Effect of menstrual cycle phase on corticolimbic brain activation by visual food cues

Food intake is decreased during the late follicular phase and increased in the luteal phase of the menstrual cycle. While a changing ovarian steroid milieu is believed to be responsible for this behavior, the specific mechanisms involved are poorly understood. Brain activity in response to visual food stimuli was compared during the estrogen dominant peri-ovulatory phase and the progesterone dominant luteal phase of the menstrual cycle. Twelve women underwent functional magnetic resonance imaging during the peri-ovulatory and luteal phases of the menstrual cycle in a counterbalanced fashion. Whole brain T2* images were collected while subjects viewed pictures of high calorie (HC) foods, low calorie (LC) foods, and control (C) pictures presented in a block design. Blood oxygen level dependent (BOLD) signal in the late follicular phase and luteal phase was determined for the contrasts HC-C, LC-C, HC-LC, and LC-HC. Both HC and LC stimuli activated numerous corticolimbic brain regions in the follicular phase, whereas only HC stimuli were effective in the luteal phase. Activation of the nucleus accumbens (NAc), amygdala, and hippocampus in response to the HC-C contrast and the hippocampus in response to the LC-C contrast was significantly increased in the late follicular phase compared to the luteal phase. Activation of the orbitofrontal cortex and mid cingulum in response to the HC-LC contrast was greater during the luteal phase. These results demonstrate for the first time that brain responses to visual food cues are influenced by menstrual cycle phase. We postulate that ovarian steroid modulation of the corticolimbic brain contributes to changes in ingestive behavior during the menstrual cycle.

[1]  M. Kretsch,et al.  Changes in dietary intake, urinary nitrogen, and urinary volume across the menstrual cycle. , 1993, The American journal of clinical nutrition.

[2]  S. Kalra,et al.  Evidence that Hypothalamic Neuropeptide Y Gene Expression Increases Before the Onset of the Preovulatory LH Surge * , 1995, Journal of neuroendocrinology.

[3]  T. Paolo,et al.  Modulation of brain and pituitary dopamine receptors by estrogens and prolactin , 1985, Progress in Neuro-Psychopharmacology and Biological Psychiatry.

[4]  Richard F. Thompson,et al.  Progesterone receptors: Form and function in brain , 2008, Frontiers in Neuroendocrinology.

[5]  D. A. Vugt Brain imaging studies of appetite in the context of obesity and the menstrual cycle , 2010 .

[6]  G. Beaton,et al.  Menstrual-cycle patterns in energy and macronutrient intake. , 1991, The American journal of clinical nutrition.

[7]  J. Becker Direct effect of 17β‐estradiol on striatum: Sex differences in dopamine release , 1990 .

[8]  M. Ferin,et al.  Food intake and the menstrual cycle in rhesus monkeys , 1980, Physiology & Behavior.

[9]  M. Brammer,et al.  Cerebral processing of food-related stimuli: Effects of fasting and gender , 2006, Behavioural Brain Research.

[10]  Nicole L. Nollen,et al.  Neural Mechanisms Underlying Hyperphagia in Prader‐Willi Syndrome , 2006, Obesity.

[11]  M. Kritzer,et al.  Estrogen receptor‐β immunoreactivity in the midbrain of adult rats: Regional, subregional, and cellular localization in the A10, A9, and A8 dopamine cell groups , 2002 .

[12]  A. Nobre,et al.  Hunger selectively modulates corticolimbic activation to food stimuli in humans. , 2001, Behavioral neuroscience.

[13]  D. Belsham,et al.  Coordinate regulation of neuropeptide Y and agouti-related peptide gene expression by estrogen depends on the ratio of estrogen receptor (ER) alpha to ERbeta in clonal hypothalamic neurons. , 2006, Molecular endocrinology.

[14]  E. Silbergeld,et al.  Estrogen treatment enhances dopamine receptor sensitivity in the rat striatum. , 1980, European journal of pharmacology.

[15]  Piotr Bogorodzki,et al.  Cortical and limbic activation during viewing of high- versus low-calorie foods , 2003, NeuroImage.

[16]  J. Gustafsson,et al.  The Estrogen Receptor β Subtype: A Novel Mediator of Estrogen Action in Neuroendocrine Systems , 1998, Frontiers in Neuroendocrinology.

[17]  D. Garner,et al.  The Eating Attitudes Test: psychometric features and clinical correlates , 1982, Psychological Medicine.

[18]  J. O'Doherty,et al.  Encoding Predictive Reward Value in Human Amygdala and Orbitofrontal Cortex , 2003, Science.

[19]  Paul J. Laurienti,et al.  An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets , 2003, NeuroImage.

[20]  S. Barr,et al.  Energy intakes are higher during the luteal phase of ovulatory menstrual cycles. , 1995, The American journal of clinical nutrition.

[21]  Donald B. Twieg,et al.  Widespread reward-system activation in obese women in response to pictures of high-calorie foods , 2008, NeuroImage.

[22]  S. Eisele,et al.  Changes in food intake during menstrual cycles and pregnancy of normal and diabetic rhesus monkeys , 2004, Diabetologia.

[23]  J. Ramos,et al.  Time-course of the effects of ovarian steroids on the activity of limbic and striatal dopaminergic neurons in female rat brain , 1990, Pharmacology Biochemistry and Behavior.

[24]  E. Rolls,et al.  The functional neuroanatomy of the human orbitofrontal cortex: evidence from neuroimaging and neuropsychology , 2004, Progress in Neurobiology.

[25]  K. Berridge,et al.  The Neuroscience of Natural Rewards: Relevance to Addictive Drugs , 2002, The Journal of Neuroscience.

[26]  J. Blundell,et al.  Menstrual cycle and appetite control: implications for weight regulation. , 1997, Human reproduction.

[27]  J. Michael Schurr,et al.  Relation Between Obesity and Blunted Striatal Response to Food Is Moderated by TaqIA A1 Allele , 2008, Science.

[28]  D. Dluzen,et al.  Intermittent infusion of progesterone potentiates whereas continuous infusion reduces amphetamine-stimulated dopamine release from ovariectomized estrogen-primed rat striatal fragments superfused in vitro , 1987, Brain Research.

[29]  Hans-Christian Bauknecht,et al.  Differential activation of the dorsal striatum by high-calorie visual food stimuli in obese individuals , 2007, NeuroImage.

[30]  Alain Dagher,et al.  Ghrelin modulates brain activity in areas that control appetitive behavior. , 2008, Cell metabolism.

[31]  J. Daniel Ragland,et al.  Images of desire: food-craving activation during fMRI , 2004, NeuroImage.

[32]  S. Wardlaw,et al.  Estradiol regulation of proopiomelanocortin gene expression and peptide content in the hypothalamus. , 1992, Neuroendocrinology.

[33]  J. A. Czaja Ovarian influences on primate food intake: Assessment of progesterone actions , 1978, Physiology & Behavior.

[34]  J. Levine,et al.  Progesterone Receptors as Neuroendocrine Integrators , 2001, Frontiers in Neuroendocrinology.

[35]  D. Calloway,et al.  Menstrual cycle and voluntary food intake. , 1989, The American journal of clinical nutrition.

[36]  S. Kohama,et al.  Steroid regulation of estrogen and progestin receptor messenger ribonucleic acid in monkey hypothalamus and pituitary. , 1996, Endocrinology.

[37]  Jean Logan,et al.  Brain dopamine and obesity , 2001, The Lancet.

[38]  Jason R Tregellas,et al.  Effects of overfeeding on the neuronal response to visual food cues. , 2007, The American journal of clinical nutrition.

[39]  S. Abraham,et al.  Reduction of food intake in the ovulatory phase of the menstrual cycle. , 1989, The American journal of clinical nutrition.

[40]  T. L. Thompson,et al.  Alteration of dopamine transport in the striatum and nucleus accumbens of ovariectomized and estrogen-primed rats following N-(p-isothiocyanatophenethyl) spiperone (NIPS) treatment , 2001, Brain Research Bulletin.

[41]  R. Palmiter Is dopamine a physiologically relevant mediator of feeding behavior? , 2007, Trends in Neurosciences.

[42]  Daniella J. Furman,et al.  Menstrual cycle phase modulates reward-related neural function in women , 2007, Proceedings of the National Academy of Sciences.

[43]  P. Holland,et al.  Amygdalo-Hypothalamic Circuit Allows Learned Cues to Override Satiety and Promote Eating , 2002, The Journal of Neuroscience.

[44]  P. Shughrue,et al.  Comparative distribution of estrogen receptor‐α and ‐β mRNA in the rat central nervous system , 1997, The Journal of comparative neurology.

[45]  H. Urbanski,et al.  Distribution of estrogen receptor beta (ERbeta) mRNA in hypothalamus, midbrain and temporal lobe of spayed macaque: continued expression with hormone replacement. , 2000, Brain research. Molecular brain research.

[46]  W. G. Johnson,et al.  Energy regulation over the menstrual cycle , 1994, Physiology & Behavior.

[47]  G. Schoenbaum,et al.  Orbitofrontal cortex and basolateral amygdala encode expected outcomes during learning , 1998, Nature Neuroscience.

[48]  R. Gorski,et al.  The effects of ovarian steroids on food and water intake and body weight in the female rat. , 1973, Acta endocrinologica.

[49]  R. Roth,et al.  Estrogen Is Essential for Maintaining Nigrostriatal Dopamine Neurons in Primates: Implications for Parkinson's Disease and Memory , 2000, The Journal of Neuroscience.

[50]  Hubert Preissl,et al.  Subjective feeling of appetite modulates brain activity An fMRI study , 2006, NeuroImage.

[51]  R. Reid,et al.  Printed in U.S.A. Copyright © 1999 by The Endocrine Society The Effects of Estrogen and Progesterone on Corticotropin-Releasing Hormone and Arginine Vasopressin Messenger Ribonucleic Acid Levels in the Paraventricular Nucleus and Supraoptic Nucleus of the , 2022 .

[52]  E. Ravussin,et al.  Neuroanatomical correlates of hunger and satiation in humans using positron emission tomography. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[53]  Deborah A Yurgelun-Todd,et al.  Affect modulates appetite-related brain activity to images of food. , 2006, The International journal of eating disorders.

[54]  Laura M. Holsen,et al.  Neural mechanisms underlying food motivation in children and adolescents , 2005, NeuroImage.

[55]  Edwin W. Cook,et al.  Motivational state modulates the hedonic value of food images differently in men and women , 2007, Appetite.

[56]  J. Becker,et al.  Sex differences in the rapid and acute effects of estrogen on striatal D2 dopamine receptor binding , 1994, Brain Research.

[57]  J. Blaustein,et al.  Ovarian influences on the meal patterns of female rats , 1976, Physiology & Behavior.

[58]  Michela Gallagher,et al.  Control of food consumption by learned cues: A forebrain–hypothalamic network , 2007, Physiology & Behavior.

[59]  G. Wade Some effects of ovarian hormones on food intake and body weight in female rats. , 1975, Journal of comparative and physiological psychology.

[60]  A. Prentice,et al.  Food intake and the menstrual cycle: A retrospective analysis, with implications for appetite research , 1995, Physiology & Behavior.

[61]  M. Cabanac Physiological Role of Pleasure , 1971, Science.

[62]  S. Dalvit The effect of the menstrual cycle on patterns of food intake. , 1981, The American journal of clinical nutrition.

[63]  Joy Hirsch,et al.  Human cortical specialization for food: a functional magnetic resonance imaging investigation. , 2005, The Journal of nutrition.

[64]  A. Lawrence,et al.  Individual Differences in Reward Drive Predict Neural Responses to Images of Food , 2006, The Journal of Neuroscience.

[65]  E. Rolls,et al.  Sensory-specific and motivation-specific satiety for the sight and taste of food and water in man , 1983, Physiology & Behavior.

[66]  B. McEwen,et al.  Estrogen actions in the central nervous system. , 1999, Endocrine reviews.

[67]  L. Lissner,et al.  Variation in energy intake during the menstrual cycle: implications for food-intake research. , 1988, The American journal of clinical nutrition.

[68]  A. Fleming,et al.  Food intake, body weight, and sweetness preferences over the menstrual cycle in humans , 1983, Physiology & Behavior.

[69]  P. Holland,et al.  Amygdala–frontal interactions and reward expectancy , 2004, Current Opinion in Neurobiology.