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Research Articles, Behavioral/Cognitive

The pain of sleep loss: A brain characterization in humans

Adam J. Krause, Aric A. Prather, Tor D. Wager, Martin A. Lindquist and Matthew P. Walker
Journal of Neuroscience 28 January 2019, 2408-18; DOI: https://doi.org/10.1523/JNEUROSCI.2408-18.2018
Adam J. Krause
Center for Human Sleep Science, Department of Psychology, University of California, Berkeley, California 94720-1650, USA.
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Aric A. Prather
Department of Psychiatry, University of California, San Francisco, CA, USA
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Tor D. Wager
Department of Psychology and Neuroscience, University of Colorado, Boulder, CO, USA
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Martin A. Lindquist
Department of Biostatistics, Johns Hopkins University, Baltimore, MD, USA
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Matthew P. Walker
Center for Human Sleep Science, Department of Psychology, University of California, Berkeley, California 94720-1650, USA.Helen Wills Neuroscience Institute, University of California, Berkeley, California 94720-1650, USA.
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Abstract

Sleep loss increases the experience of pain. However, the brain mechanisms underlying altered pain processing following sleep deprivation are unknown. Moreover, it remains unclear whether ecologically modest night-to-night changes in sleep, within an individual, confer consequential day-to-day changes in experienced pain. Here, we demonstrate that acute sleep-deprivation amplifies pain reactivity within human (male and female) primary somatosensory cortex yet blunts pain-reactivity in higher-order valuation and decision-making regions of the striatum and insula cortex. Consistent with this altered neural signature, we further show that sleep deprivation expands the temperature range for classifying a stimulus as painful, specifically through a lowering of pain thresholds. Moreover, the degree of amplified reactivity within somatosensory cortex following sleep deprivation significantly predicts this expansion of experienced pain across individuals. Finally, outside of the laboratory setting, we similarly show that even modest nightly changes in sleep quality (increases and decreases) within an individual determine consequential day-to-day changes in experienced pain (decreases and increases, respectively). Together, these data provide a central brain framework underlying the impact of sleep loss on pain, and furthermore, establish that the association between sleep and pain is expressed in a night-to-day, bidirectional relationship within a sample of the general population. More broadly, our findings highlight sleep as a novel therapeutic target for pain management within and outside the clinic, including circumstances where sleep is frequently short yet pain is abundant (e.g. the hospital setting).

SIGNIFICANCE STATEMENT

Are you experiencing pain? Did you have a bad night of sleep? This study provides underlying brain and behavioral mechanisms explaining this common co-occurrence. We show that sleep deprivation enhances pain responsivity within the primary sensing regions of the brain's cortex yet blunts activity in other regions that modulate pain processing-the striatum and insula. We further establish that even subtle night-to-night changes in sleep in a sample of the general population predict consequential day-to-day changes in pain (bidirectionally). Considering the societal rise in chronic pain conditions in lock-step with the decline in sleep time through the industrial world, our data support the hypothesis that these two trends may not simply be co-occurring but are significantly inter-related.

Footnotes

  • The authors declare no competing financial interests.

  • We would like to thank the following research assistants: Samika Kumar, Harlene Grewel, Grace Kim, Kaycee Ching, Harshika Chowdhary, Jessica Kendall-Bar, Mandana Mostofi, Jay Gupta.

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The pain of sleep loss: A brain characterization in humans
Adam J. Krause, Aric A. Prather, Tor D. Wager, Martin A. Lindquist, Matthew P. Walker
Journal of Neuroscience 28 January 2019, 2408-18; DOI: 10.1523/JNEUROSCI.2408-18.2018

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The pain of sleep loss: A brain characterization in humans
Adam J. Krause, Aric A. Prather, Tor D. Wager, Martin A. Lindquist, Matthew P. Walker
Journal of Neuroscience 28 January 2019, 2408-18; DOI: 10.1523/JNEUROSCI.2408-18.2018
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JNeurosci   Print ISSN: 0270-6474   Online ISSN: 1529-2401