Top

Journal of Autism and Developmental Disorders

Tip

Swipe om te navigeren naar een ander artikel

Gepubliceerd in:

01-10-2008 | Original Paper

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

Auteurs: Anastasia Dimitropoulos, Robert T. Schultz

Gepubliceerd in: Journal of Autism and Developmental Disorders | Uitgave 9/2008

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.

vorige artikel Social Behavior and Autism Traits in a Sex Chromosomal Disorder: Klinefelter (47XXY) Syndrome

volgende artikel Quality of Life of Adults with Pervasive Developmental Disorders and Intellectual Disabilities

This research was approved by the Human Investigations Committee of the Yale University School of Medicine. In order to prepare our participants for the MRI procedure, we conducted a mock scanning session using a replica of the actual MRI scanner, equipped with audio equipment to simulate the MRI noise level.

Prior to scanning this sample, a pilot study of six healthy-weight adults was conducted to solidify the study design and replicate previous findings with healthy-weight participants. No attempt was made to match the pilot sample to the PWS sample. Pilot data indicated food-related activation in areas consistent with previous research in normal-weight individuals, including the insula, thalamus, FG, and OFC (Dimitropoulos and Schultz 2004).

In PWS: (1) paroxetine, (2) paroxetine, risperidone, (3) fluoxetine. In MR/DD: (1) escitalopram, topiramate, (2) methylphenidate hydrochloride, (3) risperidone, (4) atomoxetine, zonisamide, sertraline, (5) methylphenidate hydrochloride , (6) divalproex sodium, olanzapine, (7) divalproex sodium, risperidone, (8) bupropion.

Our first three PWS participants received these stimuli presented over three runs instead of two (Stimulus duration = 3,000 ms, ISI = 1,500 ms) but short response times and high accuracy on the task led us to shorten the protocol to two runs. A direct comparison between data from those who received three runs versus two runs did not reveal any differences in activation level in our primary ROIs (p > .20).

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. PubMed

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. PubMedCrossRef

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. PubMedCrossRef

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. PubMedCrossRef

Cahill, L., Babinsky, R., Markowitsch, H. J., & McCaugh, J. L. (1995). The amygdala and emotional memory. Nature, 377, 295–296. PubMedCrossRef

Carpenter, M. B. (1985). Core text of neuroanatomy (3rd ed.). Baltimore: Williams & Wilkins.

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. CrossRef

Coons, E. E., Levak, M., & Miller, N. E. (1965). Lateral hypothalamus: Learning of food-seeking response motivated by electrical stimulation. Science, 150, 1320–1321. PubMedCrossRef

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. PubMed

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. PubMedCrossRef

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. CrossRef

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. PubMedCrossRef

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.

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. PubMed

Duvernoy, H. M. (1991). The human brain: Structure, three-dimensional sectional anatomy and MRI. New York: Springer-Verlag.

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. PubMedCrossRef

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. PubMedCrossRef

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. PubMed

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. PubMedCrossRef

Grossman, S. P. (1975). Role of the hypothalamus in the regulation of food and water intake. Psychological Review, 82(3), 200–224. PubMedCrossRef

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. PubMedCrossRef

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. PubMedCrossRef

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. PubMedCrossRef

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. CrossRef

Holland, A., Whittington, J., & Hinton, E. (2003). The paradox of Prader-Willi syndrome: a genetic model of starvation. The Lancet, 362, 989–991. CrossRef

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. PubMed

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. PubMedCrossRef

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. PubMedCrossRef

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. PubMed

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.

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. PubMedCrossRef

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. PubMedCrossRef

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.

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. PubMedCrossRef

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. PubMedCrossRef

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. PubMedCrossRef

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. PubMedCrossRef

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. PubMedCrossRef

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. PubMedCrossRef

Oomura, Y. (1973). Central mechanism of feeding. Advances in Biophysics, 5, 65–142. PubMed

Pritchard, T. C., Macaluso, D. A., & Eslinger, P. J. (1999). Taste perception in patients with insular cortex lesions. Behavior Neuroscience, 113(4), 663–71. CrossRef

Reilly, S. (1998). The role of the gustatory thalamus in taste-guided behavior. Neuroscience and Biobehavioral Reviews, 22(6), 883–901. PubMedCrossRef

Rolls, E. T. (1999). The brain and emotion. New York: Oxford University Press.

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. PubMedCrossRef

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. PubMedCrossRef

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. PubMedCrossRef

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. PubMedCrossRef

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. PubMedCrossRef

Talairach, J., & Tournoux, P. (1988). Co-planar steriotaxic atlas of the human brain. New York: Thieme.

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. CrossRef

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. PubMed

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.

Vuilleumier, P. (2000). Faces call for attention: Evidence from patients with visual extinction. Neuropsychologia, 38, 693–700. PubMedCrossRef

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.

Zald, D. H. (2003). The human amygdala and the emotional evaluation of sensory stimuli. Brain Research Reviews, 41, 88–123. PubMedCrossRef

Titel: Food-related Neural Circuitry in Prader-Willi Syndrome: Response to High- Versus Low-calorie Foods
Auteurs: Anastasia Dimitropoulos
Robert T. Schultz
Publicatiedatum: 01-10-2008
Uitgeverij: Springer US
Gepubliceerd in: Journal of Autism and Developmental Disorders / Uitgave 9/2008
Print ISSN: 0162-3257
Elektronisch ISSN: 1573-3432
DOI: https://doi.org/10.1007/s10803-008-0546-x

Bohn Stafleu van Loghum

Tip

Swipe om te navigeren naar een ander artikel

Deel dit onderdeel of sectie (kopieer de link)

Abstract

Log in om toegang te krijgen

Andere artikelen Uitgave 9/2008

Beware of Over-Interpreting Negative Trials

The Effectiveness of Parent–Child Interaction Therapy for Families of Children on the Autism Spectrum

The Prevalence and Incidence of Mental Ill-Health in Adults with Autism and Intellectual Disabilities

When Prototypes Are Not Best: Judgments Made by Children with Autism

The Effects of Improvisational Music Therapy on Joint Attention Behaviors in Autistic Children: A Randomized Controlled Study

Predictors of Psychiatric Symptoms in Children with an Autism Spectrum Disorder