Rested-Baseline Responsivity of the Ventral Striatum Is Associated With Caloric and Macronutrient Intake During One Night of Sleep Deprivation
AffiliationUniv Arizona, Social Cognit & Affect Neurosci Lab, Dept Psychiat, Coll Med
MetadataShow full item record
PublisherFRONTIERS MEDIA SA
CitationSatterfield BC, Raikes AC and Killgore WDS (2019) Rested-Baseline Responsivity of the Ventral Striatum Is Associated With Caloric and Macronutrient Intake During One Night of Sleep Deprivation. Front. Psychiatry 9:749. doi: 10.3389/fpsyt.2018.00749
JournalFRONTIERS IN PSYCHIATRY
Rights© 2019 Satterfield, Raikes and Killgore. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY).
Collection InformationThis item from the UA Faculty Publications collection is made available by the University of Arizona with support from the University of Arizona Libraries. If you have questions, please contact us at email@example.com.
AbstractBackground: Sleep loss contributes to obesity through a variety of mechanisms, including neuroendocrine functioning, increased hunger, and increased food intake. Additionally, sleep loss alters functional activation within brain regions associated with reward and behavioral control. However, it remains unknown whether individual differences in baseline neural functioning can predict eating behaviors during total sleep deprivation (TSD). We used functional magnetic resonance imaging (fMRI) to test the hypothesis that individuals with increased baseline responsiveness within reward regions are more vulnerable to TSD-induced overeating. Methods:N = 45 subjects completed several fMRI scans during a single pre-TSD session that included performance on the Multi-Source Interference Task (MSIT) and the n-back task. Subjects returned to the laboratory for an overnight TSD session, during which they were given ad libitum access to 10,900 kcal of food. Leftover food and packaging were collected every 6 h (00:00, 06:00, and 12:00) to measure total food consumption. Subjects reported sleepiness every hour and performed a food rating task every 3 h. Results: Functional activation within the ventral striatum during the MSIT and n-back positively correlated with total caloric and carbohydrate intake during the final 6 h (06:00-12:00) of TSD. Activation within the middle and superior temporal gyri during the MSIT also correlated with total carbohydrates consumed. Food consumption did not correlate with subjective sleepiness, hunger, or food desire. Conclusions: Individual differences in neural activity of reward processing areas (i.e., nucleus accumbens) prior to sleep deprivation are associated with an individual's propensity to overeat during subsequent sleep deprivation. This suggests that individual differences within reward processing pathways are potential key factors in sleep loss related overeating. Sleep loss and obesity are tightly linked. Both phenomena have been associated with increased neural activation in regions associated with reward, inhibitory control, and disrupted dopamine signaling. Elevated baseline reward sensitivity in the ventral striatum appears to be further compounded by sleep deprivation induced dysfunction in the reward neurocircuitry, increasing the likelihood of overeating. Our findings suggest that large individual differences in baseline responsiveness of hedonic reward pathways may modulate the association between sleep loss and obesity.
NoteOpen access journal
VersionFinal published version
SponsorsDefense Advanced Research Projects Agency (DARPA), DARPA Young Faculty Award [D12AP00241]
- Sleep Deprivation Selectively Upregulates an Amygdala-Hypothalamic Circuit Involved in Food Reward.
- Authors: Rihm JS, Menz MM, Schultz H, Bruder L, Schilbach L, Schmid SM, Peters J
- Issue date: 2019 Jan 30
- Phenotypic Stability of Energy Balance Responses to Experimental Total Sleep Deprivation and Sleep Restriction in Healthy Adults.
- Authors: Dennis LE, Spaeth AM, Goel N
- Issue date: 2016 Dec 19
- Acute sleep deprivation enhances the brain's response to hedonic food stimuli: an fMRI study.
- Authors: Benedict C, Brooks SJ, O'Daly OG, Almèn MS, Morell A, Åberg K, Gingnell M, Schultes B, Hallschmid M, Broman JE, Larsson EM, Schiöth HB
- Issue date: 2012 Mar
- The Effects of Experimental Manipulation of Sleep Duration on Neural Response to Food Cues.
- Authors: Demos KE, Sweet LH, Hart CN, McCaffery JM, Williams SE, Mailloux KA, Trautvetter J, Owens MM, Wing RR
- Issue date: 2017 Nov 1
- Altered salience network connectivity predicts macronutrient intake after sleep deprivation.
- Authors: Fang Z, Spaeth AM, Ma N, Zhu S, Hu S, Goel N, Detre JA, Dinges DF, Rao H
- Issue date: 2015 Feb 3