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Pain-related nucleus accumbens function

modulation by reward and sleep disruption

Seminowicz, David A.a,b; Remeniuk, Bethanyb,c; Krimmel, Samuel R.a,b,d; Smith, Michael T.c; Barrett, Frederick S.c; Wulff, Andreas B.a,d; Furman, Andrew J.a,b,d; Geuter, Stephane,f; Lindquist, Martin A.e; Irwin, Michael R.g; Finan, Patrick H.c,*

doi: 10.1097/j.pain.0000000000001498
Research Paper
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The nucleus accumbens (NAc) has been implicated in sleep, reward, and pain modulation, but the relationship between these functional roles is unclear. This study aimed to determine whether NAc function at the onset and offset of a noxious thermal stimulus is enhanced by rewarding music, and whether that effect is reversed by experimental sleep disruption. Twenty-one healthy subjects underwent functional magnetic resonance imaging scans on 2 separate days after both uninterrupted sleep and experimental sleep disruption. During functional magnetic resonance imaging scans, participants experienced noxious stimulation while listening to individualized rewarding or neutral music. Behavioral results revealed that rewarding music significantly reduced pain intensity compared with neutral music, and disrupted sleep was associated with decreased pain intensity in the context of listening to music. In whole-brain family-wise error cluster-corrected analysis, the NAc was activated at pain onset, but not during tonic pain or at pain offset. Sleep disruption attenuated NAc activation at pain onset and during tonic pain. Rewarding music altered NAc connectivity with key nodes of the corticostriatal circuits during pain onset. Sleep disruption increased reward-related connectivity between the NAc and the anterior midcingulate cortex at pain onset. This study thus indicates that experimental sleep disruption modulates NAc function during the onset of pain in a manner that may be conditional on the presence of competing reward-related stimuli. These findings point to potential mechanisms for the interaction between sleep, reward, and pain, and suggest that sleep disruption affects both the detection and processing of aversive stimuli that may have important implications for chronic pain.

This study contributes to our understanding of mechanisms supporting the association of sleep, reward, and pain by showing that sleep disruption attenuates nucleus accumbens activation during pain onset, and increases connectivity with the anterior midcingulate cortex when rewarding and noxious stimuli are presented at the same time.

aDepartment of Neural and Pain Sciences, School of Dentistry, University of Maryland Baltimore, Baltimore, MD, United States

bCenter to Advance Chronic Pain Research, University of Maryland Baltimore, Baltimore, MD, United States

cDepartment of Psychiatry and Behavioral Sciences, Johns Hopkins University School of Medicine, Baltimore, MD, United States

dProgram in Neuroscience, School of Medicine, University of Maryland, Baltimore, MD, United States

eDepartment of Biostatistics, Johns Hopkins University Bloomberg School of Public Health, Baltimore, MD, United States

fInstitute of Cognitive Science, University of Colorado Boulder, Boulder, CO, United States

gCousins Center for Psychoneuroimmunology, UCLA Semel Institute for Neuroscience and Human Behavior, Los Angeles, CA, United States

Corresponding author. Address: Department of Psychiatry and Behavioral Sciences, Johns Hopkins University School of Medicine, 5510 Nathan Shock Dr, Suite 100, Baltimore, MD 21224, United States. Tel.: 410-550-7901. E-mail address: pfinan1@jhu.edu (P.H. Finan).

Sponsorships or competing interests that may be relevant to content are disclosed at the end of this article.

Supplemental digital content is available for this article. Direct URL citations appear in the printed text and are provided in the HTML and PDF versions of this article on the journal's Web site (www.painjournalonline.com).

Received May 31, 2018

Received in revised form November 13, 2018

Accepted January 10, 2019

© 2019 International Association for the Study of Pain
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