The DOI matches its Crossref record; 528 of the 538 references it cites were found in a registry or an index.
Metabolic fuels and reproduction in female mammals
Abstract
A complete reproductive cycle of ovulation, conception, pregnancy, and lactation is one of the most energetically expensive activities that a female mammal can undertake. A reproductive attempt at a time when calories are not sufficiently available can result in a reduced return on the maternal energetic investment or even in the death of the mother and her offspring. Numerous physiological and behavioral mechanisms link reproduction and energy metabolism. Reproductive attempts may be interrupted or deferred when food is scarce or when other physiological processes, such as thermoregulation or fattening, make extraordinary energetic demands. Food deprivation suppresses both ovulation and estrous behavior. The neural mechanisms controlling pulsatile release of gonadotropin-releasing hormone (GnRH) and, consequently, luteinizing hormone secretion and ovarian function appear to respond to minute-to-minute changes in the availability of metabolic fuels. It is not clear whether GnRH-secreting neurons are able to detect the availability of metabolic fuels directly or whether this information is relayed from detectors elsewhere in the brain. Although pregnancy is less affected by fuel availability, both lactational performance and maternal behaviors are highly responsive to the energy supply. When a reproductive attempt is made, changes in hormone secretion have dramatic effects on the partitioning and utilization of metabolic fuels. During ovulatory cycles and pregnancy, the ovaria…
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“A suppression of estrus also occurs in fasting females where energy conservation is essential (Wade and Schneider, 1992).”
From Human Vomeronasal Organ Function: A Critical Review of Best and Worst Cases (2001) · cites this paper as Wade and Schneider, 1992
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Endocrine Studies During the Refeeding of Young Women With Nutritional Amenorrhea and Infertility
McArthur, J. W., OʼLoughlin, K., Beitins, I. Z., Johnson, L. R., Hourihan, J., & Alonso, C. (1976) · Mayo Clinic Proceedings · doi:10.1016/s0025-6196(25)05179-1 · Cited by 50
Stotsenburg, J. M. (1913) · The Anatomical Record · doi:10.1002/ar.1090070602 · Cited by 48
Role of sympathetic nerves in effects of estradiol on rat white adipose tissue
Lazzarini, S. J., & Wade, G. N. (1991) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1991.260.1.r47 · Cited by 48
Self-citationRecovery of mating behavior in the female rat following VMH lesions
Vaque, T. J. L., & Rodgers, C. H. (1975) · Physiology & Behavior · doi:10.1016/0031-9384(75)90142-0 · Cited by 48
Lacasa, D., Agli, B., Pecquery, R., & Giudicelli, Y. (1991) · Endocrinology · doi:10.1210/endo-128-2-747 · Cited by 48
Reduction in postprandial energy expenditure during pregnancy.
Illingworth, P. J., Jung, R. T., Howie, P., & Isles, T. E. (1987) · BMJ · doi:10.1136/bmj.294.6587.1573 · Cited by 47
Suppression of feeding by intrahypothalamic implants of estradiol in male and female rats
Beatty, W. W., O’Briant, D. A., & Vilberg, T. R. (1974) · Bulletin of the Psychonomic Society · doi:10.3758/bf03333466 · Cited by 46
MATERNAL PROCESSES IN THE COLD‐ADAPTATION OF MICE
Barnett, S. A. (1973) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/j.1469-185x.1973.tb01567.x · Cited by 46
Vernon, R. G., BARBER, M. C., & Finley, E. (1991) · Biochemical Journal · doi:10.1042/bj2740543 · Cited by 46
Cosgrove, J. R., Booth, P. J., & Foxcroft, G. R. (1991) · Reproduction · doi:10.1530/jrf.0.0910277 · Cited by 45
Gentry, R. T., Wade, G. N., & Blaustein, J. D. (1977) · Brain Research · doi:10.1016/0006-8993(77)91057-5 · Cited by 44
Self-citationTaste responses in the parabrachial pons of ovariectomized rats
Lorenzo, P. M. D., & Monroe, S. (1990) · Brain Research Bulletin · doi:10.1016/0361-9230(90)90052-2 · Cited by 44
Thermoendocrine influences on maternal nesting behavior in rats.
Woodside, B. C., & Leon, M. (1980) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0077652 · Cited by 43
Resource Partitioning During Reproduction in the Norway Rat
Woodside, B. C., Wilson, R., Chee, P., & Leon, M. (1981) · Science · doi:10.1126/science.7444451 · Cited by 43
Neural integration of physiological mechanisms and behaviour
Morgane, P. J. (1976) · Brain Research Bulletin · doi:10.1016/0361-9230(76)90106-4 · Cited by 43
Ahdieh, H. B., Mayer, A. D., & Rosenblatt, J. S. (2008) · Neuroendocrinology · doi:10.1159/000124875 · Cited by 43
A Review: Relationships of Some Hormones to Growth and Carcass Quality of Ruminants
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Evidence for a role of the sodium pump of hepatocytes in the control of food intake
Langhans, W., & Scharrer, E. (1987) · Journal of the Autonomic Nervous System · doi:10.1016/0165-1838(87)90149-4 · Cited by 42
Brown Adipose Tissue Metabolism in Lactating Rats: The Effect of Litter Size
Isler, D., Trayhurn, P., & Lunn, P. G. (1984) · Annals of Nutrition and Metabolism · doi:10.1159/000176789 · Cited by 42
MOORE, B. J., & Brasel, J. A. (1984) · Journal of Nutrition · doi:10.1093/jn/114.9.1548 · Cited by 42
Relationship between nutrition during lactation and maternal behaviour of rats.
Franková, S. (1971) · PubMed · Cited by 42
Studies in diet, nutrition, and fertility among a group of Kalahari Bushmen in Botswana
Wilmsen, E. Ν. (1982) · Social Science Information · doi:10.1177/053901882021001006 · Cited by 41
Time course of effects of ovarian hormones on food intake and metabolism
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Murphy, M. R. (1985) · Springer eBooks · doi:10.1007/978-1-4757-0815-8_1 · Cited by 41
Hormonal modulation of responsiveness to an aversive taste stimulus in rats
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Self-citationSpecific macromolecular binding of estradiol in the mammalian liver supernatant
Eisenfeld, A. J., Aten, R. F., Haselbacher, G. K., & Halpern, K. (1977) · Biochemical Pharmacology · doi:10.1016/0006-2952(77)90466-x · Cited by 41
do Nascimento, C. M. O., Ilic, V., & Williamson, D. H. (1989) · Biochemical Journal · doi:10.1042/bj2580273 · Cited by 41
Fantino, M., & Brinnel, H. (1986) · Physiology & Behavior · doi:10.1016/0031-9384(86)90469-5 · Cited by 40
Sex steroid hormones and adipose tissue metabolism in ovariectomized and adrenalectomized rats
Rebuffé-Scrive, M. (1987) · Acta Physiologica Scandinavica · doi:10.1111/j.1365-201x.1987.tb10620.x · Cited by 40
Ovarian hormone effects on activity, glucoregulation and thyroid hormones in the rat.
Thomas, D. K., Storlien, L., Bellingham, W. P., & Gillette, K. A. (1986) · Physiology and Behavior · doi:10.1016/0031-9384(86)90332-x · Cited by 40
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Haresign, W. (1981) · Animal Science · doi:10.1017/s0003356100025009 · Cited by 40
Bartness, T. J., Wade, G. N., & Goldman, B. D. (1987) · Journal of Experimental Zoology · doi:10.1002/jez.1402440310 · Cited by 39
Self-citationChanges 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
The Effects of Low Temperature and Food Intake on Ovulation in Domestic Mice
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Estrogen receptor in rat pancreatic islets
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Energy requirements during reproduction of Peromyscus maniculatus
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THE CHANGES IN THE AMOUNT OF DAILY FOOD-INTAKE OF THE ALBINO RAT DURING PREGNANCY AND LACTATION
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Dudley, S. D., Ramírez, I., & Wade, G. N. (2008) · Neuroendocrinology · doi:10.1159/000123192 · Cited by 38
Self-citationDietary self-selection in cycling and neonatally ovariectomized rats.
Geiselman, P., Martin, J. R., Vanderweele, D. A., & Novin, D. (1981) · Appetite · doi:10.1016/s0195-6663(81)80002-5 · Cited by 37
Effects of ovarian steroids on energy balance in rats fed a highly palatable diet
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Overeating induced by progesterone in the ovariectomized, adrenalectomized rat*1
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Exercise Reverses Photoperiodic Anestrus in Golden Hamsters
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INCREASED LH-SUPPRESSING EFFECT OF OESTROGEN IN OVARIECTOMIZED RATS AS A RESULT OF UNDERFEEDING
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Stimulatory and Inhibitory Action of Estradiol on TSH Secretion1
Fisher, J. S., & D’Angelo, S. A. (1971) · Endocrinology · doi:10.1210/endo-88-3-687 · Cited by 37
Nutrition, lactation, and postpartum amenorrhea ,
Hl, D., Lechtig, A., Martorell, R., Brineman, E., & Klein, R. E. (1978) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/31.2.322 · Cited by 37
Kenagy, R., Weinstein, I., & Heimberg, M. (1981) · Endocrinology · doi:10.1210/endo-108-5-1613 · Cited by 36
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Potentiation of epinephrine-induced lipolysis in fat cells from estrogen-treated rats
Benoit, V., Valette, A., Mercier, L., Meignen, J. M., & Boyer, J. (1982) · Biochemical and Biophysical Research Communications · doi:10.1016/0006-291x(82)91902-7 · Cited by 36
Ambient Temperature and Reproductive Success in Rodents Living at Different Latitudes 1
Bronson, F. H., & Pryor, S. (1983) · Biology of Reproduction · doi:10.1095/biolreprod29.1.72 · Cited by 36
Hamilton, J. M., & Wade, G. N. (1988) · Physiology & Behavior · doi:10.1016/0031-9384(88)90102-3 · Cited by 35
Self-citationThe effects of thyroxine and estradiol benzoate on wheel running activity in female rats
Stern, J. J., & Murphy, M. E. (1972) · Physiology & Behavior · doi:10.1016/0031-9384(72)90269-7 · Cited by 35
Metabolic changes during the menstrual cycle
Bisdee, J. T., Garlick, P. J., & James, W. P. T. (1989) · British Journal Of Nutrition · doi:10.1079/bjn19890151 · Cited by 35
Body Fat at Puberty in Rats: Alteration by Changes in Diet
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Physiological and behavioral responses to glucoprivation in the golden hamster
Rowland, N. E. (1983) · Physiology & Behavior · doi:10.1016/0031-9384(83)90172-5 · Cited by 35
Interaction between estradiol-17 beta and growth hormone in control of food intake in weanling rats.
Wade, G. N. (1974) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0035945 · Cited by 34
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The Importance of the Period of Dietary Restriction of the Dam on Behavior and Growth in the Rat
Hsueh, A. M., SIMONSON, M., Chow, B. F., & Hanson, H. M. (1974) · Journal of Nutrition · doi:10.1093/jn/104.1.37 · Cited by 34
Effects of food restriction on the length of lactational diestrus in rats
Woodside, B. C. (1991) · Hormones and Behavior · doi:10.1016/0018-506x(91)90040-o · Cited by 34
ENERGY REQUIREMENTS OF PREGNANCY
Durnin, J. V. G. A. (1987) · The Lancet · doi:10.1016/s0140-6736(87)91382-1 · Cited by 33
Roy, E. J., Maass, C. A., & Wade, G. N. (1977) · Physiology & Behavior · doi:10.1016/0031-9384(77)90105-6 · Cited by 33
Self-citationFlint, D. J., Clegg, R. A., & Knight, C. H. (1984) · Journal of Endocrinology · doi:10.1677/joe.0.1020231 · Cited by 33
Protein metabolism in the mouse during pregnancy and lactation
Millican, P. E., Vernon, R. G., & Pain, V. M. (1987) · Biochemical Journal · doi:10.1042/bj2480251 · Cited by 33
Richard, D., & Trayhurn, P. (1985) · Journal of Nutrition · doi:10.1093/jn/115.5.593 · Cited by 33
Hypoglycaemia, An Apparent Cause of Infertility of Lactating Cows
McClure, T. J. (1968) · British Veterinary Journal · doi:10.1016/s0007-1935(17)39506-4 · Cited by 33
Lactation Increases the Efficiency of Energy Utilization in Rats
Roberts, S. B., & Coward, W. A. (1984) · Journal of Nutrition · doi:10.1093/jn/114.12.2193 · Cited by 32
Ovarian hormones influence brown adipose tissue
Kemnitz, J. W., Glick, Z., & Bray, G. A. (1983) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(83)90281-2 · Cited by 32
Body Composition and Menstrual Function in Athletes
Sinning, W. E., & Little, K. D. (1987) · Sports Medicine · doi:10.2165/00007256-198704010-00004 · Cited by 32
McClure, T. J., & Saunders, J. (1985) · Reproduction · doi:10.1530/jrf.0.0740057 · Cited by 32
Merson, M. H., & Kirkpatrick, R. L. (1981) · The American Midland Naturalist · doi:10.2307/2425166 · Cited by 32
The Growth and Development of Mice in Three Climatic Environments
Biggers, J. D., Ashoub, M. R., McClaren, A., & Michie, D. (1958) · Journal of Experimental Biology · doi:10.1242/jeb.35.1.144 · Cited by 32
Effects of estradiol on tissue distribution of newly-synthesized fatty acids in rats and hamsters
Edens, N. K., & Wade, G. N. (1983) · Physiology & Behavior · doi:10.1016/s0031-9384(83)80007-9 · Cited by 32
Self-citationMeredith, S., Kirkpatrick-Keller, D., & Butcher, R. L. (1986) · Biology of Reproduction · doi:10.1095/biolreprod35.1.68 · Cited by 32
Brown Adipose Tissue Thermogenesis during Pregnancy in Mice
Andrews, J. F., Richard, D., Jennings, G., & Trayhurn, P. (1986) · Annals of Nutrition and Metabolism · doi:10.1159/000177180 · Cited by 31
Prolactin stimulates food intake in the absence of ovarian progesterone
Gerardo-Gettens, T., MOORE, B. J., Stern, J. S., & Horwitz, B. A. (1989) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1989.256.3.r701 · Cited by 31
Prolactin-steroid influences on the thermal basis for mother–young contact in Norway rats.
Woodside, B. C., Leon, M., Attard, M., Feder, H. H., Siegel, H. I., & Fishette, C. (1981) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0077822 · Cited by 31
Progesterone and the ovarian-adrenal modulation of energy balance in rats.
Ross, G. E., & Zucker, I. (1974) · Hormones and Behavior · doi:10.1016/0018-506x(74)90006-3 · Cited by 31
The effect of undernutrition of beef cows on blood hormone and metabolite concentrations post partum
Easdon, M. P., Chesworth, J. M., Aboul-Ela, M. B., & Henderson, G. (1985) · annales de biologie animale biochimie biophysique · doi:10.1051/rnd:19850111 · Cited by 31
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Metadata
- Authors
- Wade, G. N., & Schneider, J. E.
- Affiliations
- University of Massachusetts Amherst (US)
- Corresponding author
- Wade, George N.
- ORCID
- Schneider, Jill E.
- Venue
- Neuroscience & Biobehavioral Reviews
- Publisher
- Elsevier BV
- Published
- 1992-06
- Volume
- 16
- Issue
- 2
- Pages
- 235-272
- ISSN
- 0149-7634 (ISSN-L)
- OpenAlex
- W2004945873
- Cited by
- 686
- References
- 538
- Citations by year
- 2026: 8 · 2025: 17 · 2024: 13 · 2023: 18 · 2022: 21 · 2021: 13 · 2020: 18 · 2019: 20 · 2018: 17 · 2017: 28 · 2016: 17 · 2015: 17 · 2014: 25 · 2013: 25 · 2012: 26
- FWCI
- 11.94
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Neuroscience & Biobehavioral Reviews (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (5r01dk032976-09)
- National Institute of Mental Health (MH 00321)
- National Institute of Diabetes and Digestive and Kidney Diseases (DK 32976)
- National Institute of Neurological Disorders and Stroke (NS 10873)
- Topics
- Health Sciences › Medicine › Reproductive Medicine › Hypothalamic control of reproductive hormones
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Regulation of Appetite and Obesity
- Health Sciences › Medicine › Reproductive Medicine › Reproductive Biology and Fertility
- Keywords
- energy metabolism, reproduction, female mammals, food deprivation, ovulation, estrous cycle, pregnancy, lactation, gonadotropin-releasing hormone, luteinizing hormone, estradiol, progesterone, prolactin, growth hormone, dietary intake, thermoregulation, maternal behavior
- MeSH terms
- Animals, Female, Humans, Mammals, Metabolism, Reproduction
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