Journal of Autism and Developmental Disorders

, Volume 38, Issue 9, pp 1642–1653 | Cite as

Food-related Neural Circuitry in Prader-Willi Syndrome: Response to High- Versus Low-calorie Foods

Original Paper

Abstract

Prader-Willi syndrome (PWS) is a neurodevelopmental disorder characterized by hyperphagia and food preoccupations. Although dysfunction of the hypothalamus likely has a critical role in hyperphagia, it is only one of several regions involved in the regulation of eating. The purpose of this research was to examine food-related neural circuitry using functional magnetic resonance imaging in individuals with PWS and matched controls. Individuals with PWS showed increased activation in neural circuitry known to mediate hunger and motivation (hypothalamus, OFC) in response to high- versus low-calorie foods and in comparison to controls. This suggests neural circuitry for PWS is abnormally activated during hunger, particularly for high-calorie foods, and may mediate abnormally strong hunger states, therefore playing a significant role in PWS-induced hyperphagia.

Keywords

Prader-Willi syndrome fMRI Hypothalamus Food-related Genetic 

References

  1. Anand, B. K., & Brobeck, J. R. (1951). Localization of a feeding center in he hypothalamus of the rat. Proceedings of the Society for Experimental Biology and Medicine, 77, 323–324.PubMedGoogle Scholar
  2. Araujo, I. E., & Rolls, E. T. (2004). Representation in the human brain of food texture and oral fat. The Journal of Neuroscience, 24(12), 3086–3093.PubMedCrossRefGoogle Scholar
  3. Baylis, L. L., Rolls, E. T., & Baylis, G. C. (1995). Afferent connections of the caudolateral orbitofrontal cortex taste area of the primate. Neuroscience, 64, 801–812.PubMedCrossRefGoogle Scholar
  4. Burton, M. J., Rolls, E. T., & Mora, F. (1976). Effects of hunger on the responses of neurons in the lateral hypothalamus to the sight and taste of food. Experimental Neurology, 51, 668–677.PubMedCrossRefGoogle Scholar
  5. Cahill, L., Babinsky, R., Markowitsch, H. J., & McCaugh, J. L. (1995). The amygdala and emotional memory. Nature, 377, 295–296.PubMedCrossRefGoogle Scholar
  6. Carpenter, M. B. (1985). Core text of neuroanatomy (3rd ed.). Baltimore: Williams & Wilkins.Google Scholar
  7. Clark, J. M., Clark, A. J. M., Bartle, A., & Winn, P. (1991). The regulation of feeding and drinking in rats with lesions of the lateral hypothalamus made by N-methyl-D-aspartate. Neuroscience, 4, 631–640.CrossRefGoogle Scholar
  8. Coons, E. E., Levak, M., & Miller, N. E. (1965). Lateral hypothalamus: Learning of food-seeking response motivated by electrical stimulation. Science, 150, 1320–1321.PubMedCrossRefGoogle Scholar
  9. Critchley, H. D., & Rolls, E. T. (1996). Hunger and satiety modify the responses of olfactory and visual neurons in the primate orbitofrontal cortex. Journal of Neurophysiology, 75, 1673–1686.PubMedGoogle Scholar
  10. DeFalco, J., Tomishima, M., Liu, H., Zhao, C., Cai, X., Marth, J. D., et al. (2001). Virus-assisted mapping of neural inputs to a feeding center in the hypothalamus. Science, 291, 2608–2613.PubMedCrossRefGoogle Scholar
  11. Del Parigi, A., Tschop, M., Heiman, M., Salbe, A., Vozarova, B., Sell, S., et al. (2002). High circulating ghrelin: A potential cause for hyperphagia and obesity in PWS. Journal of Clinical Endocrinology & Metabolism, 87(12), 5461–5464.CrossRefGoogle Scholar
  12. Dimitropoulos, A., Feurer, I., Butler, M., & Thompson, T. (2001). Emergence of compulsive behavior and tantrums in children with Prader-Willi syndrome. American Journal on Mental Retardation, 106(1), 39–51.PubMedCrossRefGoogle Scholar
  13. Dimitropoulos, A., & Schultz, R. (2004, March). Hyperphagia in Prader-Willi syndrome: Using fMRI to explore brain mechanisms in response to food stimuli. Paper presented at the 37th Annual Gatlinburg Conference on Research and Theory in Mental Retardation and Developmental Disabilities, San Diego, California.Google Scholar
  14. Doyle, P., Rohner-Jeanrenaud, F., & Jeanrenaud, B. (1993). Local cerebral glucose utilization in brains of lean and genetically obese (fa/fa) rats. American Journal of Physiology, 264(1), E29–E36.PubMedGoogle Scholar
  15. Duvernoy, H. M. (1991). The human brain: Structure, three-dimensional sectional anatomy and MRI. New York: Springer-Verlag.Google Scholar
  16. Fieldstone, A., Zipf, W. B., Schwartz, H. C., & Berntson, G. G. (1997). Food preferences in Prader-Willi syndrome, normal weight and obese controls. International Journal of Obesity, 21, 1046–1052.PubMedCrossRefGoogle Scholar
  17. Gauthier, I., Skudlarski, P., Gore, J. C., & Anderson, A. W. (2000). Expertise for cars and birds recruits areas involved in face recognition. Nature Neuroscience, 3(2), 191–197.PubMedCrossRefGoogle Scholar
  18. Glover, D., Maltzman, I., & Williams, C. (1996). Food preferences among individuals with and without Prader-Willi syndrome. American Journal on Mental Retardation, 101(2), 195–205.PubMedGoogle Scholar
  19. Grelotti, D. J., Klin, A. J., Gauthier, I., Skudlarski, P., Cohen, D. J., Gore, J. C., et al. (2005). fMRI activation of the fusiform gyrus and amygdala to cartoon characters but not to faces in a boy with autism. Neuropsychologia, 43(3), 373–385.PubMedCrossRefGoogle Scholar
  20. Grossman, S. P. (1975). Role of the hypothalamus in the regulation of food and water intake. Psychological Review, 82(3), 200–224.PubMedCrossRefGoogle Scholar
  21. Haqq, A., Farooqi, I., O’Rahilly, S., Stadler, D., Rosenfeld, R., Pratt, K., et al. (2003). Serum ghrelin levels are inversely correlated with body mass index, age, and insulin concentrations in normal children and are markedly increased in PWS. Journal of Clinical Endocrinology and Metabolism, 88(1), 174–178.PubMedCrossRefGoogle Scholar
  22. Hinton E. C., Holland A. J., Gellatly M. S., Soni S., & Owen A. M. (2006a). An investigation into food preferences and the neural basis of food-related incentive motivation in Prader-Willi syndrome. Journal of Intellectual Disability Research, 50(Pt 9), 633–642.PubMedCrossRefGoogle Scholar
  23. Hinton E. C., Holland A. J., Gellatly M. S., Soni S., Patterson M., Ghatei M. A., & Owen A. M. (2006b). Neural representations of hunger and satiety in Prader-Willi syndrome. International Journal of Obesity, 30(2), 313–321.PubMedCrossRefGoogle Scholar
  24. Holland, A. J. (1998). Understanding the eating disorder affecting people with Prader-Willi syndrome. Journal of Applied Research in Intellectual Disabilities, 11(3), 192–206.CrossRefGoogle Scholar
  25. Holland, A., Whittington, J., & Hinton, E. (2003). The paradox of Prader-Willi syndrome: a genetic model of starvation. The Lancet, 362, 989–991.CrossRefGoogle Scholar
  26. Holm, V. A., Cassidy, S. B., Butler, M. G., Hanchett, J. M., Greenswag, L. R., Whitman, B. Y., et al. (1993). Prader-Willi syndrome: Consensus Diagnostic Criteria. Pediatrics, 91, 398–402.PubMedGoogle Scholar
  27. Holsen L. M., Zarcone J. R., Brooks W. M., Butler M. G., Thompson T. I., Ahluwalia J. S., Nollen N. L., & Savage C. R. (2006). Neural mechanisms underlying hyperphagia in Prader-Willi syndrome. Obesity, 14(6), 1028–1037.PubMedCrossRefGoogle Scholar
  28. Joseph, B., Egli, M., Koppekin, A., & Thompson, T. (2002). Food choice in people with Prader-Willi syndrome: Quantity and relative preference. American Journal on Mental Retardation, 107(2), 128–135.PubMedCrossRefGoogle Scholar
  29. Kanwisher, N., McDermott, J., & Chun, M. M. (1997). The fusiform face area: A module in human extrastriate cortex specialized for face perception. The Journal of Neuroscience, 17(11), 4302–4311.PubMedGoogle Scholar
  30. Killgore, W. D. S., Young, A. D., Femia, L. A., Bogorodzki, P., Rogowska, J., & Yurgelun-Todd, D. A. (2003). Cortical and limbic activation during viewing of high- versus low-calorie foods. Neuroimage, 1381–1394.Google Scholar
  31. Kringelbach, M. L., Doherty, J. O., Rolls, E. T., & Andrews, C. (2003). Activation of the human orbitofrontal cortex to a liquid food stimulus is correlated with its subjective pleasantness. Cerebral Cortex, 13, 1064–1071.PubMedCrossRefGoogle Scholar
  32. LaBar, K. S., Gitelman, D. R., Parrish, T. B., Kim, Y., Nobre, A. C., Mesulam, M. (2001). Hunger selectively modulates corticolimbic activation to food stimuli in humans. Behavioral Neuroscience, 115(2), 493–500.PubMedCrossRefGoogle Scholar
  33. Ledbetter, D. H., Riccardi, V. M., Youngbloom, S. A., Strobel, R. J., Keenan, B. S., Crawford, J. D., & Louro, J. M. (1980). Deletion (15q) as a cause of the Prader-Willi syndrome (PWS). American Journal of Human Genetics, 32, 77A.Google Scholar
  34. Martin, A., State, M., Anderson, G. M., Kaye, W. M., Hanchett, J. M., McConahay, C. W., et al. (1998). Cerebrospinal fluid levels of oxytocin in Prader-Willi syndrome: A preliminary report. Biological Psychiatry, 44, 1349–1352.PubMedCrossRefGoogle Scholar
  35. Miller, L., Angula, M., Price, D., & Taneja, S. (1996). MR of the pituitary in patients with Prader-Willi syndrome: size determination and imaging findings. Pediatric Radiology, 26, 43–47.PubMedCrossRefGoogle Scholar
  36. Mora, F., Rolls, E. T., & Burton, M. J. (1976). Modulation during learning of the responses of neurons in the hypothalamus to the sight of food. Experimental Neurology, 53, 508–519.PubMedCrossRefGoogle Scholar
  37. Morris, J. S., Friston, K. J., Buchel, C., Frith, C. D., Young, A. W., Calder, A. J., Dolan, R.J. (1998). A neuromodulatory role for the human amygdala in processing emotional facial expressions. Brain, 121, 47–57.PubMedCrossRefGoogle Scholar
  38. Nicholls, R. D., Knoll, J. H. M., Butler, M. G., Karam, S., & Lalande, M. (1989). Genetic imprinting suggested by maternal heterodisomy in non-deletion Prader-Willi syndrome. Nature, 342, 281–285.PubMedCrossRefGoogle Scholar
  39. Ongur, D., & Price, J. L. (2000). The organization of networks within the orbital and medial prefrontal cortex of rats, monkeys, and humans. Cerebral Cortex, 10, 206–219.PubMedCrossRefGoogle Scholar
  40. Oomura, Y. (1973). Central mechanism of feeding. Advances in Biophysics, 5, 65–142.PubMedGoogle Scholar
  41. Pritchard, T. C., Macaluso, D. A., & Eslinger, P. J. (1999). Taste perception in patients with insular cortex lesions. Behavior Neuroscience, 113(4), 663–71.CrossRefGoogle Scholar
  42. Reilly, S. (1998). The role of the gustatory thalamus in taste-guided behavior. Neuroscience and Biobehavioral Reviews, 22(6), 883–901.PubMedCrossRefGoogle Scholar
  43. Rolls, E. T. (1999). The brain and emotion. New York: Oxford University Press.Google Scholar
  44. Rolls, E. T., Sienkiewicz, Z. J., & Yaxley, S. (1989). Hunger modulates the responses to gustatory stimuli of single neurons in the caudolateral orbitofrontal cortex of the macaque monkey. European Journal of Neuroscience, 1, 53–60.PubMedCrossRefGoogle Scholar
  45. Schneider, F., Grodd, W., Weiss, U., Klose, U., Mayer, K. R., Nagele, T., et al. (1997). Functional MRI reveals left amygdala activation during emotion. Psychiatry Research: Neuroimaging, 76, 75–82.PubMedCrossRefGoogle Scholar
  46. Shapira, N. A., Lessig, M. C., He, A. G., James, G. A., Driscoll, D. J., Liu, Y. (2005). Satiety dysfunction in Prader-Willi syndrome demonstrated by fMRI. Journal of Neurology, Neurosurgery, and Psychiatry, 76, 260–262.PubMedCrossRefGoogle Scholar
  47. Simmons, W. K., Martin, A., & Barsalou, L. W. (2005). Pictures of appetizing foods activate gustatory cortices for taste and reward. Cerebral Cortex, 15(10), 1602–1608.PubMedCrossRefGoogle Scholar
  48. Swaab, D. F., Purba, J. S., & Hofman, M. A. (1995). Alterations in the hypothalamic paraventricular nucleus and its oxytocin neurons (putative satiety cells) in Prader-Willi syndrome: A study of five cases. Journal of Clinical Endocrinology and Metabolism, 80, 573–579.PubMedCrossRefGoogle Scholar
  49. Talairach, J., & Tournoux, P. (1988). Co-planar steriotaxic atlas of the human brain. New York: Thieme.Google Scholar
  50. Tataranni, P. A., Gautier, J., Chen, K., Uecker, A., Bandy, D., Salbe, A. D., et al. (1999). Neuroanatomical correlates of hunger and satiation in humans using positron emission tomography. Proceedings of the National Academy of Sciences, 96, 4569–4574.CrossRefGoogle Scholar
  51. Taylor, R. L., & Caldwell, M. L. (1985). Type and strength of food preference of individuals with Prader-Willi syndrome. Journal of Mental Deficiency Research, 29, 109–112.PubMedGoogle Scholar
  52. Thompson, T., Butler, M. G., MacLean, Jr., W. E., Joseph, B., & Delaney, D. (1999). Cognition, behavior, neurochemistry, and genetics in Prader-Willi syndrome. In H. Tager-Flusberg (Ed.), Neurodevelopmental disorders (pp. 155–178). Cambridge: The MIT Press.Google Scholar
  53. Vuilleumier, P. (2000). Faces call for attention: Evidence from patients with visual extinction. Neuropsychologia, 38, 693–700.PubMedCrossRefGoogle Scholar
  54. Yaxley, S., Rolls, E. T., & Sienkiewicz. (1988). The responsiveness of neurons in the insular gustatory cortex of the macaque monkey is independent of hunger. Physiology & Behavior, 42, 223–229.Google Scholar
  55. Zald, D. H. (2003). The human amygdala and the emotional evaluation of sensory stimuli. Brain Research Reviews, 41, 88–123.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2008

Authors and Affiliations

  • Anastasia Dimitropoulos
    • 1
    • 2
  • Robert T. Schultz
    • 1
    • 3
    • 4
  1. 1.Developmental Neuroimaging LaboratoryYale Child Study Center, Yale University School of MedicineNew HavenUSA
  2. 2.Department of PsychologyCase Western Reserve UniversityClevelandUSA
  3. 3.Yale Child Study Center and Department of Diagnostic RadiologyYale University School of MedicineNew HavenUSA
  4. 4.Department of PediatricsChildren’s Hospital of PhiladelphiaPhiladelphiaUSA

Personalised recommendations