Delta and gamma oscillations in operculo-insular cortex underlie innocuous cold thermosensation

Author:

Fardo Francesca123,Vinding Mikkel C.34,Allen Micah56,Jensen Troels Staehelin17,Finnerup Nanna Brix1

Affiliation:

1. Danish Pain Centre, Department of Clinical Medicine, Aarhus University, Aarhus, Denmark;

2. Interacting Minds Centre, Aarhus University, Aarhus, Denmark;

3. Center of Functionally Integrative Neuroscience, Aarhus University, Aarhus, Denmark;

4. Swedish National Facility for Magnetoencephalography, Department of Clinical Neuroscience, Karolinska Institutet, Stockholm, Sweden;

5. Wellcome Trust Center for Neuroimaging, University College London, London, United Kingdom;

6. Institute of Cognitive Neuroscience, University College London, London, United Kingdom; and

7. Department of Neurology, Aarhus University Hospital, Aarhus, Denmark

Abstract

Cold-sensitive and nociceptive neural pathways interact to shape the quality and intensity of thermal and pain perception. Yet the central processing of cold thermosensation in the human brain has not been extensively studied. Here, we used magnetoencephalography and EEG in healthy volunteers to investigate the time course (evoked fields and potentials) and oscillatory activity associated with the perception of cold temperature changes. Nonnoxious cold stimuli consisting of Δ3°C and Δ5°C decrements from an adapting temperature of 35°C were delivered on the dorsum of the left hand via a contact thermode. Cold-evoked fields peaked at around 240 and 500 ms, at peak latencies similar to the N1 and P2 cold-evoked potentials. Importantly, cold-related changes in oscillatory power indicated that innocuous thermosensation is mediated by oscillatory activity in the range of delta (1–4 Hz) and gamma (55–90 Hz) rhythms, originating in operculo-insular cortical regions. We suggest that delta rhythms coordinate functional integration between operculo-insular and frontoparietal regions, while gamma rhythms reflect local sensory processing in operculo-insular areas. NEW & NOTEWORTHY Using magnetoencephalography, we identified spatiotemporal features of central cold processing, with respect to the time course, oscillatory profile, and neural generators of cold-evoked responses in healthy human volunteers. Cold thermosensation was associated with low- and high-frequency oscillatory rhythms, both originating in operculo-insular regions. These results support further investigations of central cold processing using magnetoencephalography or EEG and the clinical utility of cold-evoked potentials for neurophysiological assessment of cold-related small-fiber function and damage.

Funder

Novo Nordisk Foundation

Wellcome Trust

Det Frie Forskningsråd (Danish Council for Independent Research)

Publisher

American Physiological Society

Subject

Physiology,General Neuroscience

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