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Pain-preferential thalamocortical neural dynamics across species

Nature Human Behaviour volume 8, pages 149–163 (2024)Cite this article

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Abstract

Searching for pain-preferential neural activity is essential for understanding and managing pain. Here, we investigated the preferential role of thalamocortical neural dynamics in encoding pain using human neuroimaging and rat electrophysiology across three studies. In study 1, we found that painful stimuli preferentially activated the medial-dorsal (MD) thalamic nucleus and its functional connectivity with the dorsal anterior cingulate cortex (dACC) and insula in two human functional magnetic resonance imaging (fMRI) datasets (n = 399 and n = 25). In study 2, human fMRI and electroencephalography fusion analyses (n = 220) revealed that pain-preferential MD responses were identified 89–295 ms after painful stimuli. In study 3, rat electrophysiology further showed that painful stimuli preferentially activated MD neurons and MD–ACC connectivity. These converging cross-species findings provided evidence for pain-preferential thalamocortical neural dynamics, which could guide future pain evaluation and management strategies.

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Fig. 1: Research questions and design.
Fig. 2: Sensory experiment and fMRI BOLD responses.
Fig. 3: Pain-preferential thalamic responses and thalamocortical connectivity.
Fig. 4: The experimental design and results for controlling salience effects on thalamic BOLD responses.
Fig. 5: EEG time series and decoding performance.
Fig. 6: EEG–fMRI fusion decoding performance.
Fig. 7: Experiment and spike results in rats.

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Data availability

Individual fMRI, EEG and rodent electrophysiological data are available at ScienceDB (https://doi.org/10.57760/sciencedb.psych.00120).

Code availability

MRI and EEG data analyses were based on standard procedures and codes in SPM and EEGLAB. The machine learning based analyses were based on the codes in LIBSVM. Customized codes for EEG-fMRI fusion can be requested from the corresponding authors.

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Acknowledgements

Y.T. is supported by STI2030-Major Projects by the Ministry of Science and Technology of China (grant no. 2022ZD0206400), National Natural Science Foundation of China (grant nos. 32171078 and 32322035), Scientific Foundation of the Institute of Psychology, Chinese Academy of Sciences (grant nos. E0CX52 and E2CX4015) and Young Elite Scientist Sponsorship Program by the China Association for Science and Technology (grant no. E1KX0210). L.H. is supported by National Natural Science Foundation of China (grant no. 32071061) and Beijing Natural Science Foundation (grant no. JQ22018). The funders had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript.

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Authors and Affiliations

  1. CAS Key Laboratory of Mental Health, Institute of Psychology, Chinese Academy of Sciences, Beijing, China

    Yiheng Tu, Zhenjiang Li, Libo Zhang, Huijuan Zhang, Yanzhi Bi, Lupeng Yue & Li Hu

  2. Department of Psychology, University of Chinese Academy of Sciences, Beijing, China

    Yiheng Tu, Zhenjiang Li, Libo Zhang, Huijuan Zhang, Yanzhi Bi, Lupeng Yue & Li Hu

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Contributions

This work was conceptualized by Y.T. and L.H. who also developed the methodology, undertook project administration and supervision and acquired funding. Investigation was undertaken by Y.T., H.Z., Z.L., Y.B., L.Y. and L.H. Visualization was by Y.T. and Z.L. The original draft was written by Y.T., with review and editing by Y.T., L.Z. and L.H.

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Correspondence to Yiheng Tu or Li Hu.

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Nature Human Behaviour thanks Ulrike Bingel, Giulia Liberati and Yuan B. Peng for their contribution to the peer review of this work. Peer reviewer reports are available. Peer reviewer reports are available.

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Tu, Y., Li, Z., Zhang, L. et al. Pain-preferential thalamocortical neural dynamics across species. Nat Hum Behav 8, 149–163 (2024). https://doi.org/10.1038/s41562-023-01714-6

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