Sleep Deprivation Selectively Upregulates an Amygdala-Hypothalamic Circuit Involved in Food Reward

被引:43
|
作者
Rihm, Julia S. [1 ]
Menz, Mareike M. [1 ]
Schultz, Heidrun [2 ]
Bruder, Luca [3 ]
Schilbach, Leonhard [4 ]
Schmid, Sebastian M. [5 ]
Peters, Jan [3 ]
机构
[1] Univ Med Ctr Hamburg Eppendorf, Dept Syst Neurosci, D-20246 Hamburg, Germany
[2] Univ Birmingham, Sch Psychol, Birmingham B15 2TT, W Midlands, England
[3] Univ Cologne, Dept Psychol, Biol Psychol, D-50969 Cologne, Germany
[4] Max Planck Inst Psychiat, Max Planck Res Grp Social Neurosci, D-80804 Munich, Germany
[5] Univ Hosp Schleswig Holstein, Sect Endocrinol & Diabet, Dept Internal Med 1, D-23562 Lubeck, Germany
来源
JOURNAL OF NEUROSCIENCE | 2019年 / 39卷 / 05期
关键词
decision making; food intake; hypothalamus; obesity; reward; sleep deprivation; STIMULATES LOCOMOTOR-ACTIVITY; DES-ACYL GHRELIN; DIFFUSION-MODEL; ORBITOFRONTAL CORTEX; INSULIN-RESISTANCE; ELEVATED GHRELIN; PLASMA GHRELIN; REACTION-TIME; WEIGHT-GAIN; DURATION;
D O I
10.1523/JNEUROSCI.0250-18.2018
中图分类号
Q189 [神经科学];
学科分类号
071006 ;
摘要
Sleep loss is associated with increased obesity risk, as demonstrated by correlations between sleep duration and change in body mass index or body fat percentage. Whereas previous studies linked this weight gain to disturbed endocrine parameters after sleep deprivation or restriction, neuroimaging studies revealed upregulated neural processing of food rewards after sleep loss in reward-processing areas such as the anterior cingulate cortex, ventral striatum, and insula. To address this ongoing debate between hormonal versus hedonic factors underlying sleep-loss-associated weight gain, we rigorously tested the association between sleep deprivation and food cue processing using high-resolution fMRI and assessment of hormones. After taking blood samples from 32 lean, healthy, human male participants, they underwent fMRI while performing a neuroeconomic, value-based decision-making task with snack food and trinket rewards following a full night of habitual sleep and a night of sleep deprivation in a repeated-measures crossover design. We found that des-acyl ghrelin concentrations were increased after sleep deprivation compared with habitual sleep. Despite similar hunger ratings due to fasting in both conditions, participants were willing to spend more money on food items only after sleep deprivation. Furthermore, fMRI data paralleled this behavioral finding, revealing a food-reward-specific upregulation of hypothalamic valuation signals and amygdala-hypothalamic coupling after a single night of sleep deprivation. Behavioral and fMRI results were not significantly correlated with changes in acyl, des-acyl, or total ghrelin concentrations. Our results suggest that increased food valuation after sleep loss might be due to hedonic rather than hormonal mechanisms.
引用
收藏
页码:888 / 899
页数:12
相关论文
共 8 条
  • [1] The effect of REM sleep deprivation on motivation for food reward
    Hanlon, EC
    Andrzejewski, ME
    Harder, BK
    Kelley, AE
    Benca, RM
    BEHAVIOURAL BRAIN RESEARCH, 2005, 163 (01) : 58 - 69
  • [2] TITLE: SLEEP RESTRICTION IN RATS UPREGULATES THE EXPRESSION OF STRIATAL OPIOID PEPTIDE GENES INVOLVED IN FOOD REWARD: COMPARISON TO EFFECTS ON FEEDING-RELATED HYPOTHALAMIC PEPTIDE GENES
    Baldo, B.
    Hanlon, E.
    Jones, S.
    Paletz, E.
    Bremmer, Q.
    Benca, R.
    SLEEP, 2011, 34 : A42 - A42
  • [3] Intermittent food restriction upregulates critical hypothalamic genes involved in energy regulation imbalance
    Fernandez, Mariana Rosas
    Vilca, Carlos Concha
    Batista, Leandro Oliveira
    do Carmo, Maria das Gracas Tavares
    de Albuquerque, Kelse Tibau
    NUTRITION, 2023, 110
  • [4] The effect of REM sleep deprivation on acquisition and maintenance of food reward in an Operant task
    Hanlon, EC
    Harder, BK
    Obermeyer, W
    Kelley, AE
    Benca, RM
    SLEEP, 2003, 26 : A172 - A173
  • [5] Paradoxical sleep deprivation activates hypothalamic nuclei that regulate food intake and stress response
    Lara Galvao, Milene de Oliveira
    Sinigaglia-Coimbra, Rita
    Kawakami, Suzi Emiko
    Tufik, Sergio
    Suchecki, Deborah
    PSYCHONEUROENDOCRINOLOGY, 2009, 34 (08) : 1176 - 1183
  • [6] REM sleep deprivation produces a motivational deficit for food reward that is reversed by intra-accumbens amphetamine in rats
    Hanlon, Erin C.
    Benca, Ruth M.
    Baldo, Brian A.
    Kelley, Ann E.
    BRAIN RESEARCH BULLETIN, 2010, 83 (05) : 245 - 254
  • [7] Dopamine receptor D2, but not D1, mediates the reward circuit from the ventral tegmental area to the central amygdala, which is involved in pain relief
    Huang, Minjie
    Wang, Guoqing
    Lin, Yazhou
    Guo, Yanyan
    Ren, Xiuhua
    Shao, Jinping
    Cao, Jing
    Zang, Weidong
    Li, Zhihua
    MOLECULAR PAIN, 2022, 18
  • [8] Sleep, brain energy levels, and food intakeRelationship between hypothalamic ATP concentrations, food intake, and body weight during sleep–wake and sleep deprivation in ratsSchlaf, Gehirnenergiestoffwechsel und NahrungsaufnahmeZusammenhang zwischen hypothalamischen ATP-Konzentrationen, Nahrungsaufnahme und Körpergewicht im Schlaf- und Wachzustand und bei Schlafentzug bei adulten Ratten
    M. Dworak
    T. Kim
    R.W. McCarley
    R. Basheer
    Somnologie - Schlafforschung und Schlafmedizin, 2011, 15 (2) : 111 - 117