to both resting state and non-painful stimulation.

Keywords: Chronic pain; Deep brain stimulation; Electroencephalogram; Insula; Local field potential; Neuromodulation; Neuropathic pain; Oscillation; Peripheral neuropathy; Theta band.

Intraoperative recordings from the posterior superior insula in awake humans with peripheral neuropathic pain