A potential role for the midbrain in integrating fat-free mass determined energy needs: An H215O PET study

Human Brain Mapping

Volumn 36, Issue 6, 2015, Pages 2406-2415

  Weise, Christopher M ^a,b   Thiyyagura, Pradeep ^c   Reiman, Eric M ^c,d   Chen, Kewei ^c   Krakoff, Jonathan ^a  

^a NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^b UNIVERSITY OF LEIPZIG   (Germany)

^c BANNER ALZHEIMER S INSTITUTE   (United States)

^d TRANSLATIONAL GENOMICS RESEARCH INSTITUTE   (United States)

Author keywords

Body composition; Brain; Energy homeostasis; Hunger; Regional cerebral blood flow

Indexed keywords

GLUCOSE; INSULIN; DEUTERIUM; OXYGEN; RADIOPHARMACEUTICAL AGENT;

ADULT; ARTICLE; BODY FAT; BODY MASS; BRAIN BLOOD FLOW; DISEASE PREDISPOSITION; ENDOCRINE FUNCTION TEST; ENERGY EXPENDITURE; FAT FREE MASS; FAT MASS; FEEDING BEHAVIOR; FEMALE; FOOD INTAKE; HUMAN; HUMAN TISSUE; INFERIOR TEMPORAL GYRUS; INSULA; MAJOR CLINICAL STUDY; MALE; MESENCEPHALON; OCCIPITAL CORTEX; PERIAQUEDUCTAL GRAY MATTER; PET SCANNER; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; SUBTHALAMIC NUCLEUS; VENTRAL TEGMENTUM; ADIPOSE TISSUE; ADOLESCENT; BLOOD FLOW; BRAIN CIRCULATION; BRAIN MAPPING; DIET RESTRICTION; HOMEOSTASIS; HUNGER; METABOLISM; MIDDLE AGED; PHYSIOLOGY; REGRESSION ANALYSIS; SCINTISCANNING; YOUNG ADULT;

ADIPOSE TISSUE; ADOLESCENT; ADULT; BRAIN MAPPING; CEREBROVASCULAR CIRCULATION; DEUTERIUM; FASTING; FEMALE; HOMEOSTASIS; HUMANS; HUNGER; MALE; MESENCEPHALON; MIDDLE AGED; OXYGEN RADIOISOTOPES; POSITRON-EMISSION TOMOGRAPHY; RADIOPHARMACEUTICALS; REGIONAL BLOOD FLOW; REGRESSION ANALYSIS; YOUNG ADULT;

EID: 84928765311     PISSN: 10659471     EISSN: 10970193     Source Type: Journal    
DOI: 10.1002/hbm.22780     Document Type: Article

References (64)

1. Bailey P, Davis EW (1942): Effects of lesions of the periaqueductal gray matter in the cat. Proc Soc Exp Biol Med 51:305-306.
2. Benarroch EE (2012): Periaqueductal gray: An interface for behavioral control. Neurology 78:210-217.
3. Berthoud H-R, Morrison C (2008): The brain, appetite, and obesity. Annu Rev Psychol 59:55-92.
4. Bie-Olsen LG, Kjaer TW, Pedersen-Bjergaard U, Lonsdale MN, Holst JJ, Law I, Thorsteinsson B (2009): Changes of cognition and regional cerebral activity during acute hypoglycemia in normal subjects: A H215O positron emission tomographic study. J Neurosci Res 87:1922-1928.
5. Blatt B, Lyon M (1968): The interrelationship of forebrain and midbrain structures involved in feeding behavior. Acta Neurol Scand 44:576-595.
6. Blundell JE, Caudwell P, Gibbons C, Hopkins M, Näslund E, King NA, Finlayson G (2012): Body composition and appetite: Fat-free mass (but not fat mass or BMI) is positively associated with self-determined meal size and daily energy intake in humans. Br J Nutr 107:445-449.
7. Brooks SJ, Cedernaes J, Schiöth HB (2013): Increased prefrontal and parahippocampal activation with reduced dorsolateral prefrontal and insular cortex activation to food images in obesity: A meta-analysis of fMRI studies. PLoS ONE 8:e60393.
8. Carmichael ST, Price JL (1996): Connectional networks within the orbital and medial prefrontal cortex of macaque monkeys. J Comp Neurol 371:179-207.
9. Cerin E, Mackinnon DP (2009): A commentary on current practice in mediating variable analyses in behavioural nutrition and physical activity. Public Health Nutr 12:1182-1188.
10. Cornier M-A, Kaenel SSV, Bessesen DH, Tregellas JR (2007): Effects of overfeeding on the neuronal response to visual food cues. Am J Clin Nutr 86:965-971.
11. Cornier M-A, Salzberg AK, Endly DC, Bessesen DH, Rojas DC, Tregellas JR (2009): The effects of overfeeding on the neuronal response to visual food cues in thin and reduced-obese individuals. PLoS One 4:e6310.
12. Craig AD (1996): An ascending general homeostatic afferent pathway originating in lamina I. Prog Brain Res 107:225-242.
13. Craig AD (2002): How do you feel? Interoception: The sense of the physiological condition of the body. Nat Rev Neurosci 3:655-666.
14. Craig AD (2003): A new view of pain as a homeostatic emotion. Trends Neurosci 26:303-307.
15. Craig ADB (2009): How do you feel-now? The anterior insula and human awareness. Nat Rev Neurosci 10:59-70.
16. Critchley HD (2009): Psychophysiology of neural, cognitive and affective integration: fMRI and autonomic indicants. Int J Psychophysiol 73:88-94.
17. Critchley HD, Mathias CJ, Josephs O, O'Doherty J, Zanini S, Dewar B-K, Cipolotti L, Shallice T, Dolan RJ (2003): Human cingulate cortex and autonomic control: Converging neuroimaging and clinical evidence. Brain 126:2139-2152.
18. Friston KJ, Frith CD, Frackowiak RS, Turner R (1995): Characterizing dynamic brain responses with fMRI: A multivariate approach. Neuroimage 2:166-172.
19. Friston KJ, Penny WD, Glaser DE (2005): Conjunction revisited. Neuroimage 25:661-667.
20. Goran M, Fields DA, Hunter GR, Herd SL, Weinsier RL (2000): Total body fat does not influence maximal aerobic capacity. Int J Obes Relat Metab Disord 24:841-848.
21. Hayes AF (2009): Beyond Baron and Kenny: Statistical mediation analysis in the new millennium. Commun Monogr 76:408-420.
22. Hayes AF (2012): PROCESS: A versatile computational tool for observed variable mediation, moderation, and conditional process modeling. Available at: www.afhayes.com.
23. Heni M, Kullmann S, Ketterer C, Guthoff M, Bayer M, Staiger H, Machicao F, Häring H-U, Preissl H, Veit R, Fritsche A (2014): Differential effect of glucose ingestion on the neural processing of food stimuli in lean and overweight adults. Hum Brain Mapp 35:918-928.
24. Keesey RE, Powley TL (2008): Body energy homeostasis. Appetite 51:442-445.
25. Kondo H, Saleem KS, Price JL (2003): Differential connections of the temporal pole with the orbital and medial prefrontal networks in macaque monkeys. J Comp Neurol 465:499-523.
26. Kullmann S, Frank S, Heni M, Ketterer C, Veit R, Häring H-U, Fritsche A, Preissl H (2013): Intranasal insulin modulates intrinsic reward and prefrontal circuitry of the human brain in lean women. Neuroendocrinology 97:176-182.
27. LaBar KS, Gitelman DR, Parrish TB, Kim YH, Nobre AC, Mesulam MM (2001): Hunger selectively modulates corticolimbic activation to food stimuli in humans. Behav Neurosci 115:493-500.
28. Lancaster JL, Woldorff MG, Parsons LM, Liotti M, Freitas CS, Rainey L, Kochunov PV, Nickerson D, Mikiten SA, Fox PT (2000): Automated Talairach atlas labels for functional brain mapping. Hum Brain Mapp 10:120-131.
29. Linnman C, Moulton EA, Barmettler G, Becerra L, Borsook D (2012): Neuroimaging of the periaqueductal gray: State of the field. Neuroimage 60:505-522.
30. Lonstein JS, Stern JM (1997): Role of the midbrain periaqueductal gray in maternal nurturance and aggression: c-fos and electrolytic lesion studies in lactating rats. J Neurosci 17:3364-3378.
31. Lyon M, Halpern M, Mintz E (1968): The significance of the mesencephalon for coordinated feeding behavior. Acta Neurol Scand 44:323-346.
32. McDermott LJ, Grossman SP (1979): Regulation of calorie intake in rats with rostral zona incerta lesions: Effects of caloric density or palatability of the diet. Physiol Behav 23:1135-1140.
33. Mohanty A, Gitelman DR, Small DM, Mesulam MM (2008): The spatial attention network interacts with limbic and monoaminergic systems to modulate motivation-induced attention shifts. Cereb Cortex 18:2604-2613.
34. Moran TH, Ladenheim EE (2011): Adiposity signaling and meal size control. Physiol Behav 103:21-24.
35. Nichols T, Brett M, Andersson J, Wager T, Poline J-B (2005): Valid conjunction inference with the minimum statistic. Neuroimage 25:653-660.
36. Nolan-Poupart S, Veldhuizen MG, Geha P, Small DM (2013): Midbrain response to milkshake correlates with ad libitum milkshake intake in the absence of hunger. Appetite 60:168-174.
37. Ongür D, Price JL (2000): The organization of networks within the orbital and medial prefrontal cortex of rats, monkeys and humans. Cereb Cortex 10:206-219.
38. Ongür D, Ferry AT, Price JL (2003): Architectonic subdivision of the human orbital and medial prefrontal cortex. J Comp Neurol 460:425-449.
39. Page KA, Chan O, Arora J, Belfort-Deaguiar R, Dzuira J, Roehmholdt B, Cline GW, Naik S, Sinha R, Constable RT, Sherwin RS (2013): Effects of fructose vs glucose on regional cerebral blood flow in brain regions involved with appetite and reward pathways. JAMA 309:63-70.
40. Pandit R, de Jong JW, Vanderschuren LJMJ, Adan RAH (2011): Neurobiology of overeating and obesity: The role of melanocortins and beyond. Eur J Pharmacol 660:28-42.
41. Price JL (1999): Prefrontal cortical networks related to visceral function and mood. Ann N Y Acad Sci 877:383-396.
42. Price JL (2007): Definition of the orbital cortex in relation to specific connections with limbic and visceral structures and other cortical regions. Ann N Y Acad Sci 1121:54-71.
43. Raben A, Tagliabue A, Astrup A (1995): The reproducibility of subjective appetite scores. Br J Nutr 73:517-530.
44. Ravussin E, Burnand B, Schutz Y, Jéquier E (1982): Twenty-four-hour energy expenditure and resting metabolic rate in obese, moderately obese, and control subjects. Am J Clin Nutr 35:566-573.
45. Ravussin E, Lillioja S, Anderson TE, Christin L, Bogardus C (1986): Determinants of 24-hour energy expenditure in man. Methods and results using a respiratory chamber. J Clin Invest 78:1568-1578.
46. Rieu I, Derost P, Ulla M, Marques A, Debilly B, De Chazeron I, Chéreau I, Lemaire JJ, Boirie Y, Llorca PM, Durif F (2011): Body weight gain and deep brain stimulation. J Neurol Sci 310:267-270.
47. Rucker DD, Preacher KJ, Tormala ZL, Petty RE (2011): Mediation analysis in social psychology: Current practices and new recommendations. Social Personality Psychol Compass 5:359-371.
48. Růžička F, Jech R, Nováková L, Urgošík D, Vymazal J, Růžička E (2012): Weight gain is associated with medial contact site of subthalamic stimulation in Parkinson's disease. PLoS ONE 7:e38020.
49. Saleem KS, Kondo H, Price JL (2008): Complementary circuits connecting the orbital and medial prefrontal networks with the temporal, insular, and opercular cortex in the macaque monkey. J Comp Neurol 506:659-693.
50. Sewards TV, Sewards MA (2003): Representations of motivational drives in mesial cortex, medial thalamus, hypothalamus and midbrain. Brain Res Bull 61:25-49.
51. Shrout PE, Bolger N (2002): Mediation in experimental and nonexperimental studies: New procedures and recommendations. Psychol Methods 7:422-445.
52. Sisley S, Sandoval D (2011): Hypothalamic control of energy and glucose metabolism. Rev Endocr Metab Disord 12:219-233.
53. Smith SM, Nichols TE (2009): Threshold-free cluster enhancement: Addressing problems of smoothing, threshold dependence and localisation in cluster inference. Neuroimage 44:83-98.
54. Tataranni PA, Gautier JF, Chen K, Uecker A, Bandy D, Salbe AD, Pratley RE, Lawson M, Reiman EM, Ravussin E (1999): Neuroanatomical correlates of hunger and satiation in humans using positron emission tomography. Proc Natl Acad Sci USA 96:4569-4574.
55. Tomasi D, Wang G-J, Wang R, Backus W, Geliebter A, Telang F, Jayne MC, Wong C, Fowler JS, Volkow ND (2009): Association of Body Mass and Brain Activation during Gastric Distention: Implications for Obesity. PLoS ONE 4:e6847.
56. Tracy AL, Jarrard LE, Davidson T. (2001): The hippocampus and motivation revisited: Appetite and activity. Behav Brain Res 127:13-23.
57. Van Erp AM, Kruk MR, Meelis W, Veening JG (1993): Periaqueductal gray lesions do not affect grooming, induced electrically in the hypothalamic paraventricular area in the rat. Behav Brain Res 59:95-101.
58. Wang G-J, Yang J, Volkow ND, Telang F, Ma Y, Zhu W, Wong CT, Tomasi D, Thanos PK, Fowler JS (2006): Gastric stimulation in obese subjects activates the hippocampus and other regions involved in brain reward circuitry. Proc Natl Acad Sci USA 103:15641-15645.
59. Weise CM, Thiyyagura P, Reiman EM, Chen K, Krakoff J (2013): Fat-free body mass but not fat mass is associated with reduced gray matter volume of cortical brain regions implicated in autonomic and homeostatic regulation. Neuroimage 64:712-721.
60. Weise CM, Hohenadel MG, Krakoff J, Votruba SB (2014): Body composition and energy expenditure predict ad-libitum food and macronutrient intake in humans. Int J Obes (Lond) 38:243-251.
61. Weston CSE (2012): Another major function of the anterior cingulate cortex: the representation of requirements. Neurosci Biobehav Rev 36:90-110.
62. Wyrwicka W, Doty RW (1966): Feeding induced in cats by electrical stimulation of the brain stem. Exp Brain Res 1:152-160.
63. Zhao X, Lynch JG Jr, Chen Q (2010): Reconsidering baron and kenny: Myths and truths about mediation analysis. J Consumer Res 37:197-206.
64. Zhu J-N, Wang J-J(2008): The cerebellum in feeding control: Possible function and mechanism. Cell Mol Neurobiol 28:469-478.