Effect of menstrual cycle phase on corticolimbic brain activation by visual food cues
Abstract
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.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Women were not included in this initial study to avoid confounding that might have arisen from the menstrual cycle.
“Women were not included in this initial study to avoid the confounding that might have arisen from the menstrual cycle (19).”
From Effects of dietary glycemic index on brain regions related to reward and craving in men (2013) · cites this paper as [19]
Cites
Maldjian, J., Laurienti, P., Kraft, R., & Burdette, J. (2003) · NeuroImage · doi:10.1016/s1053-8119(03)00169-1 · Cited by 5,453 · see citing works
The Eating Attitudes Test: psychometric features and clinical correlates
Garner, D. M., Olmsted, M., Bohr, Y., & Garfinkel, P. (1982) · Psychological Medicine · doi:10.1017/s0033291700049163 · Cited by 4,902 · see citing works
KRINGELBACH, M. (2004) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2004.03.006 · Cited by 1,977 · see citing works
Wang, G.-J., Volkow, N. D., Logan, J., Pappas, N. R., Wong, C. T., Zhu, W., Netusll, N., & Fowler, J. S. (2001) · The Lancet · doi:10.1016/s0140-6736(00)03643-6 · Cited by 1,864 · see citing works
Cabanac, M. (1971) · Science · doi:10.1126/science.173.4002.1103 · Cited by 1,521 · see citing works
Estrogen Actions in the Central Nervous System
McEwen, B. S., & Alves, S. E. (1999) · Endocrine Reviews · doi:10.1210/edrv.20.3.0365 · Cited by 1,483 · see citing works
The Neuroscience of Natural Rewards: Relevance to Addictive Drugs
Kelley, A. E., & Berridge, K. C. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-09-03306.2002 · Cited by 1,465 · see citing works
Encoding Predictive Reward Value in Human Amygdala and Orbitofrontal Cortex
Gottfried, J. A., O'Doherty, J., & Dolan, R. J. (2003) · Science · doi:10.1126/science.1087919 · Cited by 1,165 · see citing works
Widespread reward-system activation in obese women in response to pictures of high-calorie foods
Stoeckel, L. E., Weller, R. E., Cook, E. W., Twieg, D. B., Knowlton, R. C., & Cox, J. E. (2008) · NeuroImage · doi:10.1016/j.neuroimage.2008.02.031 · Cited by 857 · see citing works
Orbitofrontal cortex and basolateral amygdala encode expected outcomes during learning
Schoenbaum, G. M., Chiba, A. A., & Gallagher, M. (1998) · Nature Neuroscience · doi:10.1038/407 · Cited by 849 · see citing works
Stice, E., Spoor, S., Bohon, C., & Small, D. M. (2008) · Science · doi:10.1126/science.1161550 · Cited by 786 · see citing works
Rothemund, Y., Preuschhof, C., Bohner, G., Bauknecht, H.-C., Klingebiel, R., Flor, H., & Klapp, B. F. (2007) · NeuroImage · doi:10.1016/j.neuroimage.2007.05.008 · Cited by 679 · see citing works
Ghrelin Modulates Brain Activity in Areas that Control Appetitive Behavior
Malik, S., McGlone, F., Bedrossian, D., & Dagher, A. (2008) · Cell Metabolism · doi:10.1016/j.cmet.2008.03.007 · Cited by 677 · see citing works
Progesterone receptors: form and function in brain
Brinton, R. D., Thompson, R. F., Foy, M. R., Baudry, M., Wang, J., Finch, C. E., Morgan, T. E., Pike, C. J., Mack, W. J., Stanczyk, F. Z., et al. (2008) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2008.02.001 · Cited by 675 · see citing works
Images of desire: food-craving activation during fMRI
Pelchat, M. L., Johnson, A., Chan, R., Valdez, J., & Ragland, J. D. (2004) · NeuroImage · doi:10.1016/j.neuroimage.2004.08.023 · Cited by 667 · see citing works
Individual Differences in Reward Drive Predict Neural Responses to Images of Food
Beaver, J. D., Lawrence, A. D., van Ditzhuijzen, J., Davis, M. H., Woods, A., & Calder, A. J. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.0350-06.2006 · Cited by 594 · see citing works
Neuroanatomical correlates of hunger and satiation in humans using positron emission tomography
Tataranni, P. A., Gautier, J., Chen, K., Uecker, A., Bandy, D. J., Salbe, A. D., Pratley, R. E., Lawson, M. A., Reiman, E. M., & Ravussin, É. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.8.4569 · Cited by 592 · see citing works
Cortical and limbic activation during viewing of high- versus low-calorie foods
Killgore, W. D. S., Young, A. D., Femia, L. A., Bogorodzki, P., Rogowska, J., & Yurgelun-Todd, D. A. (2003) · NeuroImage · doi:10.1016/s1053-8119(03)00191-5 · Cited by 581 · see citing works
Menstrual cycle phase modulates reward-related neural function in women
Dreher, J.-C., Schmidt, P. J., Kohn, P., Furman, D., Rubinow, D., & Berman, K. F. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0605569104 · Cited by 567 · see citing works
Is dopamine a physiologically relevant mediator of feeding behavior?
Palmiter, R. D. (2007) · Trends in Neurosciences · doi:10.1016/j.tins.2007.06.004 · Cited by 469 · see citing works
Hunger selectively modulates corticolimbic activation to food stimuli in humans
LaBar, K. S., Gitelman, D. R., Parrish, T. B., Kim, Y.-H., Nobre, A. C., & Mesulam, M. M. (2001) · Behavioral Neuroscience · doi:10.1037/0735-7044.115.2.493 · Cited by 444 · see citing works
The Estrogen Receptor β Subtype: A Novel Mediator of Estrogen Action in Neuroendocrine Systems
Kuiper, G. G. J. M., Shughrue, P. J., Merchenthaler, I. J., & Gustafsson, J.-Α. (1998) · Frontiers in Neuroendocrinology · doi:10.1006/frne.1998.0170 · Cited by 439 · see citing works
Estrogen actions in the central nervous system
McMillan, P. J., & Dorsa, D. M. (1999) · Current Opinion in Endocrinology & Diabetes · doi:10.1097/00060793-199902000-00006 · Cited by 391 · see citing works
Amygdala–frontal interactions and reward expectancy
Holland, P. C., & Gallagher, M. (2004) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2004.03.007 · Cited by 390 · see citing works
Direct effect of 17β‐estradiol on striatum: Sex differences in dopamine release
Becker, J. B. (1990) · Synapse · doi:10.1002/syn.890050211 · Cited by 360 · see citing works
Some effects of ovarian hormones on food intake and body weight in female rats.
Wade, G. N. (1975) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0076186 · Cited by 308 · see citing works
Menstrual cycle and appetite control: implications for weight regulation
Dye, L., & Blundell, J. E. (1997) · Human Reproduction · doi:10.1093/humrep/12.6.1142 · Cited by 304 · see citing works
Ovarian influences on the meal patterns of female rats
BLAUSTEIN, J., & WADE, G. (1976) · Physiology & Behavior · doi:10.1016/0031-9384(76)90064-0 · Cited by 273 · see citing works
Léránth, C., Roth, R. H., Elsworth, J. D., Naftolin, F. N., Horváth, T. L., & Redmond, D. E. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-23-08604.2000 · Cited by 267 · see citing works
Cerebral processing of food-related stimuli: effects of fasting and gender
Uher, R., Treasure, J., Heining, M., Brammer, M. J., & Campbell, I. C. (2006) · Behavioural Brain Research · doi:10.1016/j.bbr.2005.12.008 · Cited by 258 · see citing works
BUFFENSTEIN, R. (1995) · Physiology & Behavior · doi:10.1016/0031-9384(95)02003-9 · Cited by 252 · see citing works
Sensory-specific and motivation-specific satiety for the sight and taste of food and water in man
Rolls, E. T., Rolls, B. J., & Rowe, E. A. (1983) · Physiology & Behavior · doi:10.1016/0031-9384(83)90003-3 · Cited by 249 · see citing works
Sex differences in the rapid and acute effects of estrogen on striatal D2 dopamine receptor binding
Bazzett, T. J., & Becker, J. B. (1994) · Brain Research · doi:10.1016/0006-8993(94)91229-7 · Cited by 222 · see citing works
Amygdalo-Hypothalamic Circuit Allows Learned Cues to Override Satiety and Promote Eating
Petrovich, G. D., Setlow, B., Holland, P. C., & Gallagher, M. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-19-08748.2002 · Cited by 205 · see citing works
THE EFFECTS OF OVARIAN STEROIDS ON FOOD AND WATER INTAKE AND BODY WEIGHT IN THE FEMALE RAT
Tarttelin, M. F., & Gorski, R. A. (1973) · European Journal of Endocrinology · doi:10.1530/acta.0.0720551 · Cited by 202 · see citing works
Gundlah, C., Kohama, S. G., Mirkes, S. J., Garyfallou, V. T., Urbanski, H. F., & Bethea, C. L. (2000) · Molecular Brain Research · doi:10.1016/s0006-8993(99)02475-0 · Cited by 199 · see citing works
Neural Mechanisms Underlying Hyperphagia in Prader‐Willi Syndrome
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) · Obesity · doi:10.1038/oby.2006.118 · Cited by 189 · see citing works
Estrogen treatment enhances dopamine receptor sensitivity in the rat striatum
Hruska, R. E., & Silbergeld, E. K. (1980) · European Journal of Pharmacology · doi:10.1016/0014-2999(80)90081-3 · Cited by 174 · see citing works
Neural mechanisms underlying food motivation in children and adolescents
Holsen, L. M., Zarcone, J. R., Thompson, T., Brooks, W., Anderson, M. F., Ahluwalia, J., Nollen, N., & Savage, C. (2005) · NeuroImage · doi:10.1016/j.neuroimage.2005.04.043 · Cited by 164 · see citing works
Menstrual cycle and voluntary food intake
Gong, E. J., Garrel, D., & Calloway, D. H. (1989) · The American Journal of Clinical Nutrition · doi:10.1093/ajcn/49.2.252 · Cited by 163 · see citing works
Subjective feeling of appetite modulates brain activity
Porubská, K., Veit, R., Preissl, H. T., Fritsche, A., & Birbaumer, N. (2006) · NeuroImage · doi:10.1016/j.neuroimage.2006.04.216 · Cited by 162 · see citing works
Energy intakes are higher during the luteal phase of ovulatory menstrual cycles
Barr, S., Janelle, K., & Prior, J. (1995) · The American Journal of Clinical Nutrition · doi:10.1093/ajcn/61.1.39 · Cited by 162 · see citing works
Effects of overfeeding on the neuronal response to visual food cues
Cornier, M.-A., Von Kaenel, S. S., Bessesen, D. H., & Tregellas, J. R. (2007) · The American Journal of Clinical Nutrition · doi:10.1093/ajcn/86.4.965 · Cited by 160 · see citing works
The effect of the menstrual cycle on patterns of food intake.
Dalvit, S. P. (1981) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/34.9.1811 · Cited by 160 · see citing works
Creutz, L. M., & Kritzer, M. F. (2002) · The Journal of Comparative Neurology · doi:10.1002/cne.10207 · Cited by 151 · see citing works
Reduction of food intake in the ovulatory phase of the menstrual cycle
Lyons, P., Truswell, A. S., Mira, M., Vizzard, J., & Abraham, S. F. (1989) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/49.6.1164 · Cited by 138 · see citing works
Roy, B. N., Reid, R. L., & Vugt, D. A. V. (1999) · Endocrinology · doi:10.1210/endo.140.5.6684 · Cited by 128 · see citing works
Variation in energy intake during the menstrual cycle: implications for food-intake research
Lissner, L., Stevens, J., Levitsky, D. A., Rasmussen, K., & Strupp, B. J. (1988) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/48.4.956 · Cited by 117 · see citing works
Energy regulation over the menstrual cycle
Johnson, W. G., Corrigan, S. A., Lemmon, C. R., Bergeron, K. C., & Crusco, A. H. (1994) · Physiology & Behavior · doi:10.1016/0031-9384(94)90296-8 · Cited by 115 · see citing works
Titolo, D., Cai, F., & Belsham, D. D. (2006) · Molecular Endocrinology · doi:10.1210/me.2006-0027 · Cited by 115 · see citing works
Food intake, body weight, and sweetness preferences over the menstrual cycle in humans
Pliner, P., & Fleming, A. S. (1983) · Physiology & Behavior · doi:10.1016/0031-9384(83)90240-8 · Cited by 113 · see citing works
Progesterone Receptors as Neuroendocrine Integrators
Levine, J. E., Chappell, P. E., Schneider, J. S., Sleiter, N. C., & Szabó, M. (2001) · Frontiers in Neuroendocrinology · doi:10.1006/frne.2001.0210 · Cited by 94 · see citing works
Menstrual-cycle patterns in energy and macronutrient intake
Tarasuk, V. S., & Beaton, G. H. (1991) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/53.2.442 · Cited by 94 · see citing works
Affect modulates appetite‐related brain activity to images of food
Killgore, W. D. S., & Yurgelun-Todd, D. A. (2006) · International Journal of Eating Disorders · doi:10.1002/eat.20240 · Cited by 94 · see citing works
Changes in dietary intake, urinary nitrogen, and urinary volume across the menstrual cycle
Fong, A., & Kretsch, M. (1993) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/57.1.43 · Cited by 84 · see citing works
Control of food consumption by learned cues: A forebrain–hypothalamic network
Petrovich, G. D., & Gallagher, M. (2007) · Physiology & Behavior · doi:10.1016/j.physbeh.2007.04.014 · Cited by 84 · see citing works
Bethea, C. L., Brown, N., & Kohama, S. (1996) · Endocrinology · doi:10.1210/endo.137.10.8828498 · Cited by 79 · see citing works
Human Cortical Specialization for Food: a Functional Magnetic Resonance Imaging Investigation
St‐Onge, M., Sy, M., Heymsfield, S. B., & Joy Hirsch, C. (2005) · Journal of Nutrition · doi:10.1093/jn/135.5.1014 · Cited by 76 · see citing works
Motivational state modulates the hedonic value of food images differently in men and women
Stoeckel, L. E., Cox, J. E., Cook, E. W., & Weller, R. E. (2006) · Appetite · doi:10.1016/j.appet.2006.07.079 · Cited by 76 · see citing works
Brain imaging studies of appetite in the context of obesity and the menstrual cycle
Vugt, D. A. V. (2009) · Human Reproduction Update · doi:10.1093/humupd/dmp051 · Cited by 68 · see citing works
Ovarian influences on primate food intake: assessment of progesterone actions.
Czaja, J. A. (1978) · Physiology and Behavior · doi:10.1016/0031-9384(78)90167-1 · Cited by 67 · see citing works
Dluzen, D. E., & Ramirez, V. D. (1987) · Brain Research · doi:10.1016/0006-8993(87)90762-1 · Cited by 63 · see citing works
Food intake and the menstrual cycle in rhesus monkeys.
Rosenblatt, H., Dyrenfurth, I., Ferin, M., & Wiele, R. V. V. (1980) · Physiology and Behavior · doi:10.1016/0031-9384(80)90234-6 · Cited by 60 · see citing works
Estradiol Regulation of Proopiomelanocortin Gene Expression and Peptide Content in the Hypothalamus
Treiser, S. L., & Wardlaw, S. L. (2008) · Neuroendocrinology · doi:10.1159/000126111 · Cited by 53 · see citing works
Sahu, A., Crowley, W. R., & Kalra, S. P. (1995) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.1995.tb00760.x · Cited by 50 · see citing works
Fernández‐Ruíz, J., de Miguel, R., Hernández, M., & Ramos, J. A. (1990) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(90)90262-g · Cited by 41 · see citing works
Changes in food intake during menstrual cycles and pregnancy of normal and diabetic rhesus monkeys
Kemnitz, J. W., Eisele, S. G., Lindsay, K. A., Engle, M. J., PERELMAN, R. H., & Farrell, P. M. (1984) · Diabetologia · doi:10.1007/bf00252265 · Cited by 39 · see citing works
Modulation of brain and pituitary dopamine receptors by estrogens and prolactin
Paolo, T. D., & Falardeau, P. (1985) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/0278-5846(85)90004-1 · Cited by 35 · see citing works
Thompson, T. L., Bridges, S., & Weirs, W. J. (2001) · Brain Research Bulletin · doi:10.1016/s0361-9230(01)00472-5 · Cited by 30 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Sex differences in the physiology of eating
Asarian, L., & Geary, N. (2013) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00446.2012 · Cited by 513 · see citing works
Leeners, B., Geary, N., Tobler, P. N., & Asarian, L. (2017) · Human Reproduction Update · doi:10.1093/humupd/dmw045 · Cited by 407 · see citing works
Lawrence, N. S., Hinton, E. C., Parkinson, J. A., & Lawrence, A. D. (2012) · NeuroImage · doi:10.1016/j.neuroimage.2012.06.070 · Cited by 242 · see citing works
A narrative review of sex differences in eating disorders: Is there a biological basis?
Culbert, K. M., Sisk, C. L., & Klump, K. L. (2021) · Clinical Therapeutics · doi:10.1016/j.clinthera.2020.12.003 · Cited by 142 · see citing works
Effects of dietary glycemic index on brain regions related to reward and craving in men
Lennerz, B. S., Alsop, D. C., Holsen, L. M., Stern, E., Rojas, R., Ebbeling, C. B., Goldstein, J. M., & Ludwig, D. S. (2013) · The American Journal of Clinical Nutrition · doi:10.3945/ajcn.113.064113 · Cited by 140 · see citing works
- Authors
- Frank, T. C., Kim, G. L., Krzemien, A., & Van Vugt, D. A.
- Affiliations
- Queen's University (CA)
- Venue
- Brain Research
- Publisher
- Elsevier BV
- Published
- 2010-12
- Volume
- 1363
- Pages
- 81-92
- ISSN
- 0006-8993 (ISSN-L)
- OpenAlex
- W2081552422
- Cited by
- 122
- References
- 70
- Citations by year
- 2026: 1 · 2025: 5 · 2024: 8 · 2023: 18 · 2022: 11 · 2021: 4 · 2020: 7 · 2019: 11 · 2018: 7 · 2017: 4 · 2016: 7 · 2015: 8 · 2014: 7 · 2013: 11 · 2012: 10
- FWCI
- 3.48
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Brain Research (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Physicians Services Incorporated
- Botterell Foundation
- Topics
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Regulation of Appetite and Obesity
- Social Sciences › Psychology › Clinical Psychology › Eating Disorders and Behaviors
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Keywords
- menstrual cycle, luteal phase, follicular phase, visual food cues, corticolimbic system, nucleus accumbens, amygdala, hippocampus, orbitofrontal cortex, midcingulate cortex, ovarian steroids, estrogen, progesterone, dietary intake, high-calorie foods, low-calorie foods, ingestive behavior
- MeSH terms
- Adolescent, Adult, Amygdala, Cerebral Cortex, Eating, Female, Follicular Phase, Food, Food Preferences, Gyrus Cinguli, Hippocampus, Humans, Limbic System, Luteal Phase, Magnetic Resonance Imaging, Menstrual Cycle, Neural Pathways, Nucleus Accumbens, Photic Stimulation, Young Adult
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review