A multistudy analysis reveals that evoked pain intensity representation is distributed across brain systems.
Information is coded in the brain at multiple anatomical scales: locally, distributed across regions and networks, and globally. For pain, the scale of representation has not been formally tested, and quantitative comparisons of pain representations across regions and networks are lacking. In this m...
| Main Authors: | , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
Public Library of Science (PLoS)
2022-05-01
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| Series: | PLoS Biology |
| Online Access: | https://doi.org/10.1371/journal.pbio.3001620 |
| _version_ | 1797788310574202880 |
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| author | Bogdan Petre Philip Kragel Lauren Y Atlas Stephan Geuter Marieke Jepma Leonie Koban Anjali Krishnan Marina Lopez-Sola Elizabeth A Reynolds Losin Mathieu Roy Choong-Wan Woo Tor D Wager |
| author_facet | Bogdan Petre Philip Kragel Lauren Y Atlas Stephan Geuter Marieke Jepma Leonie Koban Anjali Krishnan Marina Lopez-Sola Elizabeth A Reynolds Losin Mathieu Roy Choong-Wan Woo Tor D Wager |
| author_sort | Bogdan Petre |
| collection | DOAJ |
| description | Information is coded in the brain at multiple anatomical scales: locally, distributed across regions and networks, and globally. For pain, the scale of representation has not been formally tested, and quantitative comparisons of pain representations across regions and networks are lacking. In this multistudy analysis of 376 participants across 11 studies, we compared multivariate predictive models to investigate the spatial scale and location of evoked heat pain intensity representation. We compared models based on (a) a single most pain-predictive region or resting-state network; (b) pain-associated cortical-subcortical systems developed from prior literature ("multisystem models"); and (c) a model spanning the full brain. We estimated model accuracy using leave-one-study-out cross-validation (CV; 7 studies) and subsequently validated in 4 independent holdout studies. All spatial scales conveyed information about pain intensity, but distributed, multisystem models predicted pain 20% more accurately than any individual region or network and were more generalizable to multimodal pain (thermal, visceral, and mechanical) and specific to pain. Full brain models showed no predictive advantage over multisystem models. These findings show that multiple cortical and subcortical systems are needed to decode pain intensity, especially heat pain, and that representation of pain experience may not be circumscribed by any elementary region or canonical network. Finally, the learner generalization methods we employ provide a blueprint for evaluating the spatial scale of information in other domains. |
| first_indexed | 2024-03-13T01:33:46Z |
| format | Article |
| id | doaj.art-4818be50901a4cb0a594c30efc73e9c2 |
| institution | Directory Open Access Journal |
| issn | 1544-9173 1545-7885 |
| language | English |
| last_indexed | 2024-03-13T01:33:46Z |
| publishDate | 2022-05-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Biology |
| spelling | doaj.art-4818be50901a4cb0a594c30efc73e9c22023-07-04T05:31:09ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852022-05-01205e300162010.1371/journal.pbio.3001620A multistudy analysis reveals that evoked pain intensity representation is distributed across brain systems.Bogdan PetrePhilip KragelLauren Y AtlasStephan GeuterMarieke JepmaLeonie KobanAnjali KrishnanMarina Lopez-SolaElizabeth A Reynolds LosinMathieu RoyChoong-Wan WooTor D WagerInformation is coded in the brain at multiple anatomical scales: locally, distributed across regions and networks, and globally. For pain, the scale of representation has not been formally tested, and quantitative comparisons of pain representations across regions and networks are lacking. In this multistudy analysis of 376 participants across 11 studies, we compared multivariate predictive models to investigate the spatial scale and location of evoked heat pain intensity representation. We compared models based on (a) a single most pain-predictive region or resting-state network; (b) pain-associated cortical-subcortical systems developed from prior literature ("multisystem models"); and (c) a model spanning the full brain. We estimated model accuracy using leave-one-study-out cross-validation (CV; 7 studies) and subsequently validated in 4 independent holdout studies. All spatial scales conveyed information about pain intensity, but distributed, multisystem models predicted pain 20% more accurately than any individual region or network and were more generalizable to multimodal pain (thermal, visceral, and mechanical) and specific to pain. Full brain models showed no predictive advantage over multisystem models. These findings show that multiple cortical and subcortical systems are needed to decode pain intensity, especially heat pain, and that representation of pain experience may not be circumscribed by any elementary region or canonical network. Finally, the learner generalization methods we employ provide a blueprint for evaluating the spatial scale of information in other domains.https://doi.org/10.1371/journal.pbio.3001620 |
| spellingShingle | Bogdan Petre Philip Kragel Lauren Y Atlas Stephan Geuter Marieke Jepma Leonie Koban Anjali Krishnan Marina Lopez-Sola Elizabeth A Reynolds Losin Mathieu Roy Choong-Wan Woo Tor D Wager A multistudy analysis reveals that evoked pain intensity representation is distributed across brain systems. PLoS Biology |
| title | A multistudy analysis reveals that evoked pain intensity representation is distributed across brain systems. |
| title_full | A multistudy analysis reveals that evoked pain intensity representation is distributed across brain systems. |
| title_fullStr | A multistudy analysis reveals that evoked pain intensity representation is distributed across brain systems. |
| title_full_unstemmed | A multistudy analysis reveals that evoked pain intensity representation is distributed across brain systems. |
| title_short | A multistudy analysis reveals that evoked pain intensity representation is distributed across brain systems. |
| title_sort | multistudy analysis reveals that evoked pain intensity representation is distributed across brain systems |
| url | https://doi.org/10.1371/journal.pbio.3001620 |
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