Sex-dependent metabolic, neuroendocrine, and cognitive responses to dietary energy restriction and excess

Martin, Bronwen; Pearson, Michele; Kebejian, Lisa; Golden, Erin; Keselman, Alex; Bender, Meredith; Carlson, Olga; Egan, Josephine; Ladenheim, Bruce; Cadet, Jean-Lud; Becker, Kevin G.; Wood, William; Duffy, Kara; Vinayakumar, Prabhu; Maudsley, Stuart; Mattson, Mark P.

doi:10.1210/en.2007-0161

Cited by 199Regulation of Appetite and ObesityDietary Effects on HealthEating Disorders and Behaviors

Sex-dependent metabolic, neuroendocrine, and cognitive responses to dietary energy restriction and excess

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Martin, Bronwen, Pearson, Michele, Kebejian, Lisa, Golden, Erin, Keselman, Alex, Bender, Meredith, Carlson, Olga, Egan, Josephine +8 more·2007·Endocrinology

DOI 10.1210/en.2007-0161PMC PMC2622430

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Abstract

Females and males typically play different roles in survival of the species and would be expected to respond differently to food scarcity or excess. To elucidate the physiological basis of sex differences in responses to energy intake, we maintained groups of male and female rats for 6 months on diets with usual, reduced [20% and 40% caloric restriction (CR), and intermittent fasting (IF)], or elevated (high-fat/high-glucose) energy levels and measured multiple physiological variables related to reproduction, energy metabolism, and behavior. In response to 40% CR, females became emaciated, ceased cycling, underwent endocrine masculinization, exhibited a heightened stress response, increased their spontaneous activity, improved their learning and memory, and maintained elevated levels of circulating brain-derived neurotrophic factor. In contrast, males on 40% CR maintained a higher body weight than the 40% CR females and did not change their activity levels as significantly as the 40% CR females. Additionally, there was no significant change in the cognitive ability of the males on the 40% CR diet. Males and females exhibited similar responses of circulating lipids (cholesterols/triglycerides) and energy-regulating hormones (insulin, leptin, adiponectin, ghrelin) to energy restriction, with the changes being quantitatively greater in males. The high-fat/high-glucose diet had no significant effects on most variables measured but adversely affected the reproductive cycle in females. Heightened cognition and motor activity, combined with reproductive shutdown, in females may maximize the probability of their survival during periods of energy scarcity and may be an evolutionary basis for the vulnerability of women to anorexia nervosa.

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Female rats subjected to prolonged CR become infertile in a reversible fashion.
“Female rats subjected to prolonged CR become infertile in a reversible fashion (Martin et al., 2007), and moderate CR may be harmful to lean human beings (Fontana et al., 2010).”
From The Search for Antiaging Interventions: From Elixirs to Fasting Regimens (2014) · cites this paper as Martin et al., 2007

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“Every other day (EOD) feeding resulted in approximately a 10–15% reduction in the average daily food intake compared to ad libitum (AL) control mice (data not shown) [21,22].”
Retracted
Intermittent Fasting Promotes Fat Loss With Lean Mass Retention, Increased Hypothalamic Norepinephrine Content, and Increased Neuropeptide Y Gene Expression in Diet-Induced Obese Male Mice
Gotthardt, J. D., Verpeut, J. L., Yeomans, B. L., Yang, J., Yasrebi, A., Roepke, T. A., & Bello, N. T. (2015) · Endocrinology · doi:10.1210/en.2015-1622 · Cited by 123 · see citing works
“Reductions in plasma levels of insulin levels also have been noted with intermittent fasting protocols in non-obese rodents (27-29, 33, 42).”
Influential
Dietary restriction started after spinal cord injury improves functional recovery
Plunet, W. T., Streijger, F., Lam, C. K., Lee, J. H. T., Liu, J., & Tetzlaff, W. (2008) · Experimental Neurology · doi:10.1016/j.expneurol.2008.04.011 · Cited by 116 · see citing works
“Whilewe did notmeasure food intake in this experiment we have observed in subsequent SCI experiments EODF animals consume ~78% overall as much as control animals (unpublished observations),which is similar to previous reports in SD male rats (Wan et al., 2003; Martin et al., 2007).”
Result
The KATP Channel Activator Diazoxide Ameliorates Amyloid-β and Tau Pathologies and Improves Memory in the 3xTgAD Mouse Model of Alzheimer's Disease
Liu, D., PITTA, M. G. R., Lee, J.-H., Ray, B., Lahiri, D. K., Furukawa, K., Mughal, M. R., Jiang, H., Villarreal, J. S., Cutler, R. G., et al. (2010) · Journal of Alzheimer s Disease · doi:10.3233/jad-2010-101017 · Cited by 113 · see citing works
“At 12 months of age, the behavioraltests of spatial learning and memory (Morris Water Maze) and spontaneous locomotor activity (open ﬁeld) were performed using methods described previously [33].”
Evaluation of the effect of caloric restriction on serum BDNF in overweight and obese subjects: preliminary evidences
Araya, A. V., Orellana, X., & Espinoza, J. (2008) · Endocrine · doi:10.1007/s12020-008-9090-x · Cited by 107 · see citing works
VennPlex–A Novel Venn Diagram Program for Comparing and Visualizing Datasets with Differentially Regulated Datapoints
Cai, H., Chen, H., Yi, T., Daimon, C. M., Boyle, J. P., Peers, C., Maudsley, S. R., & Martin, B. (2013) · PLoS ONE · doi:10.1371/journal.pone.0053388 · Cited by 105 · see citing works
“The RNA was then examined for quantity and quality using an Agilent Bioanalyzer 2100 (Agilent Technology, Palo Alto, CA). cDNA probe preparation and microarray hybridization were performed as described previously [1,3].”
BackgroundMethod
Reduced Levels of Brain Derived Neurotrophic Factor (BDNF) in the Serum of Diabetic Retinopathy Patients and in the Retina of Diabetic Rats
Ola, M. S., Nawaz, M. I., El‐Asrar, A. M. A., Abouammoh, M., & Alhomida, A. S. (2012) · Cellular and Molecular Neurobiology · doi:10.1007/s10571-012-9901-8 · Cited by 103 · see citing works
“This observation is supported by Martin et al. (2007) who reported that BDNF concentration in plasma is unrelated to levels found in the cortex and hippocampus of brain.”
Background
Plasma BDNF Is Associated with Age-Related White Matter Atrophy but Not with Cognitive Function in Older, Non-Demented Adults
Driscoll, I. F., Martin, B., An, Y., Maudsley, S. R., Ferrucci, L., Mattson, M. P., & Resnick, S. M. (2012) · PLoS ONE · doi:10.1371/journal.pone.0035217 · Cited by 99 · see citing works
Alternate‐day versus daily energy restriction diets: which is more effective for weight loss? A systematic review and meta‐analysis
Alhamdan, B. A., García-Álvarez, A., Alzahrnai, A. H., Karanxha, J., Stretchberry, D. R., Contrera, K. J., Utria, A. F., & Cheskin, L. J. (2016) · Obesity Science & Practice · doi:10.1002/osp4.52 · Cited by 95 · see citing works
“One study found that only female mice demonstrated increases in arousal and reduced Gherlin, suggesting that women may stand to achieve greater benefit from ADF (47).”
Background
Activity Based Anorexia as an Animal Model for Anorexia Nervosa–A Systematic Review
Schalla, M. A., & Stengel, A. (2019) · Frontiers in Nutrition · doi:10.3389/fnut.2019.00069 · Cited by 96 · see citing works
“↑ Body weight loss and hyperactivity (121)”
Effects of Intermittent Fasting on the Circulating Levels and Circadian Rhythms of Hormones
Kim, B. H., Joo, Y., Kim, M., Choe, H. K., Tong, Q., & Kwon, O. (2021) · Endocrinology and Metabolism · doi:10.3803/enm.2021.405 · Cited by 98 · see citing works
Caloric restriction: Impact upon pituitary function and reproduction
Martin, B., Golden, E. J., Carlson, O. D., Egan, J. M., Mattson, M. P., & Maudsley, S. R. (2008) · Ageing Research Reviews · doi:10.1016/j.arr.2008.01.002 · Cited by 93 · see citing works
The effects of the ketogenic diet on behavior and cognition
Hallböök, T., Ji, S., Maudsley, S. R., & Martin, B. (2011) · Epilepsy Research · doi:10.1016/j.eplepsyres.2011.04.017 · Cited by 89 · see citing works
“…in diets exert multifactorial direct, indirect and adaptive physiological effects in multiple physiological systems such as somatic energy management, diverse hormonal changes and alterations in the genomic output of different cells in different tissues of the body (Martin et al., 2007,2008,2009).”
Background
Ghrelin, neuropeptide Y, and other feeding-regulatory peptides active in the hippocampus: role in learning and memory
Beck, B., & Pourié, G. (2013) · Nutrition Reviews · doi:10.1111/nure.12045 · Cited by 86 · see citing works
A meta-analysis of circulating BDNF concentrations in anorexia nervosa
Brandys, M. K., Kas, M. J., Elburg, A. A. V., Campbell, I. C., & Adan, R. A. H. (2011) · The World Journal of Biological Psychiatry · doi:10.3109/15622975.2011.562244 · Cited by 85 · see citing works
“Studies in rodents (Martin et al. 2007) and humans (Piccinni et al. 2008) show that the patterns of change in BDNF concentrations in brain plasma and serum can be different.”
Background
Intermittent Fasting Improves Functional Recovery after Rat Thoracic Contusion Spinal Cord Injury
Jeong, M., Plunet, W. T., Streijger, F., Lee, J. H. T., Plemel, J. R., Park, S., Lam, C. K., Liu, J., & Tetzlaff, W. (2011) · Journal of Neurotrauma · doi:10.1089/neu.2010.1609 · Cited by 84 · see citing works
“This addresses the question of whether the positive results of EODF could be due to the general 20–30% reduction in calories typically observed in rats on EODF (Martin et al., 2007; Wan et al., 2003), or is something more speciﬁc to the 24-h fasting periods followed by 24h of overfeeding.”
Pharmacomimetics of Exercise: Novel Approaches for Hippocampally- Targeted Neuroprotective Agents
Stranahan, A. M., Zhou, Y., Martin, B., & Maudsley, S. R. (2009) · Current Medicinal Chemistry · doi:10.2174/092986709789878292 · Cited by 83 · see citing works
Sex differences in the effects of chronic stress and food restriction on body weight gain and brain expression of CRF and relaxin‐3 in rats
Lenglos, C., Mitra, A., Guèvremont, G., & Timofeeva, E. (2013) · Genes Brain & Behavior · doi:10.1111/gbb.12028 · Cited by 82 · see citing works
“This result is in agreement with a higher increase in the levels of plasma corticosterone reported for the food-restricted female rats compared with male counterparts (Martin et al. 2007).”
BackgroundResult
Long-Term Artificial Sweetener Acesulfame Potassium Treatment Alters Neurometabolic Functions in C57BL/6J Mice
Cong, W., Wang, R., Cai, H., Daimon, C. M., Scheibye‐Knudsen, M., Bohr, V. A., Turkin, R., Wood, W. H., Becker, K. G., Moaddel, R., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0070257 · Cited by 79 · see citing works
Selectively Starving Cancer Cells Through Dietary Manipulation: Methods and Clinical Implications
Simone, B. A., Champ, C. E., Rosenberg, A., Berger, A. C., Monti, D., Dicker, A. P., & Simone, N. L. (2013) · Future Oncology · doi:10.2217/fon.13.31 · Cited by 75 · see citing works
“One study noted a disproportionate change in brain chemistry when compared with male rats and female rats ceased to ovulate when undergo ing IF [61].”
Background
Long-term intermittent feeding, but not caloric restriction, leads to redox imbalance, insulin receptor nitration, and glucose intolerance
Cerqueira, F. M., da Cunha, F. M., da Silva, C. C. C., Chausse, B., Romano, R. L., Garcia, C. C. M., Colepicolo, P., de Medeiros, M. H. G., & Kowaltowski, A. J. (2011) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2011.07.006 · Cited by 73 · see citing works
“It should be stressed that our studies involved obesity-proneSprague–Dawley rats, previously used in IF protocols [38,39], and that further studies are necessary to determine if the results obtained here would also occur in other animal models.”
Low body mass index compromises live birth rate in fresh transfer in vitro fertilization cycles: a retrospective study in a Chinese population
Cai, J., Liu, L., Zhang, J., Qiu, H., Jiang, X., Li, P., Sha, A., & Ren, J. (2016) · Fertility and Sterility · doi:10.1016/j.fertnstert.2016.10.029 · Cited by 72 · see citing works
Effects of energy status and diet on Bdnf expression in the ventromedial hypothalamus of male and female rats
Liu, X., Zhu, Z., Kalyani, M., Janik, J. M., & Shi, H. (2014) · Physiology & Behavior · doi:10.1016/j.physbeh.2014.03.028 · Cited by 70 · see citing works
“Suppression of VMH Bdnf expression during positive energy balance could lead to sustained hyperphagia in males but not females beyond the 4week HFD feeding regimen, as reported that male rats continuously consume more calories from a HFD than from a LFD, whereas females consume similar amounts of total calories from b…”
Background
Dietary energy intake modifies brainstem autonomic dysfunction caused by mutant α-synuclein
Griffioen, K. J. S., Rothman, S. M., Ladenheim, B., Wan, R., Vranis, N. M., Hutchison, E. R., Okun, E., Cadet, J. L., & Mattson, M. P. (2012) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2012.07.008 · Cited by 68 · see citing works
“3), consistent with consumption of a calorie-dense diet (Martin et al., 2007).”
A cognitive deficit induced in rats by chronic intermittent cold stress is reversed by chronic antidepressant treatment
Danet, M., Lapiz-Bluhm, S., & Morilak, D. A. (2010) · The International Journal of Neuropsychopharmacology · doi:10.1017/s1461145710000039 · Cited by 63 · see citing works
Glucosensing by GnRH Neurons: Inhibition by Androgens and Involvement of AMP-Activated Protein Kinase
Roland, A. V., & Moenter, S. M. (2011) · Molecular Endocrinology · doi:10.1210/me.2010-0508 · Cited by 67 · see citing works
Minimal Peroxide Exposure of Neuronal Cells Induces Multifaceted Adaptive Responses
Chadwick, W., Zhou, Y., Park, S. S., Wang, L., Mitchell, N. A., Stone, M. D., Becker, K. G., Martin, B., & Maudsley, S. R. (2010) · PLoS ONE · doi:10.1371/journal.pone.0014352 · Cited by 64 · see citing works
“Animal care and experimental procedures followed NIH guidelines and were approved by the National Institute on Aging Animal Care and Use Committee. Male Sprague-Dawley rats (ages 4 months, n = 3: 24 months, n = 3) were euthanized humanely with isoflurane and cortical tissue was excised as previously described”
A maternal diet high in saturated fat impairs offspring hippocampal function in a sex-specific manner
Robb, J.-L., Messa, I., Lui, E., Yeung, D. H., Thacker, J. S., Satvat, E., & Mielke, J. G. (2017) · Behavioural Brain Research · doi:10.1016/j.bbr.2017.02.049 · Cited by 63 · see citing works
Plasma BDNF concentration, Val66Met genetic variant and depression- related personality traits
Terracciano, A., Martin, B., Ansari, D., Tanaka, T., Ferrucci, L., Maudsley, S., Mattson, M. P., & Costa, P. T. (2010) · Genes, Brain and Behavior · doi:10.1111/j.1601-183x.2010.00579.x · Cited by 63 · see citing works
“, 2002) but another reports that BDNF concentration in plasma is unrelated to levels found in the cortex and hippocampus (Martin et al., 2007).”
BackgroundMethodInfluential
The role of hypoleptinemia in the psychological and behavioral adaptation to starvation: Implications for anorexia nervosa
Hebebrand, J., Hildebrandt, T., Schlögl, H., Seitz, J., Denecke, S., Vieira, D. B., Gradl-Dietsch, G., Peters, T., Antel, J., Lau, D., et al. (2022) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2022.104807 · Cited by 61 · see citing works
Sex differences in feeding behavior in rats: the relationship with neuronal activation in the hypothalamus
Fukushima, A., Hagiwara, H., Fujioka, H., Kimura, F., Akema, T., & Funabashi, T. (2015) · Frontiers in Neuroscience · doi:10.3389/fnins.2015.00088 · Cited by 62 · see citing works
“Further, there were sex differences in the response to dietary disruption (Martin et al., 2007).”
BackgroundInfluential
Brain response to calorie restriction
Fusco, S., & Pani, G. (2012) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-012-1223-y · Cited by 63 · see citing works
“Interestingly, some of these effects may be sex-specific [61], and occur independently of CR action on the ARC neurons [62].”
Background
Methionine restriction alleviates age-associated cognitive decline via fibroblast growth factor 21
Ren, B., Wang, L., Shi, L. S., Jin, X., Liu, Y., Liu, R. H., Yin, F., Cadenas, E., Dai, X., Liu, Z., et al. (2021) · Redox Biology · doi:10.1016/j.redox.2021.101940 · Cited by 62 · see citing works
Manipulation of caloric content but not diet composition, attenuates the deficit in learning and memory of senescence-accelerated mouse strain P8
Komatsu, T., Chiba, T., Yamaza, H., Yamashita, K., Shimada, A., Hoshiyama, Y., Henmi, T., Ohtani, H., Higami, Y., de Cabo, R., et al. (2008) · Experimental Gerontology · doi:10.1016/j.exger.2008.01.008 · Cited by 61 · see citing works
Intermittent Fasting Induces Hypothalamic Modifications Resulting in Low Feeding Efficiency, Low Body Mass and Overeating
Chausse, B., Solon, C., da Silva, C. C. C., dos Reis, I. G. M., Manchado-Gobatto, F. D. B., Gobatto, C. A., Velloso, L. A., & Kowaltowski, A. J. (2014) · Endocrinology · doi:10.1210/en.2013-2057 · Cited by 58 · see citing works
“Previous studies have shown that changes in energy expenditure in IF are not associated with increased ambulatory activity (42, 43).”
BackgroundResult
The neuroendocrine basis of lactation-induced suppression of GnRH: Role of kisspeptin and leptin
Smith, M. S., True, C. A., & Grove, K. L. (2010) · Brain Research · doi:10.1016/j.brainres.2010.08.038 · Cited by 57 · see citing works
“Fasting, anorexia nervosa, cachexia and bulimia are examples of negative energy balance due to hypophagia, whereas lactation and exercise-induced amenorrhea are examples of negative energy balance due to excessive energy expenditure relative to the amount of food intake (Klentrou and Plyley, 2003; Loucks et al., 1998;…”
Background
Caloric restriction or resveratrol supplementation and ageing in a non-human primate: first-year outcome of the RESTRIKAL study in Microcebus murinus
Dal‐Pan, A., Terrien, J., Pifferi, F., Botalla, R., Hardy, I., Marchal, J., Zahariev, A., Chery, I., Zizzari, P., Perret, M., et al. (2010) · AGE · doi:10.1007/s11357-010-9156-6 · Cited by 57 · see citing works
“By contrast, the RMR of human subjects placed under a 25% CR decreases after three months compared with controls (Martin et al. 2007).”
Prefrontal cortex, caloric restriction and stress during aging: Studies on dopamine and acetylcholine release, BDNF and working memory
Del Arco, A., Segovia, G., de Blas, M., Garrido, P., Acuña-Castroviejo, D., Pamplona, R., & Mora, F. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2010.07.024 · Cited by 57 · see citing works
Intermittent Fasting Dietary Restriction Regimen Negatively Influences Reproduction in Young Rats: A Study of Hypothalamo-Hypophysial-Gonadal Axis
Sushil Kumar, K., & Kaur, G. (2013) · PLoS ONE · doi:10.1371/journal.pone.0052416 · Cited by 57 · see citing works
“The energy status of an animal, depending on its dietary regimen/intake is known to regulate diverse physiological functions as well as alter estradiol and testosterone levels in males and females [45].”
Background
Central Role of the EGF Receptor in Neurometabolic Aging
Siddiqui, S., Fang, M., Ni, B., Lu, D., Martin, B., & Maudsley, S. R. (2012) · International Journal of Endocrinology · doi:10.1155/2012/739428 · Cited by 57 · see citing works
“It has also been demonstrated that the EGFR is localized to the anterior pituitary [70] along with EGF [71] and TGF-α [72], implicating them in the reproductive hypothalamic-pituitary axis [73].”
Background
Mild Calorie Restriction Induces Fat Accumulation in Female C57BL/6J Mice
Li, X., Cope, M. B., Johnson, M. S., Smith, D. L., & Nagy, T. R. (2009) · Obesity · doi:10.1038/oby.2009.312 · Cited by 57 · see citing works
“The response to mild CR in male mice should be tested even though it seems there are no sex-dependent differences in lipid metabolism (28).”
Background
Testosterone and Corticosterone in the Mesocorticolimbic System of Male Rats: Effects of Gonadectomy and Caloric Restriction
Tobiansky, D. J., Korol, A. M., Ma, C., Hamden, J. E., Jalabert, C., Tomm, R. J., & Soma, K. K. (2017) · Endocrinology · doi:10.1210/en.2017-00704 · Cited by 56 · see citing works
Sex as a Biological Variable in Nutrition Research: From Human Studies to Animal Models
Chen, Y., Kim, M., Paye, S. M., & Benayoun, B. A. (2022) · Annual Review of Nutrition · doi:10.1146/annurev-nutr-062220-105852 · Cited by 56 · see citing works
Withania somnifera leaf alleviates cognitive dysfunction by enhancing hippocampal plasticity in high fat diet induced obesity model
Manchanda, S., & Kaur, G. (2017) · BMC Complementary and Alternative Medicine · doi:10.1186/s12906-017-1652-0 · Cited by 53 · see citing works
“condition in males is attributed to their less energy expenditure as compared to females on HFD despite the similar energy intake requirements in both males and females [25, 27].”
Background
Conserved and Differential Effects of Dietary Energy Intake on the Hippocampal Transcriptomes of Females and Males
Martin, B., Pearson, M., Brenneman, R., Golden, E. J., Keselman, A., Iyun, T., Carlson, O. D., Egan, J. M., Becker, K. G., Wood, W. H., et al. (2008) · PLoS ONE · doi:10.1371/journal.pone.0002398 · Cited by 51 · see citing works
Sex differences in the responses of orexin neurons in the lateral hypothalamic area and feeding behavior to fasting
Funabashi, T., Hagiwara, H., Mogi, K., Mitsushima, D., Shinohara, K., & Kimura, F. (2009) · Neuroscience Letters · doi:10.1016/j.neulet.2009.07.035 · Cited by 48 · see citing works
Accelerated cognitive aging in diabetic rats is prevented by lowering corticosterone levels
Stranahan, A. M., Lee, K. M., Pistell, P. J., Nelson, C. M., Readal, N., Miller, M. G., Spangler, E. L., Ingram, D. K., & Mattson, M. P. (2008) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2008.05.005 · Cited by 48 · see citing works
“Rats were tested in the 14-unit T-maze as described previously (Martin et al., 2007; Supplementary Movie 1).”
Method
Monoamine Oxidases Regulate Telencephalic Neural Progenitors in Late Embryonic and Early Postnatal Development
Cheng, A., Scott, A. L., Ladenheim, B., Chen, K., Ouyang, X., Lathia, J. D., Mughal, M. R., Cadet, J. L., Mattson, M. P., & Shih, J. C. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.2037-10.2010 · Cited by 47 · see citing works
“electrochemical detection, as described previously (Ladenheim et al., 2000; Krasnova et al., 2007; Martin et al., 2007).”
Method
Sustained fertility from 22 to 41 years of age in women with polycystic ovarian syndrome
Mellembakken, J. R., Berga, S. L., Kilen, M., Tanbo, T. G., Åbyholm, T., & Fedorcsák, P. (2011) · Human Reproduction · doi:10.1093/humrep/der214 · Cited by 47 · see citing works
“(Martin et al., 2007).”
MyomiRs as Markers of Insulin Resistance and Decreased Myogenesis in Skeletal Muscle of Diet-Induced Obese Mice
Frias, F. D. T., de Mendonça, M., Martins, A. R., Gindro, A. F., Cogliati, B., Curi, R., & Rodrigues, A. C. (2016) · Frontiers in Endocrinology · doi:10.3389/fendo.2016.00076 · Cited by 43 · see citing works
“Researchers have shown reducing daily food intake or providing exercise training results in increased plasma adiponectin and reduced insulin levels (34) and increases whole body insulin sensitivity mainly related to raised skeletal muscle glucose”
Background
ICV leptin effects on spontaneous physical activity and feeding behavior in rats
Choi, Y., Li, C., Hartzell, D. L., Little, D. E., Della‐Fera, M. A., & Baile, C. A. (2007) · Behavioural Brain Research · doi:10.1016/j.bbr.2007.10.024 · Cited by 41 · see citing works
The Role of Steroid Hormones in the Modulation of Neuroinflammation by Dietary Interventions
Vasconcelos, A. R., Cabral‐Costa, J. V., Mazucanti, C. H., Scavone, C., & Kawamoto, E. M. (2016) · Frontiers in Endocrinology · doi:10.3389/fendo.2016.00009 · Cited by 41 · see citing works
“Other studies also showed DER to inhibit estradiol levels (29, 30).”
Background
Adipose tissue loss in adjuvant arthritis is associated with a decrease in lipogenesis, but not with an increase in lipolysis
Martı́n, A. I., Castillero, E., Granado, M., López-Menduiña, M., Villanúa, M. A., & López‐Calderón, A. (2008) · Journal of Endocrinology · doi:10.1677/joe-07-0491 · Cited by 40 · see citing works
Gonadal Transcriptome Alterations in Response to Dietary Energy Intake: Sensing the Reproductive Environment
Martin, B., Pearson, M., Brenneman, R., Golden, E. J., Wood, W. H., Prabhu, V. V., Becker, K. G., Mattson, M. P., & Maudsley, S. R. (2009) · PLoS ONE · doi:10.1371/journal.pone.0004146 · Cited by 39 · see citing works
“The availability of energy in the form of food is a critical factor in the maintenance of the reproductive capacity of mammals. Low, moderate and high levels of dietary energy intake can affect reproductive function in different ways. Maintaining reproductive capacity is an energy-consuming process which is tightly re…”
Background
Neuroprotection provided by dietary restriction in rats is further enhanced by reducing glucocortocoids
Qiu, G., Spangler, E. L., Wan, R., Miller, M. G., Mattson, M. P., So, K., de Cabo, R., Zou, S., & Ingram, D. K. (2012) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2011.11.025 · Cited by 36 · see citing works
“Studies of DR in rodent models have provided consistent support for the hypothesis that a substantial (20–40%) decrease in calories consumed both sustains neuronal viability and neuroprotection when faced with an insult, such as stroke or exposure to a neurotoxin (Martin et al., 2007; Mattson, 2010).”
Age-related synapse loss in hippocampal CA3 is not reversed by caloric restriction
Adams, M. M., Donohue, H. S., Linville, M. C., Iversen, E., Newton, I. G., & Brunso-Bechtold, J. K. (2010) · Neuroscience · doi:10.1016/j.neuroscience.2010.09.022 · Cited by 34 · see citing works
High fat diet intake during pre and periadolescence impairs learning of a conditioned place preference in adulthood
Privitera, G. J., Zavala, A. R., Sanabria, F., & Sotak, K. L. (2011) · Behavioral and Brain Functions · doi:10.1186/1744-9081-7-21 · Cited by 33 · see citing works
“Animal studies show impaired learning, spatial memory, memory retention, and hippocampal synaptic plasticity in genetically obese animal models and HF diet-induced obesity models [ 12-15 ].”
GIT2 Acts as a Systems-Level Coordinator of Neurometabolic Activity and Pathophysiological Aging
Martin, B., Chadwick, W., Janssens, J., Premont, R. T., Schmalzigaug, R., Becker, K. G., Lehrmann, E., Wood, W. H., Zhang, Y., Siddiqui, S., et al. (2016) · Frontiers in Endocrinology · doi:10.3389/fendo.2015.00191 · Cited by 34 · see citing works
“Therapeutic interventions, such as caloric restriction or visceral fat depletion, designed to address features of metabolic/ glycemic aging, have succeeded in improving insulinotropic activity and life span in rodents (7, 8).”
Background
Chronic dietary creatine enhances hippocampal-dependent spatial memory, bioenergetics, and levels of plasticity-related proteins associated with NF-κB
Snow, W. M., Cadonic, C., Cortes-Perez, C., Roy Chowdhury, S. K., Djordjevic, J., Thomson, E., Bernstein, M. J., Suh, M., Fernyhough, P., & Albensi, B. C. (2018) · Learning & Memory · doi:10.1101/lm.046284.117 · Cited by 31 · see citing works
“Food intake and weight gain To confirm that food intake was not affected by supplementation with Cr, as caloric restriction has been associated with improved learning and memory in mice (Martin et al. 2007), food intake data (mean g/day/g body weight) were analyzed across weeks and between groups.”
Method
Brain-derived neurotrophic factor not associated with metabolic syndrome but inversely correlated with vascular cell adhesion molecule-1 in men without diabetes
Lee, I., Lee, W., Tsai, I., Liang, K., Lin, S., Wan, C., Fu, C., & Sheu, W. H. (2012) · Clinica Chimica Acta · doi:10.1016/j.cca.2012.02.013 · Cited by 31 · see citing works
“Under conditions of energy scarcity, the responses of BDNF also differed between men and women [23].”
Background
Plasma Brain-Derived Neurotrophic Factor and Reverse Dipping Pattern of Nocturnal Blood Pressure in Patients with Cardiovascular Risk Factors
Kadoya, M., Koyama, H., Kanzaki, A., Kurajoh, M., Hatayama, M., Shiraishi, J., Okazaki, H., Shoji, T., Moriwaki, Y., Yamamoto, T., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0105977 · Cited by 31 · see citing works
“In a study of rodents, the cortical level of BDNF was correlated with circulating BDNF concentration [33], while another study showed that BDNF concentration in plasma was unrelated to levels found in the cortex and hippocampus [34].”
Result
Need for gender-specific pre-analytical testing: The dark side of the moon in laboratory testing
Franconi, F., Rosano, G. M. C., & Campesi, I. (2014) · International Journal of Cardiology · doi:10.1016/j.ijcard.2014.11.019 · Cited by 30 · see citing works
“Male rats maintain body weight better than females and do not have altered activity or cognitive ability after starvation [128].”
Mini review: The relationship between energy status and adult hippocampal neurogenesis
Landry, T., & Hu, H. (2021) · Neuroscience Letters · doi:10.1016/j.neulet.2021.136261 · Cited by 30 · see citing works
A rosemary extract enriched in carnosic acid improves circulating adipocytokines and modulates key metabolic sensors in lean Zucker rats: Critical and contrasting differences in the obese genotype
Romo‐Vaquero, M., Larrosa, M., Yáñez-Gascón, M. J., Issaly, N., Flanagan, J., Roller, M., Tomás-Barberán, F. A., Espı́n, J. C., & García‐Conesa, M. (2013) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.201300524 · Cited by 29 · see citing works
Stress effects on rats chronically receiving a highly palatable diet are sex-specific
Fachin, A., Silva, R. K. S., Noschang, C. G., Pettenuzzo, L. F., Bertinetti, L., Billodre, M. N., Peres, W., Busnello, F. M., & Dalmaz, C. (2008) · Appetite · doi:10.1016/j.appet.2008.04.016 · Cited by 29 · see citing works
Brain-derived neurotrophic factor, but not body weight, correlated with a reduction in depression scale scores in men with metabolic syndrome: a prospective weight-reduction study
Lee, I., Fu, C., Lee, W., Liang, K., Lin, S., Wan, C., & Sheu, W. H. (2014) · Diabetology & Metabolic Syndrome · doi:10.1186/1758-5996-6-18 · Cited by 28 · see citing works
“[32] reported improved cognitive function and increased circulating BDNF in rats undergoing energy restriction.”
Background
Satiety Associated with Calorie Restriction and Time-Restricted Feeding: Central Neuroendocrine Integration
Tacad, D. K., Tovar, A. P., Richardson, C. E., Horn, W. F., Keim, N. L., Krishnan, G. P., & Krishnan, S. (2022) · Advances in Nutrition · doi:10.1093/advances/nmac011 · Cited by 27 · see citing works
Altered Hypothalamic Protein Expression in a Rat Model of Huntington's Disease
Cong, W., Cai, H., Wang, R., Daimon, C. M., Maudsley, S. R., Raber, K. A., Canneva, F., von Hörsten, S., & Martin, B. (2012) · PLoS ONE · doi:10.1371/journal.pone.0047240 · Cited by 27 · see citing works
Lysosomes Mediate Benefits of Intermittent Fasting in Cardiometabolic Disease: The Janitor Is the Undercover Boss
Mani, K. M., Javaheri, A., & Diwan, A. (2018) · Comprehensive physiology · doi:10.1002/cphy.c180005 · Cited by 27 · see citing works
The Relaxin-3 Receptor, RXFP3, Is a Modulator of Aging-Related Disease
Leysen, H., Walter, D., Clauwaert, L., Hellemans, L., van Gastel, J., Vasudevan, L., Martin, B., & Maudsley, S. R. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23084387 · Cited by 25 · see citing works
“Multiple experimental animal and longitudinal studies have demonstrated that dietinduced obesity promotes pro-aging phenotypes [84,97,171,172].”
Background
Reduced energy intake: the secret to a long and healthy life?
Martin, B., Golden, E. J., Egan, J. M., Mattson, M. P., & Maudsley, S. R. (2007) · PubMed · Cited by 25 · see citing works
Stress Hormone and Reproductive System in Response to Honey Supplementation Combined with Different Jumping Exercise Intensities in Female Rats
Mosavat, M., Ooi, F., & Mohamed, M. (2014) · BioMed Research International · doi:10.1155/2014/123640 · Cited by 23 · see citing works
“It was reported that low energy availability by reducing the circulation of insulin [31] and insulin-like growth factor I (IGF-I) can cause increment of IGF-binding protein (IGFBP-1) level and cortisol level.”
Background
Metabolic regulation of aging and age-related disease
Hamrick, M. W., & Stranahan, A. M. (2020) · Ageing Research Reviews · doi:10.1016/j.arr.2020.101175 · Cited by 26 · see citing works
“High-fat diet-induced obesity had no effect on cognitive performance in males or females (Martin et al, 2007), but the 14-unit T-maze task used to assess cognition recruits different structures and circuits than classical hippocampus-dependent paradigms.”
Background
Gender Differences in Response to Prolonged Every-Other-Day Feeding on the Proliferation and Apoptosis of Hepatocytes in Mice
Piotrowska, K., Tarnowski, M., Zgutka, K., & Pawlik, A. (2016) · Nutrients · doi:10.3390/nu8030176 · Cited by 23 · see citing works
“There are also data indicating gender differences in response to caloric restriction, or pharmacological treatment mimicking caloric restriction (CR) action [19–21].”
Background
Influence of Food Restriction Combined with Voluntary Running on Bone Morphology and Strength in Male Rats
Hattori, S., Park, J.-H., Agata, U., Akimoto, T., Oda, M., Higano, M., Aikawa, Y., Nabekura, Y., Yamato, H., Ezawa, I., et al. (2013) · Calcified Tissue International · doi:10.1007/s00223-013-9787-6 · Cited by 23 · see citing works
“In contrast, a 40 % caloric restriction did not affect the serum androgen concentration in male rats [39], while a 50 % caloric restriction caused a decrease in androgen concentration in male musk shrews [41].”
Background
Amitriptyline Improves Motor Function via Enhanced Neurotrophin Signaling and Mitochondrial Functions in the Murine N171-82Q Huntington Disease Model
Cong, W., Chadwick, W., Wang, R., Daimon, C. M., Cai, H., Amma, J., Wood, W. H., Becker, K. G., Martin, B., & Maudsley, S. R. (2014) · Journal of Biological Chemistry · doi:10.1074/jbc.m114.588608 · Cited by 22 · see citing works
“Plasma metabolic hormones, including insulin, leptin, peptide YY (PYY), gastric inhibitory peptide (GIP), and pancreatic peptide (PP), were measured using a rodent multiplex assay kit (Millipore, Billerica, MA) as described previously (32).”
Method
Meal pattern alterations associated with intermittent fasting for weight loss are normalized after high-fat diet re-feeding
Gotthardt, J. D., & Bello, N. T. (2017) · Physiology & Behavior · doi:10.1016/j.physbeh.2017.02.046 · Cited by 22 · see citing works
Intermittent calorie restriction largely counteracts the adverse health effects of a moderate‐fat diet in aging C57BL/6J mice
Rusli, F., Lute, C., Boekschoten, M. V., van Dijk, M., van Norren, K., Menke, A. L., Müller, M. M., & Steegenga, W. T. (2016) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.201600677 · Cited by 19 · see citing works
Homeostatic Regulation of Estrus Cycle of Young Female Mice on Western Diet
Lenert, M. E., Chaparro, M. M., & Burton, M. D. (2021) · Journal of the Endocrine Society · doi:10.1210/jendso/bvab010 · Cited by 20 · see citing works
Effect of mahanimbine, an alkaloid from curry leaves, on high‐fat diet‐induced adiposity, insulin resistance, and inflammatory alterations
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Expression of cholesterol homeostasis genes in the brain of the male rat is affected by age and dietary restriction
Perović, M., Mladenović, A., Smiljanić, K., Tanić, N., Rakić, L., Ruždijić, S., & Kanazir, S. (2009) · Biogerontology · doi:10.1007/s10522-009-9220-8 · Cited by 20 · see citing works
“Since females and males play different roles in survival of the species, a different respond to dietary manipulation could be expected (Martin et al. 2007).”
BackgroundInfluential
The effect of four-week intermittent fasting from dawn to sunset on circulating brain-derived neurotrophic factor levels in subjects with metabolic syndrome and healthy subjects
Abdulsada, M. M., Wilhelm, Z. R., Opekun, A. R., Devaraj, S., Jalal, P. K., & Mindikoglu, A. L. (2020) · Metabolism Open · doi:10.1016/j.metop.2020.100070 · Cited by 19 · see citing works
“Another study conducted in rats showed that while hippocampus BDNF levels decreased in female and male rats with alternate-day fasting, plasma BDNF levels increased in female rats and had no change in male rats [9].”
Background
Effects of dehydroepiandrosterone alone or in combination with a high-fat diet and antibiotic cocktail on the heterogeneous phenotypes of PCOS mouse models by regulating gut microbiota
Wang, X., Gu, L., Zhang, Y., Xiong, C., Peng, Y., & Ding, X. (2022) · Frontiers in Endocrinology · doi:10.3389/fendo.2022.1030151 · Cited by 19 · see citing works
“(41) found that caloric restriction led females become ceased cycling and underwent endocrine masculinization.”
Background
Insulin resistance and brain-derived neurotrophic factor levels in chronic kidney disease
Marchelek‐Myśliwiec, M., Cichocka, E., Dziedziejko, V., Dutkiewicz, E., Stępniewska, J., Safranow, K., Budkowska, M., Sałata, D., Syrenicz, A., Machaliński, B., et al. (2014) · Annals of Clinical Biochemistry International Journal of Laboratory Medicine · doi:10.1177/0004563214533514 · Cited by 19 · see citing works
“In contrast, animal studies have shown that high concentrations of estrogens improve memory.(15) Diabetes mellitus type 2 is a condition with a potent suppressive effect on BDNF concentrations.”
Result
Effect of diet-induced obesity on kisspeptin-neurokinin B-dynorphin A neurons in the arcuate nucleus and luteinizing hormone secretion in sex hormone-primed male and female rats
Minabe, S., Iwata, K., Tsuchida, H., Tsukamura, H., & Ozawa, H. (2021) · Peptides · doi:10.1016/j.peptides.2021.170546 · Cited by 19 · see citing works

Conserved and Differential Effects of Dietary Energy Intake on the Hippocampal Transcriptomes of Females and Males
Martin, B., Pearson, M., Brenneman, R., Golden, E. J., Keselman, A., Iyun, T., Carlson, O. D., Egan, J. M., Becker, K. G., Wood, W. H., et al. (2008) · PLoS ONE · doi:10.1371/journal.pone.0002398 · Cited by 51 · see citing works
Sex-related differences in energy balance in response to caloric restriction.
Valle, A., Català-Niell, A., Colom, B., García-Palmer, F., Oliver, J., & Roca, P. (2005) · American Journal of Physiology. Endocrinology and Metabolism · doi:10.1152/ajpendo.00553.2004 · Cited by 103 · see citing works
Sex-specific resilience of neocortex to food restrictionPreprint
Padamsey, Z., Katsanevaki, D., Maeso, P. A., Rizzi, M., Osterweil, E. K., & Rochefort, N. L. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.10.06.561185
Characterization of the metabolic differences between male and female C57BL/6 mice
de Souza, G. O., Wasinski, F., & Donato, J. (2022) · Life Sciences · doi:10.1016/j.lfs.2022.120636 · Cited by 98 · see citing works
Sex differences in response to short-term high fat diet in mice
Huang, K.-P., Ronveaux, C. C., Knotts, T. A., Rutkowsky, J. M., Ramsey, J. J., & Raybould, H. E. (2020) · Physiology & Behavior · doi:10.1016/j.physbeh.2020.112894 · Cited by 92 · see citing works

Authors: Martin, B., Pearson, M., Kebejian, L., Golden, E., Keselman, A., Bender, M., Carlson, O., Egan, J., Ladenheim, B., Cadet, J.-L., Becker, K. G., Wood, W., Duffy, K., Vinayakumar, P., Maudsley, S., & Mattson, M. P.
Affiliations: National Institute on Drug Abuse (US)
Corresponding author: Mattson, Mark P.
ORCID: Martin, Bronwen
Carlson, Olga
Egan, Josephine
Ladenheim, Bruce
Becker, Kevin G.
Wood, William
Maudsley, Stuart
Mattson, Mark P.
Venue: Endocrinology
Publisher: The Endocrine Society
Published: 2007-09
Volume: 148
Issue: 9
Pages: 4318-4333
ISSN: 0013-7227 (ISSN-L)
1945-7170
DOI: 10.1210/en.2007-0161
PMC: PMC2622430
OpenAlex: W2044015546
Cited by: 199
References: 68
Citations by year: 2026: 1 · 2025: 6 · 2024: 10 · 2023: 7 · 2022: 11 · 2021: 9 · 2020: 6 · 2019: 5 · 2018: 6 · 2017: 5 · 2016: 11 · 2015: 7 · 2014: 14 · 2013: 11 · 2012: 14
FWCI: 7.88
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Locations: Endocrinology (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: National Institutes of Health
National Institute on Aging (Z01AG000318)
Topics: Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Regulation of Appetite and Obesity
Health Sciences › Medicine › Physiology › Dietary Effects on Health
Social Sciences › Psychology › Clinical Psychology › Eating Disorders and Behaviors
Keywords: sex differences, caloric restriction, intermittent fasting, high-fat high-glucose diet, energy metabolism, reproductive cycle, stress response, spontaneous activity, learning and memory, brain-derived neurotrophic factor, leptin, ghrelin, adiponectin, insulin, anorexia nervosa
MeSH terms: Animals, Cognition, Diet, Reducing, Fasting, Female, Hyperphagia, Lipids, Male, Motor Activity, Sex Characteristics, Rats, Sprague-Dawley, Neurotransmitter Agents, Maze Learning, Rats

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Sex-dependent metabolic, neuroendocrine, and cognitive responses to dietary energy restriction and excess

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