Neuronal mechanisms of nociceptive-evoked gamma-band oscillations in rodents

Lupeng Yue; Chongyu Bao; Libo Zhang; Fengrui Zhang; Wenqian Zhou; Gian Domenico Iannetti; Li Hu

doi:10.1016/j.neuron.2024.12.011

Neuronal mechanisms of nociceptive-evoked gamma-band oscillations in rodents

Neuron. 2025 Jan 9:S0896-6273(24)00910-3. doi: 10.1016/j.neuron.2024.12.011. Online ahead of print.

Authors

Lupeng Yue¹, Chongyu Bao², Libo Zhang¹, Fengrui Zhang¹, Wenqian Zhou¹, Gian Domenico Iannetti³, Li Hu⁴

Affiliations

¹ State Key Laboratory of Cognitive Science and Mental Health, Institute of Psychology, Chinese Academy of Sciences, Beijing, China; Department of Psychology, University of Chinese Academy of Sciences, Beijing, China.
² State Key Laboratory of Cognitive Science and Mental Health, Institute of Psychology, Chinese Academy of Sciences, Beijing, China; Department of Psychology, University of Chinese Academy of Sciences, Beijing, China; Center for Excellence in Brain Science and Intelligence Technology, Chinese Academy of Sciences, Shanghai, China.
³ Neuroscience and Behaviour Laboratory, Italian Institute of Technology, Rome, Italy; Department of Neuroscience, Physiology, and Pharmacology, University College London, London, UK.
⁴ State Key Laboratory of Cognitive Science and Mental Health, Institute of Psychology, Chinese Academy of Sciences, Beijing, China; Department of Psychology, University of Chinese Academy of Sciences, Beijing, China. Electronic address: [email protected].

PMID: 39809278
DOI: 10.1016/j.neuron.2024.12.011

Abstract

Gamma-band oscillations (GBOs) in the primary somatosensory cortex (S1) play key roles in nociceptive processing. Yet, one crucial question remains unaddressed: what neuronal mechanisms underlie nociceptive-evoked GBOs? Here, we addressed this question using a range of somatosensory stimuli (nociceptive and non-nociceptive), neural recording techniques (electroencephalography in humans and silicon probes and calcium imaging in rodents), and optogenetics (alone or simultaneously with electrophysiology in mice). We found that (1) GBOs encoded pain intensity independent of stimulus intensity in humans, (2) GBOs in S1 encoded pain intensity and were triggered by spiking of S1 interneurons, (3) parvalbumin (PV)-positive interneurons preferentially tracked pain intensity, and critically, (4) PV S1 interneurons causally modulated GBOs and pain-related behaviors for both thermal and mechanical pain. These findings provide causal evidence that nociceptive-evoked GBOs preferentially encoding pain intensity are generated by PV interneurons in S1, thereby laying a solid foundation for developing GBO-based targeted pain therapies.

Keywords: calcium imaging; electrophysiological recording; gamma-band oscillations; neuronal encoding; optogenetics; pain; parvalbumin-positive interneurons; primary somatosensory cortex.