Leptin therapy alters appetite and neural responses to food stimuli in brain areas of leptin-sensitive subjects without altering brain structure

Journal of Clinical Endocrinology and Metabolism

Volumn 99, Issue 12, 2014, Pages E2529-E2538

  Farr, Olivia M ^a   Fiorenza, Christina ^a   Papageorgiou, Panagiotis ^a   Brinkoetter, Mary ^a   Ziemke, Florencia ^a   Koo, Bang Bon ^b   Rojas, Rafael ^a   Mantzoros, Christos S ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LEPTIN; METRELEPTIN;

ADULT; APPETITE; ARTICLE; ATTENTION; BRAIN; BRAIN FUNCTION; CASE REPORT; CONTROLLED STUDY; DIET RESTRICTION; FEEDING; FEMALE; FOOD; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HORMONE SENSITIVITY; HUMAN; HYPOTHALAMUS; LEPTIN DEFICIENCY; MORPHOLOGY; RANDOMIZED CONTROLLED TRIAL (TOPIC); REWARD; STIMULUS RESPONSE; TREATMENT RESPONSE; ADOLESCENT; ANALOGS AND DERIVATIVES; BLOOD; DEFICIENCY; DRUG EFFECTS; EATING; HORMONE SUBSTITUTION; INHIBITION (PSYCHOLOGY); NUCLEAR MAGNETIC RESONANCE IMAGING; PHOTOSTIMULATION; PSYCHOLOGY; TREATMENT OUTCOME; YOUNG ADULT;

ADOLESCENT; ADULT; APPETITE; BRAIN; EATING; FEMALE; FOOD; HORMONE REPLACEMENT THERAPY; HUMANS; HYPOTHALAMUS; INHIBITION (PSYCHOLOGY); LEPTIN; MAGNETIC RESONANCE IMAGING; PHOTIC STIMULATION; TREATMENT OUTCOME; YOUNG ADULT;

EID: 84916620242     PISSN: 0021972X     EISSN: 19457197     Source Type: Journal    
DOI: 10.1210/jc.2014-2774     Document Type: Article

References (54)

1. Chan JL, Heist K, DePaoli AM, Veldhuis JD, Mantzoros CS. The role of falling leptin levels in the neuroendocrine and metabolic adaptation to short-term starvation in healthy men. J Clin Invest. 2003; 111:1409-1421.
2. Kelesidis T, Kelesidis I, Chou S, Mantzoros CS. Narrative review: the role of leptin in human physiology: emerging clinical applications. Ann Intern Med. 2010;152:93-100.
3. Halaas JL, Gajiwala KS, Maffei M, et al. Weight-reducing effects of the plasma protein encoded by the obese gene. Science. 1995;269:543-546.
4. Pelleymounter MA, Cullen MJ, Baker MB, et al. Effects of the obese gene product on body weight regulation in ob/ob mice. Science. 1995;269:540-543.
5. Caro JF, Kolaczynski JW, Nyce MR, et al. Decreased cerebrospinal-fluid/serum leptin ratio in obesity: a possible mechanism for leptin resistance. Lancet. 1996;348:159-161.
6. Ur E, Grossman A, Després JP. Obesity results as a consequence of glucocorticoid induced leptin resistance. Horm Metab Res. 1996; 28:744-747.
7. Zakrzewska KE, Cusin I, Sainsbury A, Rohner-Jeanrenaud F, Jeanrenaud B. Glucocorticoids as counterregulatory hormones of leptin: toward an understanding of leptin resistance. Diabetes. 1997;46:717-719.
8. Frank S, Heni M, Moss A, et al. Leptin therapy in a congenital leptin-deficient patient leads to acute and long-term changes in homeostatic, reward, and food-related brain areas. J Clin Endocrinol Metab. 2011;96:E1283-E1287.
9. Farooqi IS, Bullmore E, Keogh J, Gillard J, O'Rahilly S, Fletcher PC. Leptin regulates striatal regions andhumaneating behavior. Science. 2007;317:1355.
10. Bereiter DA, Jeanrenaud B. Altered neuroanatomical organization in the central nervous system of the genetically obese (ob/ob) mouse. Brain Res. 1979;165:249-260.
11. Bouret SG, Draper SJ, Simerly RB. Trophic action of leptin on hypothalamic neurons that regulate feeding. Science. 2004;304:108-110.
12. London ED, Berman SM, Chakrapani S, et al. Short-term plasticity of gray matter associated with leptin deficiency and replacement. J Clin Endocrinol Metab. 2011;96:E1212-E1220.
13. Matochik JA, London ED, Yildiz BO, et al. Effect of leptin replacement on brain structure in genetically leptin-deficient adults. J Clin Endocrinol Metab. 2005;90:2851-2854.
14. Vannucci SJ, Gibbs EM, Simpson IA. Glucose utilization and glucose transporter proteins GLUT-1 and GLUT-3 in brains of diabetic (db/db) mice. Am J Physiol. 1997;272:E267-E274.
15. Sienkiewicz E, Magkos F, Aronis KN, et al. Long-term metreleptin treatment increases bone mineral density and content at the lumbar spine of lean hypoleptinemic women. Metabolism. 2011;60:1211-1221.
16. Welt CK, Chan JL, Bullen J, et al. Recombinant human leptin in women with hypothalamic amenorrhea. N Engl J Med. 2004;351:987-997.
17. Chou SH, Chamberland JP, Liu X, et al. Leptin is an effective treatment for hypothalamic amenorrhea. Proc Natl Acad Sci USA. 2011;108:6585-6590.
18. Baroncini M, Jissendi P, Balland E, et al. MRI atlas of the human hypothalamus. Neuroimage. 2012;59:168-180.
19. Gitelman DR, Penny WD, Ashburner J, Friston KJ. Modeling regional and psychophysiologic interactions in fMRI: the importance of hemodynamic deconvolution. Neuroimage. 2003;19:200-207.
20. Steppan CM, Swick AG. A role for leptin in brain development. Biochem Biophys Res Commun. 1999;256:600-602.
21. DeSilva A, Salem V, Long CJ, et al. The gut hormones PYY3-36 and GLP-1 7-36 amide reduce food intake and modulate brain activity in appetite centers in humans. Cell Metab. 2011;14:700-706.
22. PorubskáK, Veit R, Preissl H, Fritsche A, Birbaumer N. Subjective feeling of appetite modulates brain activity: an fMRI study. Neuroimage. 2006;32:1273-1280.
23. St-Onge MP, Sy M, Heymsfield SB, Hirsch J. Human cortical specialization for food: a functional magnetic resonance imaging investigation. J Nutr. 2005;135:1014-1018.
24. Menon V, Uddin LQ. Saliency, switching, attention and control: a network model of insula function. Brain Struct Funct. 2010;214:655-667.
25. Butter CM, McDonald JA, Snyder DR. Orality, preference behavior, and reinforcement value of nonfood object in monkeys with orbital frontal lesions. Science. 1969;164:1306-1307.
26. Baylis LL, Gaffan D. Amygdalectomy and ventromedial prefrontal ablation produce similar deficits in food choice and in simple object discrimination learning for an unseen reward. Exp Brain Res. 1991; 86:617-622.
27. Damasio AR, Tranel D, Damasio H. Individuals with sociopathic behavior caused by frontal damage fail to respond autonomically to social stimuli. Behav Brain Res. 1990;41:81-94.
28. Bechara A, Tranel D, Damasio H, Damasio AR. Failure to respond autonomically to anticipated future outcomes following damage to prefrontal cortex. Cereb Cortex. 1996;6:215-225.
29. Ursin H, Linck P, McCleary RA. Spatial differentiation of avoidance deficit following septal and cingulate lesions. J Comp Physiol Psychol. 1969;68:74-79.
30. Zysset S, Huber O, Ferstl E, von Cramon DY. The anterior fronto-median cortex and evaluative judgment: an fMRI study. Neuroimage. 2002;15:983-991.
31. Castelli F, Happé F, Frith U, Frith C. Movement and mind: a functional imaging study of perception and interpretation of complex intentional movement patterns. Neuroimage. 2000;12:314-325.
32. Del Parigi A, Gautier JF, Chen K, et al. Neuroimaging and obesity: mapping the brain responses to hunger and satiation in humans using positron emission tomography. Ann NY Acad Sci. 2002;967:389-397.
33. Del Parigi A, Chen K, Gautier JF, et al. Sex differences in the human brain's response to hunger and satiation. Am J Clin Nutr. 2002;75:1017-1022.
34. Sokol-Hessner P, Hutcherson C, Hare T, Rangel A. Decision value computation in DLPFC and VMPFC adjusts to the available decision time. Eur J Neurosci. 2012;35:1065-1074.
35. Plassmann H, O'Doherty JP, Rangel A. Appetitive and aversive goal values are encoded in the medial orbitofrontal cortex at the time of decision making. J Neurosci. 2010;30:10799-10808.
36. Berridge KC. Food reward: brain substrates of wanting and liking. Neurosci Biobehav Rev. 1996;20:1-25.
37. Bassareo V, Di Chiara G. Modulation of feeding-induced activation of mesolimbic dopamine transmission by appetitive stimuli and its relation to motivational state. Eur J Neurosci. 1999;11:4389-4397.
38. Beaver JD, Lawrence AD, van Ditzhuijzen J, Davis MH, Woods A, Calder AJ. Individual differences in reward drive predict neural responses to images of food. J Neurosci. 2006;26:5160-5166.
39. Kelley AE, Baldo BA, Pratt WE, Will MJ. Corticostriatal-hypothalamic circuitry and food motivation: integration of energy, action and reward. Physiol Behav. 2005;86:773-795.
40. Corbetta M, Shulman GL. Control of goal-directed and stimulus-driven attention in the brain. Nat Rev Neurosci. 2002;3:201-215.
41. Corbetta M, Kincade JM, Shulman GL. Neural systems for visual orienting and their relationships to spatial working memory. J Cogn Neurosci. 2002;14:508-523.
42. McFadden KL, Cornier MA, Melanson EL, Bechtell JL, Tregellas JR. Effects of exercise on resting-state default mode and salience network activity in overweight/obese adults. Neuroreport. 2013;24:866-871.
43. Capotosto P, Tosoni A, Spadone S, et al. Anatomical segregation of visual selection mechanisms in human parietal cortex. J Neurosci. 2013;33:6225-6229.
44. Esslinger C, Braun U, Schirmbeck F, et al. Activation of midbrain and ventral striatal regions implicates salience processing during a modified beads task. PLoS One. 2013;8:e58536.
45. Murdaugh DL, Cox JE, Cook EW 3rd, Weller RE. fMRI reactivity to high-calorie food pictures predicts short- and long-term outcome in a weight-loss program. Neuroimage. 2012;59:2709-2721.
46. Baskin DG, Seeley RJ, Kuijper JL, et al. Increased expression of mRNA for the long form of the leptin receptor in the hypothalamus is associated with leptin hypersensitivity and fasting. Diabetes. 1998;47:538-543.
47. Mercer JG, Moar KM, Rayner DV, Trayhurn P, Hoggard N. Regulation of leptin receptor and NPY gene expression in hypothalamus of leptin-treated obese (ob/ob) and cold-exposed lean mice. FEBS Lett. 1997;402:185-188.
48. Vaisse C, Halaas JL, Horvath CM, Darnell JE Jr, Stoffel M, Friedman JM. Leptin activation of Stat3 in the hypothalamus of wild-type and ob/ob mice but not db/db mice. Nat Genet. 1996;14:95-97.
49. Hinkle W, Cordell M, Leibel R, Rosenbaum M, Hirsch J. Effects of reduced weight maintenance and leptin repletion on functional connectivity of the hypothalamus in obese humans. PLoS One. 2013;8:e59114.
50. Rosenbaum M, Sy M, Pavlovich K, Leibel RL, Hirsch J. Leptin reverses weight loss-induced changes in regional neural activity responses to visual food stimuli. J Clin Invest. 2008;118:2583-2591.
51. Bari A, Robbins TW. Inhibition and impulsivity: behavioral and neural basis of response control. Prog Neurobiol. 2013;108:44-79.
52. Hendrick OM, Ide JS, Luo X, Li CS. Dissociable processes of cognitive control during error and non-error conflicts: a study of the stop signal task. PLoS One. 2010;5:e13155.
53. Løvstad M, Funderud I, Meling T, et al. Anterior cingulate cortex and cognitive control: neuropsychological and electrophysiological findings in two patients with lesions to dorsomedial prefrontal cortex. Brain Cogn. 2012;80:237-249.
54. Killgore WD, Young AD, Femia LA, Bogorodzki P, Rogowska J, Yurgelun-Todd DA. Cortical and limbic activation during viewing of high- versus low-calorie foods. Neuroimage. 2003;19:1381-1394.