Cited by 147Dietary Effects on HealthGenetics, Aging, and Longevity in Model OrganismsNeurological Disease Mechanisms and Treatments

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Chronic Intermittent Fasting Improves Cognitive Functions and Brain Structures in Mice

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Li, Liaoliao, Wang, Zhi, Zuo, Zhiyi·2013·PLoS ONE

DOI 10.1371/journal.pone.0066069PMC PMC3670843

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Abstract

Obesity is a major health issue. Obesity started from teenagers has become a major health concern in recent years. Intermittent fasting increases the life span. However, it is not known whether obesity and intermittent fasting affect brain functions and structures before brain aging. Here, we subjected 7-week old CD-1 wild type male mice to intermittent (alternate-day) fasting or high fat diet (45% caloric supplied by fat) for 11 months. Mice on intermittent fasting had better learning and memory assessed by the Barnes maze and fear conditioning, thicker CA1 pyramidal cell layer, higher expression of drebrin, a dendritic protein, and lower oxidative stress than mice that had free access to regular diet (control mice). Mice fed with high fat diet was obese and with hyperlipidemia. They also had poorer exercise tolerance. However, these obese mice did not present significant learning and memory impairment or changes in brain structures or oxidative stress compared with control mice. These results suggest that intermittent fasting improves brain functions and structures and that high fat diet feeding started early in life does not cause significant changes in brain functions and structures in obese middle-aged animals.

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Figure 1 The effects of various feeding protocols on body weights and blood chemicals. Seven-week old male mice had free access to regular chow or high fat diet or were allowed to have free access to regular chow every other day (intermittent fasting) for 11 months. Their growth curves are presented in panel A. Their blood was drawn at the end of the 11-month feeding to measure lipid profiles (panels B and C), glucose, albumin and creatinine (panel D). Results are means ± S.E.M (n = 12 – 15). * P<0.05 compared with mice on regular chow ad libitum. HDL: high density lipoprotein; LDL: low density lipoprotein.CC BY · PubMed Central

Figure 2 The effects of various feeding protocols on leaning and memory. Seven-week old male mice had free access to regular chow or high fat diet or were allowed to have free access to regular chow every other day (intermittent fasting) for 11 months. They were then subjected to Barnes maze, fear conditioning and rotarod tests. The results in the training sessions and memory phase of the Barnes maze are presented in panels A and B. The fear conditioning and rotarod results are shown in panels C and D, respectively. Results are means ± S.E.M (n = 15 – 35). * P<0.05 compared with mice on regular chow ad libitum.CC BY · PubMed Central

Figure 3 The effects of various feeding protocols on CA1 pyramidal cell layer thickness, neuron-specific proteins and brain derived neurotrophic factor (BDNF) in the brain. Seven-week old male mice had free access to regular chow or high fat diet or were allowed to have free access to regular chow every other day (intermittent fasting) for 11 months. Their brains were then harvested to measure CA1 pyramidal cell layer thickness (panel A) and expression of NeuN, drebrin and synaptophysin in the cerebral cortex (panel B) and hippocampus (panel C) as well as the BDNF levels in the cerebral cortex and hippocampus (panel D). The protein abundance results in each mouse were normalized by the mean value of the corresponding protein in the regular diet-fed mice. Results are means ± S.E.M (n = 7 – 12). * P<0.05 compared with mice on regular diet ad libitum. GAPDH: glyceraldehydes 3-phosphate dehydrogenase; Hippo: hippocampus; SP: synaptophysin; RD: regular diet; IF: intermittent fasting; HFD: high fat diet.CC BY · PubMed Central

Figure 4 The effects of various feeding protocols on oxidative stress status in the brain. Seven-week old male mice had free access to regular chow or high fat diet or were allowed to have free access to regular chow every other day (intermittent fasting) for 11 months. Their brains were then harvested to measure glutathione (GSH), glutathione disulfide (GSSG), 4-hydroxy-2-nonenal (HNE) and nitrotyrosine containing proteins. The levels of GSH and GSSG and ratio of GSH/GSSG in the cerebral cortex and hippocampus are presented in panels A and B, respectively. The levels of HNE and nitrotyrosine containing proteins in the cerebral cortex and hippocampus are shown in the panels C and D. Results are means ± S.E.M (n = 8). * P<0.05 compared with mice on regular chow ad libitum.CC BY · PubMed Central

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“One day after Barnes maze test, mice were subjected to fear conditioning test as we previously described [5, 19].”
MethodSelf-citation
Intermittent Fasting: Potential Utility in the Treatment of Chronic Pain across the Clinical Spectrum
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“Previous research has revealed that long-term dietary restriction modulates synaptic protein expression in the hippocampus [1].”
BackgroundInfluential
A Single Bout of Fasting (24 h) Reduces Basal Cytokine Expression and Minimally Impacts the Sterile Inflammatory Response in the White Adipose Tissue of Normal Weight F344 Rats
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“Alternate day fasting, for example, can slow the aging process [15, 16], reduce visceral adiposity [17], improve cognitive function [15, 18] and delay the development of chronic diseases [15, 19].”
Background
Precision Nutrition and Gut–Brain Axis Modulation in the Prevention of Neurodegenerative Diseases
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“Preclinical studies in animal models indicate positive effects of intermittent fasting on cognitive functions, including improved memory performance, stimulation of neurogenesis, and reduction in neuroinflammatory processes [244,245].”
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Ebrahim, H. A., El‐Gamal, R., & Sherif, R. (2021) · Cells Tissues Organs · doi:10.1159/000519088 · Cited by 28
“IF also has a positive effect on lowering the high-density lipoprotein, cholesterol, triglyceride, and low-density lipoprotein blood levels together with body weight reduction [Li et al., 2013].”
Background
The Effects of Meal Timing and Frequency, Caloric Restriction, and Fasting on Cardiovascular Health: an Overview
Maugeri, A., & Vinciguerra, M. (2020) · Journal of Lipid and Atherosclerosis · doi:10.12997/jla.2020.9.1.140 · Cited by 20
SGLT2 inhibition to target kidney aging
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“It has also been shown that mitochondrial function is improved and amyloid plaque deposition in the brain is reduced, ameliorating age-related and neurodegeneration disease [52 , 53 ].”
Background
Intermittent fasting promotes anxiolytic-like effects unrelated to synaptic mitochondrial function and BDNF support
Carteri, R. B., Menegassi, L. N., Feldmann, M., Kopczynski, A., Rodolphi, M. S., Strogulski, N. R., Almeida, A. S., Marques, D. M., Porciúncula, L. O., & Portela, L. V. (2021) · Behavioural Brain Research · doi:10.1016/j.bbr.2021.113163 · Cited by 21
Effect of Intermittent Feeding on Gonadal Function in Male And Female NMRI Mice During Chronic Stress
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“Pertinent to our findings, undernutrition has been shown to positively impact behavior in that intermittent fasting has been shown to improve Barnes maze performance and fear conditioning [71].”
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Nutrient-epigenome interactions: Implications for personalized nutrition against aging-associated diseases
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Intermittent fasting increases the expressions of SODs and catalase in granule and polymorphic cells and enhances neuroblast dendrite complexity and maturation in the adult gerbil dentate gyrus
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“Furthermore, Li et al (1) reported that, for 11 months of ImF, significant body weight change in adult CD-1 mice (7-week old) appeared after 37 weeks (around 9 months) of ImF.”
BackgroundMethod
Every-Other Day Fasting Prevents Memory Impairment Induced by High Fat-Diet: Role of Oxidative Stress.
Alzoubi, K., Khabour, O., Al-Awad, R. M., & Aburashed, Z. O. (2020) · Physiology and Behavior · doi:10.1016/j.physbeh.2020.113263 · Cited by 14
Intermittent fasting increases SOD2 and catalase immunoreactivities in the hippocampus but does not protect from neuronal death following transient ischemia in gerbils
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“Animals were fed commercially available rodent normal diet or IF (24 h fasting and 24 h feeding) was applied for 2 months according to method by published methods (9,12,17).”
Method
Isoflurane unveils a critical role of glutamate transporter type 3 in regulating hippocampal GluR1 trafficking and context-related learning and memory in mice
Cao, J., Wang, Z., Mi, W., & Zuo, Z. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2014.04.049 · Cited by 16
“Fear conditioning test Fear conditioning was performed by using the Freeze Monitor from San Diego Instruments (San Diego, CA) as we described before (Lin and Zuo, 2011; Li et al., 2013).”
MethodSelf-citation
Autophagy: Biology and Diseases: Clinical Science
Le, W., & Crusio, W. E. (2020) · doi:10.1007/978-981-15-4272-5 · Cited by 14
“Likewise, ANXA7 has become a leading compound for therapeutic drug development as it may have anti-atherosclerotic effects (Li et al. 2013a).”
BackgroundInfluential
Glucose Metabolism and Metabolomic Changes in Response to Prolonged Fasting in Individuals with Obesity, Type 2 Diabetes and Non-Obese People—A Cohort Trial
Tripolt, N. J., Hofer, S. J., Pferschy, P. N., Aziz, F., Durand, S., Aprahamian, F., Nirmalathasan, N., Waltenstorfer, M., Eisenberg, T., Obermayer, A. M., et al. (2023) · Nutrients · doi:10.3390/nu15030511 · Cited by 16
“Moreover, animal studies suggested neuroprotective effects [5] and an improvement of learning and memory after prolonged fasting in mice [6].”
Background
Neurobiological Mechanisms Modulating Emotionality, Cognition and Reward-Related Behaviour in High-Fat Diet-Fed Rodents
Ziemens, D., Touma, C., & Rappeneau, V. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23147952 · Cited by 15
High-fat diet reduces neuroprotection of isoflurane post-treatment: Role of carboxyl-terminal modulator protein-Akt signaling
Yu, H., Deng, J., & Zuo, Z. (2014) · Obesity · doi:10.1002/oby.20879 · Cited by 12
“The cytosolic fraction of the whole hippocampus or hippocampal slices after being exposed to various experimental conditions was prepared as we previously described (20,21).”
Self-citation
Repeated Sense of Hunger Leads to the Development of Visceral Obesity and Metabolic Syndrome in a Mouse Model
Han, J., Kim, H.-G., Lee, J., Choi, M., Kim, Y., & Son, C. (2014) · PLoS ONE · doi:10.1371/journal.pone.0098276 · Cited by 13
“Frequently, people in modern society attempt to reduce their body weight using a calorie-controlled diet and intermittent fasting over a short period [6,7].”
Background
Intermittent fasting alerts neurotransmitters and oxidant/antioxidant status in the brain of rats
Abdel-Rahman, M., Hussein, A. A., Ahmed-Farid, O. A.-H., Sawi, A. A., & Moneim, A. E. A. (2024) · Metabolic Brain Disease · doi:10.1007/s11011-024-01415-7 · Cited by 16
“Li et al. ( 2013 ) investigated how IF affected the expression of dopamine receptors.”
Background
Intermittent fasting—The new lifestyle?
Khedkar, P. H. (2020) · Acta Physiologica · doi:10.1111/apha.13518 · Cited by 13
Modulation of frailty syndrome by diet: A review of evidence from mouse studies
Mitchell, S. J., Mitchell, G. J., & Mitchell, J. R. (2019) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2019.04.003 · Cited by 11
Dietary-dependent sensitization of neuronal leptin signaling promotes neural repair after injury via cAMP and gene transcription
Chadwick, J., Decourt, C., Müller, F., Maldonado-Lasuncion, I., Serger, E., Kong, G., Zhou, L., Song, Y., Yan, Y., Yuan, Z., et al. (2025) · Neuron · doi:10.1016/j.neuron.2025.07.016 · Cited by 9
Intermittent Fasting Improves Social Interaction and Decreases Inflammatory Markers in Cortex and Hippocampus
García‐Juárez, M., García-Rodríguez, A., Cruz-Carrillo, G., Flores-Maldonado, O. E., Becerril-García, M. A., Garza‐Ocañas, L., Torre-Villalvazo, I., & Camacho‐Morales, A. (2024) · Molecular Neurobiology · doi:10.1007/s12035-024-04340-z · Cited by 11
“This is consistent with other studies that reported fasting reduced oxidative stress in cortex and hippocampus, as well as improved memory and learning [126] and decreased JNK signaling in senescence-accelerated mice P8 (SAMP8) [127].”
Neuroprotective Effects of Intermittent Fasting in the Aging Brain
Dong, H., Wang, S., Hu, C., Wang, M., Zhou, T., & Zhou, Y. (2024) · Annals of Nutrition and Metabolism · doi:10.1159/000538782 · Cited by 20
Intermittent fasting favored the resolution of Salmonella typhimurium infection in middle-aged BALB/c mice
Campos-Rodríguez, R., Godínez-Victoria, M., Reyna-Garfias, H., Arciniega-Martínez, I., Reséndiz-Albor, A., Abarca-Rojano, E., Cruz-Hernández, T., & Drago-Serrano, M. (2016) · AGE · doi:10.1007/s11357-016-9876-3 · Cited by 10
Effects of Caloric Restriction and Intermittent Fasting and Their Combined Exercise on Cognitive Functioning: A Review
Wang, J., Rang, Y., & Liu, C. (2024) · Current Nutrition Reports · doi:10.1007/s13668-024-00570-8 · Cited by 11
“In the mouse model, 11 months of IF not only increased the thickness of the CA1 pyramidal cell layer and the expression of the dendritic protein drebrin in the hippocampus but also reduced the occurrence of oxidative stress [21].”
Food restriction modifies ultrastructure of hippocampal synapses
Babits, R., Szőke, B., Sótonyi, P., & Rácz, B. (2015) · Hippocampus · doi:10.1002/hipo.22533 · Cited by 12
“Intermittent fasting – a widely used form of dietary restriction – has been shown to improve learning and memory (Li et al., 2013), and dietary restriction has been shown to enhance performance in tests of learning and memory (Fontan-Lozano et al., 2007; Adams et al., 2008; Mattson, 2010), while…”
Background
Systemic and transcriptional response to intermittent fasting and fasting-mimicking diet in mice
Michenthaler, H., Duszka, K., Reinisch, I., Galhuber, M., Moyschewitz, E., Stryeck, S., Madl, T., Prokesch, A., & Krstić, J. (2024) · BMC Biology · doi:10.1186/s12915-024-02061-2 · Cited by 8
Therapeutic effects of intermittent fasting on high-fat, high-fructose diet; involvement of jejunal aquaporin 1, 3, and 7
Elhessy, H. M., Berika, M. Y., Salem, Y. G., El-Desoky, M. M., Eldesoqui, M. B., Mostafa, N., Habotta, O. A., & Lashine, N. H. (2024) · Heliyon · doi:10.1016/j.heliyon.2024.e28436 · Cited by 7
Improvements during long-term fasting in patients with long COVID – a case series and literature review
Grundler, F., Mesnage, R., Cerrada, A., & de Toledo, F. W. (2023) · Frontiers in Nutrition · doi:10.3389/fnut.2023.1195270 · Cited by 11
“In the rodent brain, fasting reduced oxidative stress (29) and enhanced mitochondrial oxidative metabolism (30).”
Background
Influence of intermittent fasting on prediabetes-induced neuropathy: Insights on a novel mechanistic pathway
Dannawi, M., Riachi, M. E., Haddad, A. F., Massry, M. E., Haddad, M. E., Moukarzel, P., Harb, F., Ghadieh, H. E., & Eid, A. A. (2022) · Metabolism Open · doi:10.1016/j.metop.2022.100175 · Cited by 7
“Hence, this provides a plausible explanation of the observed non-significant difference of ROS production between IF groups while its effect on CYP1a1/a2 expression and other parameter differ significantly [62,63].”
Background
Long-Term Shaping of Corticostriatal Synaptic Activity by Acute Fasting
Campanelli, F., Laricchiuta, D., Natale, G., Marino, G., Calabrese, V., Picconi, B., Petrosini, L., Calabresi, P., & Ghiglieri, V. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22041916 · Cited by 8
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Method
Progress of Anti-aging Drugs Targeting Autophagy.
Bao, J., Liu, B., & Wu, C.-F. (2020) · Advances in Experimental Medicine and Biology · doi:10.1007/978-981-15-4272-5_50 · Cited by 7
Linoleic Acid and Alpha-Linolenic Acid Have Central Roles in Brain Energy Substrate Provision, Endogenous Lipid Production, Immune and Repair Function, via Peroxisomal Beta-Oxidation-Related Pathways?
Brown, R. A. (2016) · Springer eBooks · doi:10.1007/978-3-319-40458-5_30 · Cited by 9
Potential role for vitamin D vs. intermittent fasting in controlling aquaporin-1 and aquaporin-3 expression in HFD-induced urinary bladder alterations in rats
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“As indicated by Li et al. (2013), who discovered that a 40% reduction in caloric intake lowers oxidative stress in several parts of the brain, IF-induced caloric restriction also enhances the level of the brain ’ s redox state.”
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Influence of long-term fasting and intermittent fasting on the cognitive abilities
Crhová, M., & Kapounková, K. (2020) · Studia sportiva · doi:10.5817/sts2020-1-2 · Cited by 7
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Long-Term Alternating Fasting Increases Interleukin-13 in the Gerbil Hippocampus, But Does Not Protect BBB and Pyramidal Neurons From Ischemia–Reperfusion Injury
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Prevention of Neurologic Disease with Fasting
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Authors: Li, L., Wang, Z., & Zuo, Z.
Affiliations: University of Virginia (US)
Sun Yat-sen University (CN)
Corresponding author: Zuo, Zhiyi
ORCID: Li, Liaoliao
Wang, Zhi
Zuo, Zhiyi
Venue: PLoS ONE
Publisher: Public Library of Science (PLoS)
Published: 2013-06-03
Volume: 8
Issue: 6
Pages: e66069
ISSN: 1932-6203 (ISSN-L)
DOI: 10.1371/journal.pone.0066069
PMC: PMC3670843
OpenAlex: W1974661288
Cited by: 147
References: 23
Citations by year: 2026: 7 · 2025: 15 · 2024: 13 · 2023: 13 · 2022: 19 · 2021: 14 · 2020: 19 · 2019: 9 · 2018: 6 · 2017: 9 · 2016: 9 · 2015: 8 · 2014: 6
FWCI: 5.34
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
creativecommons.org/licenses/by/4.0/ (unspecified)
Locations: PLoS ONE (publishedVersion, cc-by)
Europe PMC (PubMed Central) (publishedVersion, other-oa)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders: American Heart Association (10GRNT3900019)
International Anesthesia Research Society (R01 GM065211)
National Institutes of Health (GM098308)
National Institute of General Medical Sciences (R01GM065211, R01GM098308)
Topics: Health Sciences › Medicine › Physiology (medical) › Dietary Effects on Health
Life Sciences › Biochemistry, Genetics and Molecular Biology › Aging › Genetics, Aging, and Longevity in Model Organisms
Life Sciences › Neuroscience › Neurology › Neurological Disease Mechanisms and Treatments
Keywords: intermittent fasting, alternate-day fasting, cognitive function, learning and memory, brain aging, high-fat diet, obesity, drebrin, oxidative stress, hyperlipidemia, exercise tolerance, Barnes maze, fear conditioning, middle-aged mice
MeSH terms: Aging, Animals, Cerebral Cortex, Cognition, Dietary Fats, Fasting, Male, Memory, Mice, Obese, Neuropeptides, Obesity, Exercise Tolerance, Oxidative Stress, Maze Learning, Mice, CA1 Region, Hippocampal, Diet, High-Fat

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Chronic Intermittent Fasting Improves Cognitive Functions and Brain Structures in Mice

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