Overview of age-related changes in psychomotor and cognitive functions in a prosimian primate, the gray mouse lemur (Microcebus murinus): Recent advances in risk factors and antiaging interventions.
aging
cognitive functions
gray mouse lemur (Microcebus murinus)
neurodegeneration
psychomotor functions
Journal
American journal of primatology
ISSN: 1098-2345
Titre abrégé: Am J Primatol
Pays: United States
ID NLM: 8108949
Informations de publication
Date de publication:
11 2021
11 2021
Historique:
revised:
23
09
2021
received:
03
02
2021
accepted:
25
09
2021
entrez:
27
10
2021
pubmed:
28
10
2021
medline:
25
11
2021
Statut:
ppublish
Résumé
Aging is not homogeneous in humans and the determinants leading to differences between subjects are not fully understood. Impaired glucose homeostasis is a major risk factor for cognitive decline in middle-aged humans, pointing at the existence of early markers of unhealthy aging. The gray mouse lemur (Microcebus murinus), a small lemuriform Malagasy primate, shows relatively slow aging with decreased psychomotor capacities at middle-age (around 5-year old). In some cases (∼10%), it spontaneously leads to pathological aging. In this case, some age-related deficits, such as severe cognitive decline, brain atrophy, amyloidosis, and glucoregulatory imbalance are congruent with what is observed in humans. In the present review, we inventory the changes occurring in psychomotor and cognitive functions during healthy and pathological aging in mouse lemur. It includes a summary of the cerebral, metabolic, and cellular alterations that occur during aging and their relation to cognitive decline. As nutrition is one of the major nonpharmacological antiaging strategies with major potential effects on cognitive performances, we also discuss its role in brain functions and cognitive decline in this species. We show that the overall approach of aging studies in the gray mouse lemur offers promising ways of investigation for understanding, prevention, and treatments of pathological aging in humans.
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
e23337Informations de copyright
© 2021 Wiley Periodicals LLC.
Références
Abdelhamid, A. S., Martin, N., Bridges, C., Brainard, J. S., Wang, X., Brown, T. J., Hanson, S., Jimoh, O. F., Ajabnoor, S. M., Deane, K. H. O., Song, F., & Hooper, L. (2018). Polyunsaturated fatty acids for the primary and secondary prevention of cardiovascular disease. Cochrane Database of Systematic Reviews, 7(7):CD012345. https://doi.org/10.1002/14651858.CD012345.pub2
Albert, M. (1993). Neuropsychological and neurophysiological changes in healthy adult humans across the age range. Neurobiology of Aging, 14(6), 623-625. https://doi.org/10.1016/0197-4580(93)90049-H
Alessandri, J. -M., Guesnet, P., Vancassel, S., Astorg, P., Denis, I., Langelier, B., Aïd, S., Poumès-Ballihaut, C., Champeil-Potokar, G., & Lavialle, M. (2004). Polyunsaturated fatty acids in the central nervous system: evolution of concepts and nutritional implications throughout life. Reproduction, Nutrition, Development, 44(6), 509-538.
Auer, R. N., Wieloch, T., Olsson, Y., & Siesjö, B. K. (1984). The distribution of hypoglycemic brain damage. Acta Neuropathologica, 64(3), 177-191. https://doi.org/10.1007/BF00688108
Aujard, F. (1997). Effect of vomeronasal organ removal on male socio-sexual response to female in a prosimian primate (Mircocebus murinus). Physiology and Behavior, 62(5), 1003-1008. https://doi.org/10.1016/S0031-9384(97)00206-0
Aujard, F., & Némoz-Bertholet, F. (2004). Response to urinary volatiles and chemosensory function decline with age in a prosimian primate. Physiology and Behavior, 81(4), 639-644. https://doi.org/10.1016/j.physbeh.2004.03.003
Aujard, F., & Perret, M. (1998). Age-related effects on reproductive function and sexual competition in the male prosimian primate, Microcebus murinus. Physiology and Behavior, 64(4), 513-519. https://doi.org/10.1016/S0031-9384(98)00087-0
Austad, S. N. (1993). The comparative perspective and choice of animal models in aging research. Aging Clinical and Experimental Research, 5(4), 259-267. https://doi.org/10.1007/BF03324171
Austad, S. N., & Fischer, K. E. (2011). The development of small primate models for aging research. ILAR Journal, 52(1), 78-88.
Basak, S., Mallick, R., & Duttaroy, A. K. (2020). Maternal docosahexaenoic acid status during pregnancy and its impact on infant neurodevelopment. Nutrients, 12(12), 3615. https://doi.org/10.3390/nu12123615
Beltran, W. A., Vanore, M., Ollivet, F., Nemoz-Bertholet, F., Aujard, F., Clerc, B., & Chahory, S. (2007). Ocular findings in two colonies of gray mouse lemurs (Microcebus murinus). Veterinary Ophthalmology, 10(1), 43-49. https://doi.org/10.1111/j.1463-5224.2007.00491.x
Bendlin, B. B., Canu, E., Willette, A., Kastman, E. K., McLaren, D. G., Kosmatka, K. J., Xu, G., Field, A. S., Colman, R. J., Coe, C. L., Weindruch, R. H., Alexander, A. L., & Johnson, S. C. (2011). Effects of aging and calorie restriction on white matter in rhesus macaques. Neurobiology of Aging, 32(12), 2319.e1-2319.11. https://doi.org/10.1016/j.neurobiolaging.2010.04.008
Berthelot, G., Bar-Hen, A., Marck, A., Foulonneau, V., Douady, S., Noirez, P., Zablocki-Thomas, P. B., da Silva Antero, J., Carter, P. A., Di Meglio, J. M., & Toussaint, J. F. (2019). An integrative modeling approach to the age-performance relationship in mammals at the cellular scale. Scientific Reports, 9(1), 418. https://doi.org/10.1038/s41598-018-36707-3
Berthelot, G., Johnson, S., Noirez, P., Antero, J., Marck, A., Desgorces, F. D., Pifferi, F., Carter, P. A., Spedding, M., Manoux, A. S., & Toussaint, J. F. (2019). The age-performance relationship in the general population and strategies to delay age related decline in performance. Archives of Public Health, 77(1), 51. https://doi.org/10.1186/s13690-019-0375-8
Bertrand, A., Pasquier, A., Petiet, A., Wiggins, C., Kraska, A., Joseph-Mathurin, N., Aujard, F., Mestre-Francés, N., & Dhenain, M. (2013). Micro-MRI study of cerebral aging: Ex vivo detection of hippocampal subfield reorganization, microhemorrhages and amyloid plaques in mouse lemur primates. PLoS One, 8(2), e56593. https://doi.org/10.1371/journal.pone.0056593
Biggar, K. K., Wu, C.-W., Tessier, S. N., Zhang, J., Pifferi, F., Perret, M., & Storey, K. B. (2015). Primate torpor: Regulation of stress-activated protein kinases during daily torpor in the grey mouse lemur, Microcebus murinus. Genomics, Proteomics & Bioinformatics, 13(2), 81-90. https://doi.org/10.1016/j.gpb.2015.03.002
Bizon, J. L., Foster, T. C., Alexander, G. E., & Glisky, E. L. (2012). Characterizing cognitive aging of working memory and executive function in animal models. Frontiers in Aging Neuroscience, 4, 19. https://doi.org/10.3389/fnagi.2012.00019
Bodkin, N. L., Ortmeyer, H. K., & Hansen, B. C. (1995). Long-term dietary restriction in older-aged rhesus monkeys: Effects on insulin resistance. Journals of Gerontology Series A Biological Sciences and Medical Sciences, 50(3), 142-147. https://doi.org/10.1093/gerona/50A.3.B142
Boettcher, F. A. (2002). Presbyacusis and the auditory brainstem response. Journal of Speech, Language, and Hearing Research, 45(6), 1249-1261. https://doi.org/10.1044/1092-4388(2002/100)
Bons, N., Mestre, N., & Petter, A. (1992). Senile plaques and neurofibrillary changes in the brain of an aged lemurian primate, Microcebus murinus. Neurobiology of Aging, 13(1), 99-105. https://doi.org/10.1016/0197-4580(92)90016-Q
Bons, N., Mestre, N., Ritchie, K., Petter, A., Podlisny, M., & Selkoe, D. (1994). Identification of amyloid beta protein in the brain of the small, short-lived lemurian primate Microcebus murinus. Neurobiology of Aging, 15(2), 215-220. https://doi.org/10.1016/0197-4580(94)90115-5
Bons, N., Rieger, F., Prudhomme, D., Fisher, A., & Krause, K.-H. (2006). Microcebus murinus: A useful primate model for human cerebral aging and Alzheimer's disease? Genes, Brain and Behavior, 5(2), 120-130. https://doi.org/10.1111/j.1601-183X.2005.00149.x
Buss, S. S., Padmanabhan, J., Saxena, S., Pascual-Leone, A., & Fried, P. J. (2018). Atrophy in distributed networks predicts cognition in Alzheimer's disease and type 2 diabetes. Journal of Alzheimer's Disease, 65(4), 1301-1312. https://doi.org/10.3233/JAD-180570
Cantlon, J. F., & Brannon, E. M. (2006). Shared system for ordering small and large numbers in monkeys and humans. Psychological Science, 17(5), 401-406. https://doi.org/10.1111/j.1467-9280.2006.01719.x
Carrié, I., Clément, M., de Javel, D., Francès, H., & Bourre, J. M. (2000). Phospholipid supplementation reverses behavioral and biochemical alterations induced by n-3 polyunsaturated fatty acid deficiency in mice. Journal of Lipid Research, 41(3), 473-480.
Cartee, G. D., Kietzke, E. W., & Briggs-Tung, C. (1994). Adaptation of muscle glucose transport with caloric restriction in adult, middle-aged, and old rats. American Journal of Physiology, 266(5), R1443-R1447. https://doi.org/10.1152/ajpregu.1994.266.5.r1443
Cayetanot, F., Némoz-Bertholet, F., & Aujard, F. (2005). Age effects on pheromone induced Fos expression in olfactory bulbs of a primate. Neuroreport, 16(10), 1091-1095. https://doi.org/10.1097/00001756-200507130-00012
Chetelat, G., Desgranges, B., de la Sayette, V., Viader, F., Berkouk, K., Landeau, B., Lalevée, C., Le Doze, F., Dupuy, B., Hannequin, D., Baron, J.-C., & Eustache, F. (2003). Dissociating atrophy and hypometabolism impact on episodic memory in mild cognitive impairment. Brain: A Journal of Neurology, 126(Pt 9), 1955-1967. https://doi.org/10.1093/brain/awg196
Chi, C. P., & Roberts, E. L. (2003). Energy substrates for neurons during neural activity: A critical review of the astrocyte-neuron lactate shuttle hypothesis. Journal of Cerebral Blood Flow and Metabolism, 23(11), 1263-1281. https://doi.org/10.1097/01.wcb.0000081369.51727.6f
Chiocchetti, R., Hitrec, T., Giancola, F., Sadeghinezhad, J., Squarcio, F., Galiazzo, G., Piscitiello, E., De Silva, M., Cerri, M., Amici, R., & Luppi, M. (2021). Phosphorylated Tau protein in the myenteric plexus of the ileum and colon of normothermic rats and during synthetic torpor. Cell and Tissue Research, 384, 287-299. https://doi.org/10.1007/s00441-020-03328-0
Cohen, N. J., & Squire, L. R. (1980). Preserved learning and retention of pattern-analyzing skill in amnesia: Dissociation of knowing how and knowing that. Science, 210(4466), 207-210. https://doi.org/10.1126/science.7414331
Colman, R. J., Anderson, R. M., Johnson, S. C., Kastman, E. K., Kosmatka, K. J., Beasley, T. M., Allison, D. B., Cruzen, C., Simmons, H. A., Kemnitz, J. W., & Weindruch, R. (2009). Caloric restriction delays disease onset and mortality in rhesus monkeys. Science, 325(5937), 201-204. https://doi.org/10.1126/science.1173635
Colman, R. J., Beasley, T. M., Kemnitz, J. W., Johnson, S. C., Weindruch, R., & Anderson, R. M. (2014). Caloric restriction reduces age-related and all-cause mortality in rhesus monkeys. Nature Communications, 5, 3557. https://doi.org/10.1038/ncomms4557
Cunnane, S. C., Plourde, M., Pifferi, F., Bégin, M., Féart, C., & Barberger-Gateau, P. (2009). Fish, docosahexaenoic acid and Alzheimer's disease. Progress in Lipid Research, 48(5), 239-256. https://doi.org/10.1016/j.plipres.2009.04.001
Dal-Pan, A., Pifferi, F., Marchal, J., Picq, J.-L., & Aujard, F. (2011). Cognitive performances are selectively enhanced during chronic caloric restriction or resveratrol supplementation in a primate. PLoS One, 6(1), e16581. https://doi.org/10.1371/journal.pone.0016581
Dal-Pan, A., Terrien, J., Pifferi, F., Botalla, R., Hardy, I., Marchal, J., Zahariev, A., Chery, I., Zizzari, P., Perret, M., Picq, J. L., Epelbaum, J., Blanc, S., & Aujard, F. (2011). Caloric restriction or resveratrol supplementation and ageing in a non-human primate: First-year outcome of the RESTRIKAL study in Microcebus murinus. Age, 33(1), 15-31. https://doi.org/10.1007/s11357-010-9156-6
Dammhahn, M., & Kappeler, P. M. (2008). Comparative feeding ecology of sympatric Microcebus berthae and M. murinus. International Journal of Primatology, 29, 1567-1589. https://doi.org/10.1007/s10764-008-9312-3
Dhenain, M., Duyckaerts, C., Michot, J. L., Volk, A., Picq, J. L., & Boller, F. (1998). Cerebral T2-weighted signal decrease during aging in the mouse lemur primate reflects iron accumulation. Neurobiology of Aging, 19(1), 65-69. https://doi.org/10.1016/S0197-4580(98)00005-0
Dirks, A. J., & Leeuwenburgh, C. (2006). Caloric restriction in humans: Potential pitfalls and health concerns. Mechanisms of Ageing and Development, 127(1), 1-7. https://doi.org/10.1016/j.mad.2005.09.001
Djelti, F., Dhenain, M., Terrien, J., Picq, J. -L., Hardy, I., Champeval, D., Perret, M., Schenker, E., Epelbaum, J., & Aujard, F. (2016). Impaired fasting blood glucose is associated to cognitive impairment and cerebral atrophy in middle-aged non-human primates. Aging, 9(1), 173-186. https://doi.org/10.18632/aging.101148
Dubicanac, M., Radespiel, U., & Zimmermann, E. (2017). A review on ocular findings in mouse lemurs: Potential links to age and genetic background. Primate Biology, 4(2), 215-228. https://doi.org/10.5194/pb-4-215-2017
Dubicanac, M., Strueve, J., Mestre-Frances, N., Verdier, J. M., Zimmermann, E., & Joly, M. (2017). Photoperiodic regime influences onset of lens opacities in a non-human primate. PeerJ, 2017(5):3258. https://doi.org/10.7717/peerj.3258
Dyall, S. C. (2015). Long-chain omega-3 fatty acids and the brain: A review of the independent and shared effects of EPA, DPA and DHA. Frontiers in Aging Neuroscience, 7, 52. https://doi.org/10.3389/fnagi.2015.00052
Ezran, C., Karanewsky, C. J., Pendleton, J. L., Sholtz, A., Krasnow, M. R., Willick, J., Razafindrakoto, A., Zohdy, S., Albertelli, M. A., & Krasnow, M. A. (2017). The mouse lemur, a genetic model organism for primate biology, behavior, and health. Genetics, 206(2), 651-664. https://doi.org/10.1534/genetics.116.199448
Ferreiro, D. N., Amaro, D., Schmidtke, D., Sobolev, A., Gundi, P., Belliveau, L., Sirota, A., Grothe, B., & Pecka, M. (2020). Sensory Island Task (SIT): A new behavioral paradigm to study sensory perception and neural processing in freely moving animals. Frontiers in Behavioral Neuroscience, 14, 576154. https://doi.org/10.3389/fnbeh.2020.576154
Fichtel, C., & Kappeler, P. M. (2002). Anti-predator behavior of group-living Malagasy primates: Mixed evidence for a referential alarm call system. Behavioral Ecology and Sociobiology, 51(3), 262-275. https://doi.org/10.1007/s00265-001-0436-0
Fichtel, C., Dinter, K., & Kappeler, P. M. (2020). The lemur baseline: How lemurs compare to monkeys and apes in the Primate Cognition Test Battery. PeerJ, 8, e10025. https://doi.org/10.7717/peerj.10025
Finch, C. E., & Austad, S. N. (2012). Primate aging in the mammalian scheme: The puzzle of extreme variation in brain aging. Age, 34(5), 1075-1091. https://doi.org/10.1007/s11357-011-9355-9
Fontana, L., Partridge, L., & Longo, V. D. (2010). Extending healthy life span-From yeast to humans. Science, 328(5976), 321-326. https://doi.org/10.1126/science.1172539
Fontán-Lozano, Á., Sáez-Cassanelli, J. L., Inda, M. C., De Los Santos-Arteaga, M., Sierra-Domínguez, S. A., López-Lluch, G., Delgado-García, J. M., & Carrión, Á. M. (2007). Caloric restriction increases learning consolidation and facilitates synaptic plasticity through mechanisms dependent on NR2B subunits of the NMDA receptor. Journal of Neuroscience, 27(38), 10185-10195. https://doi.org/10.1523/JNEUROSCI.2757-07.2007
Freemantle, E., Vandal, M., Tremblay-Mercier, J., Tremblay, S., Blachère, J.-C., Bégin, M. E., Brenna, J. T., Windust, A., & Cunnane, S. C. (2006). Omega-3 fatty acids, energy substrates, and brain function during aging. Prostaglandins, Leukotrienes, and Essential Fatty Acids, 75(3), 213-220. https://doi.org/10.1016/j.plefa.2006.05.011
Fritz, R. G., Zimmermann, E., Meier, M., Mestre-Francés, N., Radespiel, U., & Schmidtke, D. (2020). Neurobiological substrates of animal personality and cognition in a nonhuman primate (Microcebus murinus). Brain and Behavior, 10(9), e01752. https://doi.org/10.1002/brb3.1752
Fritz, R. G., Zimmermann, E., Picq, J. L., Lautier, C., Meier, M., Kästner, S., & Schmidtke, D. (2020). Sex-specific patterns of age-related cerebral atrophy in a nonhuman primate Microcebus murinus. Neurobiology of Aging, 91, 148-159. https://doi.org/10.1016/j.neurobiolaging.2020.02.027
Gallagher, M. (1993). Issues in the development of models for cognitive aging across primate and nonprimate species. Neurobiology of Aging, 14(6), 631-633. https://doi.org/10.1016/0197-4580(93)90051-C
Geijselaers, S. L. C., Sep, S. J. S., Stehouwer, C. D. A., & Biessels, G. J. (2015). Glucose regulation, cognition, and brain MRI in type 2 diabetes: A systematic review. The Lancet Diabetes & Endocrinology, 3(1), 75-89. https://doi.org/10.1016/S2213-8587(14)70148-2
Gerbi, A., Zerouga, M., Debray, M., Durand, G., Chanez, C., & Bourre, J. M. (1993). Effect of dietary alpha-linolenic acid on functional characteristic of Na+/K+-ATPase isoenzymes in whole brain membranes of weaned rats. Biochimica et Biophysica Acta, 1165(3), 291-298.
Giannakopoulos, P., Silhol, S., Jallageas, V., Mallet, J., Bons, N., Bouras, C., & Delaère, P. (1997). Quantitative analysis of tau protein-immunoreactive accumulations and β amyloid protein deposits in the cerebral cortex of the mouse lemur, Microcebus murinus. Acta Neuropathologica, 94(2), 131-139. https://doi.org/10.1007/s004010050684
Gilbert, P. E., Pirogovsky, E., Brushfield, A. M., Luu, T. T., Tolentino, J. C., & Renteria, A. F. (2009). Age-related changes in associative learning for olfactory and visual stimuli in rodents. Annals of the New York Academy of Sciences, 1170, 718-724. https://doi.org/10.1111/j.1749-6632.2009.03929.x
Guo, J., Bakshi, V., & Lin, A.-L. (2015). Early shifts of brain metabolism by caloric restriction preserve white matter integrity and long-term memory in aging mice. Frontiers in Aging Neuroscience, 7, 213. https://doi.org/10.3389/fnagi.2015.00213
Heesy, C. P. (2005). What are four trillion neurons really good for? Evolutionary Anthropology: Issues, News, and Reviews, 14(6), 238-239. https://doi.org/10.1002/evan.20078
Heilbronn, L. K., De Jonge, L., Frisard, M. I., DeLany, J. P., Larson-Meyer, D. E., Rood, J., Nguyen, T., Martin, C. K., Volaufova, J., Most, M. M., Greenway, F. L., Smith, S. R., Deutsch, W. A., Williamson, D. A., & Ravussin, E. (2006). Effect of 6-month calorie restriction on biomarkers of longevity, metabolic adaptation, and oxidative stress in overweight individuals: A randomized controlled trial. Journal of the American Medical Association, 295(13), 1539-1548. https://doi.org/10.1001/jama.295.13.1539
Hennebelle, M., Harbeby, E., Tremblay, S., Chouinard-Watkins, R., Pifferi, F., Plourde, M., Guesnet, P., & Cunnane, S. C. (2015). Challenges to determining whether DHA can protect against age-related cognitive decline. Clinical Lipidology, 10(1), 91-102. https://doi.org/10.2217/clp.14.61
Hohenbrink, P., Dempewolf, S., Zimmermann, E., Mundy, N. I., & Radespiel, U. (2014). Functional promiscuity in a mammalian chemosensory system: Extensive expression of vomeronasal receptors in the main olfactory epithelium of mouse lemurs. Frontiers in Neuroanatomy, 8, 102. https://doi.org/10.3389/fnana.2014.00102
Hohenbrink, P., Radespiel, U., & Mundy, N. I. (2012). Pervasive and ongoing positive selection in the vomeronasal-1 receptor (V1R) repertoire of mouse lemurs. Molecular Biology and Evolution, 29(12), 3807-3816. https://doi.org/10.1093/molbev/mss188
Holleschau, A. M., & Rathbun, W. B. (1994). The effects of age on glutathione peroxidase and glutathione reductase activities in lenses of old world simians and prosimians. Current Eye Research, 13(5), 331-336. https://doi.org/10.3109/02713689409167296
Hunnicutt, K. E., Tiley, G. P., Williams, R. C., Larsen, P. A., Blanco, M. B., Rasoloarison, R. M., Campbell, C. R., Zhu, K., Weisrock, D. W., Matsunami, H., & Yoder, A. D. (2019). Comparative genomic analysis of the pheromone receptor class 1 family (V1R) reveals extreme complexity in mouse lemurs (Genus, Microcebus) and a chromosomal hotspot across mammals. Genome Biology and Evolution, 12(1), 3562-3579. https://doi.org/10.1093/gbe/evz200
Indrio, F., Martini, S., Francavilla, R., Corvaglia, L., Cristofori, F., Mastrolia, S. A., Neu, J., Rautava, S., Spena, G. R., Raimondi, F., & Loverro, G. (2017). Epigenetic matters: The link between early nutrition, microbiome, and long-term health development. Frontiers in Pediatrics, 5, 178. https://doi.org/10.3389/fped.2017.00178
Jallageas, V., Privat, N., Mestre-Francés, N., & Bons, N. (1998). Age-related changes in serotonergic and catecholaminergic brain systems in the lemurian primate Microcebus murinus. Annals of the New York Academy of Sciences, 839, 628-630. https://doi.org/10.1111/j.1749-6632.1998.tb10899.x
Joffre, C., Nadjar, A., Lebbadi, M., Calon, F., & Laye, S. (2014). n-3 LCPUFA improves cognition: The young, the old and the sick. Prostaglandins, Leukotrienes, and Essential Fatty Acids, 91(1-2), 1-20. https://doi.org/10.1016/j.plefa.2014.05.001
Joly, M., Ammersdörfer, S., Schmidtke, D., & Zimmermann, E. (2014). Touchscreen-based cognitive tasks reveal age-related impairment in a primate aging model, the grey mouse lemur (Microcebus murinus). PLoS One, 9(10), e109393. https://doi.org/10.1371/journal.pone.0109393
Joly, M., Deputte, B., & Verdier, J.-M. (2006). Age effect on olfactory discrimination in a non-human primate, Microcebus murinus. Neurobiology of Aging, 27(7), 1045-1049. https://doi.org/10.1016/j.neurobiolaging.2005.05.001
Joussain, P., Bessy, M., Faure, F., Bellil, D., Landis, B. N., Hugentobler, M., Tuorila, H., Mustonen, S., Vento, S. I., Delphin-Combe, F., Krolak-Salmon, P., Rouby, C., & Bensafi, M. (2016). Application of the European Test of Olfactory Capabilities in patients with olfactory impairment. European Archives of Otorhinolaryngology, 273(2), 381-390. https://doi.org/10.1007/s00405-015-3536-6
Jung, K. J., Lee, E. K., Kim, J. Y., Zou, Y., Sung, B., Heo, H. S., Kim, M. K., Lee, J., Kim, N. D., Yu, B. P., & Chung, H. Y. (2009). Effect of short term calorie restriction on pro-inflammatory NF-κB and AP-1 in aged rat kidney. Inflammation Research, 58(3), 143-150. https://doi.org/10.1007/s00011-008-7227-2
Kemnitz, J. W., Roecker, E. B., Weindruch, R., Elson, D. F., Baum, S. T., & Bergman, R. N. (1994). Dietary restriction increases insulin sensitivity and lowers blood glucose in rhesus monkeys. American Journal of Physiology, 266, 540-547. https://doi.org/10.1152/ajpendo.1994.266.4.e540
Kitajka, K., Puskás, L. G., Zvara, A., Hackler, L., Barceló-Coblijn, G., Yeo, Y. K., & Farkas, T. (2002). The role of n-3 polyunsaturated fatty acids in brain: Modulation of rat brain gene expression by dietary n-3 fatty acids. Proceedings of the National Academy of Sciences of the United States of America, 99(5), 2619-2624. https://doi.org/10.1073/pnas.042698699
Kittler, K., Kappeler, P. M., & Fichtel, C. (2018). Instrumental problem-solving abilities in three lemur species (Microcebus murinus, Varecia variegata, and Lemur catta). Journal of Comparative Psychology, 132(3), 306-314. https://doi.org/10.1037/com0000113
Kones, R., Howell, S., & Rumana, U. (2018). N-3 polyunsaturated fatty acids and cardiovascular disease: Principles, practices, pitfalls, and promises-A contemporary review. Medical Principles and Practice, 26(6), 497-508. https://doi.org/10.1159/000485837
Kraska, A., Dorieux, O., Picq, J.--L., Petit, F., Bourrin, E., Chenu, E., Volk, A., Perret, M., Hantraye, P., Mestre-Frances, N., Aujard, F., & Dhenain, M. (2011). Age-associated cerebral atrophy in mouse lemur primates. Neurobiology of Aging, 32(5), 894-906. https://doi.org/10.1016/j.neurobiolaging.2009.05.018
Lacreuse, A., Raz, N., Schmidtke, D., Hopkins, W. D., & Herndon, J. G. (2020). Age-related decline in executive function as a hallmark of cognitive ageing in primates: An overview of cognitive and neurobiological studies. Philosophical Transactions of the Royal Society, B: Biological Sciences, 375(1811), 20190618. https://doi.org/10.1098/rstb.2019.0618
Languille, S., Aujard, F., & Pifferi, F. (2012a). Effect of dietary fish oil supplementation on the exploratory activity, emotional status and spatial memory of the aged mouse lemur, a non-human primate. Behavioural Brain Research, 235(2), 280-286. https://doi.org/10.1016/j.bbr.2012.08.014
Languille, S., Blanc, S., Blin, O., Canale, C. I., Dal-Pan, A., Devau, G., Dhenain, M., Dorieux, O., Epelbaum, J., Gomez, D., Hardy, I., Henry, P.-Y., Irving, E. A., Marchal, J., Mestre-Francés, N., Perret, M., Picq, J.-L., Pifferi, F., Rahman, A., & Aujard, F. (2012b). The grey mouse lemur: A non-human primate model for ageing studies. Ageing Research Reviews, 11, 150-162. https://doi.org/10.1016/j.arr.2011.07.001
Languille, S., Lievin-Bazin, A., Picq, J.-L., Louis, C., Dix, S., De Barry, J., Blin, O., Richardson, J., Bordet, R., Schenker, E., Djelti, F., & Aujard, F. (2015). Deficits of psychomotor and mnesic functions across aging in mouse lemur primates. Frontiers in Behavioral Neuroscience, 8, 446. https://doi.org/10.3389/fnbeh.2014.00446
Larsen, P. A., Harris, R. A., Liu, Y., Murali, S. C., Campbell, C. R., Brown, A. D., Sullivan, B. A., Shelton, J., Brown, S. J., Raveendran, M., Dudchenko, O., Machol, I., Durand, N. C., Shamim, M. S., Aiden, E. L., Muzny, D. M., Gibbs, R. A., Yoder, A. D., Rogers, J., & Worley, K. C. (2017). Hybrid de novo genome assembly and centromere characterization of the gray mouse lemur (Microcebus murinus). BMC Biology, 15(1), 110. https://doi.org/10.1186/s12915-017-0439-6
Le Bourg, E. (2018). Does calorie restriction in primates increase lifespan? Revisiting studies on macaques (Macaca mulatta) and mouse lemurs (Microcebus murinus). BioEssays, 40(10), 1800111. https://doi.org/10.1002/bies.201800111
Le Bourg, E., & Redman, L. M. (2018). Do-it-yourself calorie restriction: The risks of simplistically translating findings in animal models to humans. BioEssays, 40(9), 1800087. https://doi.org/10.1002/bies.201800087
Leybaert, L., De Bock, M., Van Moorhem, M., Decrock, E., & De Vuyst, E. (2007). Neurobarrier coupling in the brain: Adjusting glucose entry with demand. Journal of Neuroscience Research, 85(15), 3213-3220. https://doi.org/10.1002/jnr.21189
Light, L. L., & Anderson, P. A. (1985). Working-memory capacity, age, and memory for discourse. Journal of Gerontology, 40(6), 737-747. https://doi.org/10.1093/geronj/40.6.737
Liu, Z., Zhao, L., Man, Q., Wang, J., Zhao, W., & Zhang, J. (2019). Dietary micronutrients intake status among chinese elderly people living at home: Data from CNNHS 2010-2012. Nutrients, 11(8), 1787. https://doi.org/10.3390/nu11081787
Lorenzo-López, L., Maseda, A., de Labra, C., Regueiro-Folgueira, L., Rodríguez-Villamil, J. L., & Millán-Calenti, J. C. (2017). Nutritional determinants of frailty in older adults: A systematic review. BMC Geriatrics, 17(1), 108. https://doi.org/10.1186/s12877-017-0496-2
Luppi, M., Hitrec, T., Di Cristoforo, A., Squarcio, F., Stanzani, A., Occhinegro, A., Chiavetta, P., Tupone, D., Zamboni, G., Amici, R., & Cerri, M. (2019). Phosphorylation and dephosphorylation of tau protein during synthetic torpor. Frontiers in Neuroanatomy, 13, 57. https://doi.org/10.3389/fnana.2019.00057
Marchal, J., Blanc, S., Epelbaum, J., Aujard, F., & Pifferi, F. (2012). Effects of chronic calorie restriction or dietary resveratrol supplementation on insulin sensitivity markers in a primate, Microcebus murinus. PLoS One, 7(3), e34289. https://doi.org/10.1371/journal.pone.0034289
Marck, A., Berthelot, G., Foulonneau, V., Marc, A., Antero-Jacquemin, J., Noirez, P., Bronikowski, A. M., Morgan, T. J., Garland, T., Carter, P. A., Hersen, P., Di Meglio, J.-M., & Toussaint, J.-F. (2016). Age-related changes in locomotor performance reveal a similar pattern for Caenorhabditis elegans, Mus domesticus, Canis familiaris, Equus caballus, and Homo sapiens. The Journals of Gerontology Series A: Biological Sciences and Medical Sciences, 72(4), 455-463. https://doi.org/10.1093/gerona/glw136
Markowska, A. L. (1999). Life-long diet restriction failed to retard cognitive aging in Fischer-344 rats. Neurobiology of Aging, 20(2), 177-189.
Martin, A. (2001). Apports nutritionnels conseillés pour la population française (3rd ed). Tec & Doc.
Martin, S. L., Hardy, T. M., & Tollefsbol, T. O. (2013). Medicinal chemistry of the epigenetic diet and caloric restriction. Current Medicinal Chemistry, 20(32), 4050-4059.
Masoro, E. J. (2000). Dietary restriction and longevity extension as a manifestation of hormesis. Human and Ecological Risk Assessment, 6(2), 273-279. https://doi.org/10.1080/10807030009380062
Mattison, J. A., Colman, R. J., Beasley, T. M., Allison, D. B., Kemnitz, J. W., Roth, G. S., Ingram, D. K., Weindruch, R., de Cabo, R., & Anderson, R. M. (2017). Caloric restriction improves health and survival of rhesus monkeys. Nature Communications, 8, 14063. https://doi.org/10.1038/ncomms14063
Mattison, J. A., Roth, G. S., Beasley, T. M., Tilmont, E. M., Handy, A. M., Herbert, R. L., Longo, D. L., Allison, D. B., Young, J. E., Bryant, M., Barnard, D., Ward, W. F., Qi, W., Ingram, D. K., & de Cabo, R. (2012). Impact of caloric restriction on health and survival in rhesus monkeys from the NIA study. Nature, 489(7415), 318-321. https://doi.org/10.1038/nature11432
McCay, C. M., Crowell, M. F., & Maynard, L. A. (1935). The effect of retarded growth upon the length of life span and upon the ultimate body size. 1935. Nutrition, 5(3), 155-171.
Means, L. W., Higgins, J. L., & Fernandez, T. J. (1993). Mid-life onset of dietary restriction extends life and prolongs cognitive functioning. Physiology and Behavior, 54(3), 503-508. https://doi.org/10.1016/0031-9384(93)90243-9
Merritt, D., Maclean, E. L., Jaffe, S., & Brannon, E. M. (2007). A comparative analysis of serial ordering in ring-tailed lemurs (Lemur catta). Journal of Comparative Psychology, 121(4), 363-371. https://doi.org/10.1037/0735-7036.121.4.363
Merritt, D. J., MacLean, E. L., Crawford, J. C., & Brannon, E. M. (2011). Numerical rule-learning in ring-tailed Lemurs (Lemur catta). Frontiers in Psychology, 2, 23. https://doi.org/10.3389/fpsyg.2011.00023
Messier, C., Tsiakas, M., Gagnon, M., Desrochers, A., & Awad, N. (2003). Effect of age and glucoregulation on cognitive performance. Neurobiology of Aging, 24(7), 985-1003. https://doi.org/10.1016/S0197-4580(03)00004-6
Mestre-Francés, N., Keller, E., Calenda, A., Barelli, H., Checler, F., & Bons, N. (2000). Immunohistochemical analysis of cerebral cortical and vascular lesions in the primate Microcebus murinus reveal distinct amyloid β1-42 and β1-40 immunoreactivity profiles. Neurobiology of Disease, 7(1), 1-8. https://doi.org/10.1006/nbdi.1999.0270
Mobley, A. S., Rodriguez-Gil, D. J., Imamura, F., & Greer, C. A. (2014). Aging in the olfactory system. Trends in Neurosciences, 37(2), 77-84. https://doi.org/10.1016/j.tins.2013.11.004
Morris, R. G., Gick, M. L., & Craik, F. I. M. (1988). Processing resources and age differences in working memory. Memory & Cognition, 16(4), 362-366. https://doi.org/10.3758/BF03197047
Nadkarni, N. A., Bougacha, S., Garin, C., Dhenain, M., & Picq, J.-L. (2019). A 3D population-based brain atlas of the mouse lemur primate with examples of applications in aging studies and comparative anatomy. NeuroImage, 185, 85-95. https://doi.org/10.1016/j.neuroimage.2018.10.010
Nakayasu, C., Kanemura, F., Hirano, Y., Shimizu, Y., & Tonosaki, K. (2000). Sensitivity of the olfactory sense declines with the aging in senescence-accelerated mouse (SAM-P1). Physiology and Behavior, 70(1-2), 135-139. https://doi.org/10.1016/S0031-9384(00)00234-1
Nehlig, A. (1997). Cerebral energy metabolism, glucose transport and blood flow: Changes with maturation and adaptation to hypoglycaemia. Diabetes & Metabolism, 23(1), 18-29. http://www.ncbi.nlm.nih.gov/pubmed/9059763
Némoz-Bertholet, F., & Aujard, F. (2003). Physical activity and balance performance as a function of age in a prosimian primate (Microcebus murinus). Experimental Gerontology, 38(4), 407-414. https://doi.org/10.1016/S0531-5565(02)00244-9
Ohlhorst, S. D., Russell, R., Bier, D., Klurfeld, D. M., Li, Z., Mein, J. R., Milner, J., Ross, C. C., Stover, P., & Konopka, E. (2013). Nutrition research to affect food and a healthy life span. Journal of Nutrition, 143(8), 1349-1354. https://doi.org/10.3945/jn.113.180638
Olton, D. S. (1979). Mazes, maps, and memory. American Psychologist, 34(7), 583-596. https://doi.org/10.1037//0003-066x.34.7.583
Perret, M. (1995). Chemocommunication in the reproductive function of mouse lemurs. In L. Alterman, G. A. Doyle, & M. K. Izard (Eds.), Creatures of the Dark (pp. 377-392). Springer. https://doi.org/10.1007/978-1-4757-2405-9_22
Picq, J. L. (1993). Radial maze performance in young and aged grey mouse lemurs (Microcebus murinus). Primates, 34(2), 223-226. https://doi.org/10.1007/BF02381394
Picq, J. L. (1995). Effects of aging upon recent memory in Microcebus murinus. Aging, 7(1), 17-22.
Picq, J. L. (2007). Aging affects executive functions and memory in mouse lemur primates. Experimental Gerontology, 42(3), 223-232. https://doi.org/10.1016/j.exger.2006.09.013
Picq, J. L., Aujard, F., Volk, A., & Dhenain, M. (2012). Age-related cerebral atrophy in nonhuman primates predicts cognitive impairments. Neurobiology of Aging, 33(6), 1096-1109. https://doi.org/10.1016/j.neurobiolaging.2010.09.009
Picq, J. L., & Dhenain, M. (1998). Reaction to new objects and spatial changes in young and aged grey mouse lemurs (Microcebus murinus). The Quarterly Journal of Experimental Psychology, 51(4b), 337-348. https://doi.org/10.1080/02724995.1998.11733503
Picq, J. L., Dhenain, M., Michot, J.-L., Volk, A., Gauthier, C.-A., & Boller, F. (1998). Etude préliminaire du vieillissement cognitif des microcèbes murins dans une version spatiale du test de non appariement retardé. Primatologie, 1(1), 307-333.
Picq, J. L., Villain, N., Gary, C., Pifferi, F., & Dhenain, M. (2015). Jumping stand apparatus reveals rapidly specific age-related cognitive impairments in mouse lemur primates. PLoS One, 10(12), e0146238. https://doi.org/10.1371/journal.pone.0146238
Pifferi, F., Dorieux, O., Castellano, C.-A., Croteau, E., Masson, M., Guillermier, M., Van Camp, N., Guesnet, P., Alessandri, J.-M., Cunnane, S., Dhenain, M., & Aujard, F. (2015). Long-chain n-3 PUFAs from fish oil enhance resting state brain glucose utilization and reduce anxiety in an adult nonhuman primate, the grey mouse lemur. Journal of Lipid Research, 56(8), 1511-1518. https://doi.org/10.1194/jlr.M058933
Pifferi, F., Epelbaum, J., & Aujard, F. (2019). Strengths and weaknesses of the gray mouse lemur (Microcebus murinus) as a model for the behavioral and psychological symptoms and neuropsychiatric symptoms of dementia. Frontiers in Pharmacology, 10, 1291. https://doi.org/10.3389/fphar.2019.01291
Pifferi, F., Jouin, M., Alessandri, J. M., Haedke, U., Roux, F., Perrière, N., Denis, I., Lavialle, M., & Guesnet, P. (2007). n-3 Fatty acids modulate brain glucose transport in endothelial cells of the blood-brain barrier. Prostaglandins Leukotrienes and Essential Fatty Acids, 77(5-6), 279-286. https://doi.org/10.1016/j.plefa.2007.10.011
Pifferi, F., Jouin, M., Alessandri, J.-M., Roux, F., Perrière, N., Langelier, B., Lavialle, M., Cunnane, S., & Guesnet, P. (2010). N-3 long-chain fatty acids and regulation of glucose transport in two models of rat brain endothelial cells. Neurochemistry International, 56(5), 703-710. https://doi.org/10.1016/j.neuint.2010.02.006
Pifferi, F., Perret, M., Guesnet, P., Aujard, F., & Alessandri, J.-M. (2012). Fatty acid composition of the brain, retina, liver and adipose tissue of the grey mouse lemur (Microcebus murinus, Primate). Lipids, 47(8), 793-801. https://doi.org/10.1007/s11745-012-3686-x
Pifferi, F., Terrien, J., Marchal, J., Dal-Pan, A., Djelti, F., Hardy, I., Chahory, S., Cordonnier, N., Desquilbet, L., Hurion, M., Zahariev, A., Chery, I., Zizzari, P., Perret, M., Epelbaum, J., Blanc, S., Picq, J. -L., Dhenain, M., & Aujard, F. (2018). Caloric restriction increases lifespan but affects brain integrity in grey mouse lemur primates. Communications Biology, 1, 30. https://doi.org/10.1038/s42003-018-0024-8
Pifferi, F., Terrien, J., Perret, M., Epelbaum, J., Blanc, S., Picq, J. L., Dhenain, M., & Aujard, F. (2019). Promoting healthspan and lifespan with caloric restriction in primates. Communications Biology, 2, 107. https://doi.org/10.1038/s42003-019-0348-z
Plourde, M., Chouinard-Watkins, R., Vandal, M., Zhang, Y., Lawrence, P., Brenna, J. T., & Cunnane, S. C. (2011). Plasma incorporation, apparent retroconversion and β-oxidation of 13C-docosahexaenoic acid in the elderly. Nutrition and Metabolism, 8, 5. https://doi.org/10.1186/1743-7075-8-5
Plourde, M., Fortier, M., Vandal, M., Tremblay-Mercier, J., Freemantle, E., Bégin, M., Pifferi, F., & Cunnane, S. C. (2007). Unresolved issues in the link between docosahexaenoic acid and Alzheimer's disease. Prostaglandins, Leukotrienes, and Essential Fatty Acids, 77(5-6), 301-308. https://doi.org/10.1016/j.plefa.2007.10.024
Rapp, P. R. (1990). Visual discrimination and reversal learning in the aged monkey (Macaca mulatta). Behavioral Neuroscience, 104(6), 876-884. https://doi.org/10.1037//0735-7044.104.6.876
Rapp, P. R., & Amaral, D. G. (1992). Individual differences in the cognitive and neurobiological consequences of normal aging. Trends in Neurosciences, 15(9), 340-345. https://doi.org/10.1016/0166-2236(92)90051-9
Rapp, P. R., & Gallagher, M. (1997). Toward a cognitive neuroscience of normal aging, Advances in cell aging and gerontology (Vol. 2, pp. 1-21). Elsevier. https://doi.org/10.1016/S1566-3124(08)60051-6
Rasch, B., & Born, J. (2013). About sleep's role in memory. Physiological Reviews, 93(2), 681-766. https://doi.org/10.1152/physrev.00032.2012
Rathbun, W. B., & Holleschau, A. M. (1992). The effects of age on glutathione synthesis enzymes in lenses of old world simians and prosimians. Current Eye Research, 11(7), 601-607. https://doi.org/10.3109/02713689209000733
Reaven, E., Wright, D., Mondon, C. E., Solomon, R., Ho, H., & Reaven, G. M. (1983). Effect of age and diet on insulin secretion and insulin action in the rat. Diabetes, 32(2), 175-180. https://doi.org/10.2337/diab.32.2.175
Redman, L. M., Smith, S. R., Burton, J. H., Martin, C. K., Il′yasova, D., & Ravussin, E. (2018). Metabolic slowing and reduced oxidative damage with sustained caloric restriction support the rate of living and oxidative damage theories of aging. Cell Metabolism, 27(4), 805-815.e4. https://doi.org/10.1016/J.CMET.2018.02.019
Romieu, I., Dossus, L., Barquera, S., Blottière, H. M., Franks, P. W., Gunter, M., Hwalla, N., Hursting, S. D., Leitzmann, M., Margetts, B., Nishida, C., Potischman, N., Seidell, J., Stepien, M., Wang, Y., Westerterp, K., Winichagoon, P., Wiseman, M., & Willett, W. C. (2017). Energy balance and obesity: What are the main drivers? Cancer Causes and Control, 28(3), 247-258. https://doi.org/10.1007/s10552-017-0869-z
Roth, G., & Dicke, U. (2019). Origin and evolution of human cognition. In M. A. Hofman (Ed.), Progress in brain research (Vol. 250, pp. 285-316). Elsevier. https://doi.org/10.1016/bs.pbr.2019.02.004
Rouby, C., Thomas-Danguin, T., Vigouroux, M., Ciuperca, G., Jiang, T., Alexanian, J., Barges, M., Gallice, I., Degraix, J.-L., & Sicard, G. (2011). The Lyon Clinical Olfactory Test: Validation and measurement of hyposmia and anosmia in healthy and diseased populations. International Journal of Otolaryngology, 2011, 203805. https://doi.org/10.1155/2011/203805
Royo, J., Villain, N., Champeval, D., Del Gallo, F., Bertini, G., Aujard, F., & Pifferi, F. (2018). Effects of n-3 polyunsaturated fatty acid supplementation on cognitive functions, electrocortical activity and neurogenesis in a non-human primate, the grey mouse lemur (Microcebus murinus). Behavioural Brain Research, 347, 394-407. https://doi.org/10.1016/j.bbr.2018.02.029
Rutjes, A. W. S., Denton, D. A., Di Nisio, M., Chong, L. Y., Abraham, R. P., Al-Assaf, A. S., Anderson, J. L., Malik, M. A., Vernooij, R. W. M., Martínez, G., Tabet, N., & Mccleery, J. (2018). Vitamin and mineral supplementation for maintaining cognitive function in cognitively healthy people in mid and late life. Cochrane Database of Systematic Reviews, 12(12):CD011906. https://doi.org/10.1002/14651858.CD011906.pub2
Salvin, H. E., McGreevy, P. D., Sachdev, P. S., & Valenzuela, M. J. (2011). The canine sand maze: An appetitive spatial memory paradigm sensitive to age-related change in dogs. Journal of the Experimental Analysis of Behavior, 95(1), 109-118. https://doi.org/10.1901/jeab.2011.95-109
Sansalone, G., Allen, K., Ledogar, J. A., Ledogar, S., Mitchell, D. R., Profico, A., Castiglione, S., Melchionna, M., Serio, C., Mondanaro, A., Raia, P., & Wroe, S. (2020). Variation in the strength of allometry drives rates of evolution in primate brain shape. Proceedings of the Royal Society B: Biological Sciences, 287(1930), 20200807. https://doi.org/10.1098/rspb.2020.0807
Sastry, P. S. (1985). Lipids of nervous tissue: Composition and metabolism. Progress in Lipid Research, 24(2), 69-176. https://doi.org/10.1016/0163-7827(85)90011-6
Sawiak, S. J., Picq, J. -L., & Dhenain, M. (2014). Voxel-based morphometry analyses of in vivo MRI in the aging mouse lemur primate. Frontiers in Aging Neuroscience, 6, 82. https://doi.org/10.3389/fnagi.2014.00082
Schilling, A., & Perret, M. (1993). Removal of the olfactory bulbs modifies the gonadal responses to photoperiod in the lesser mouse lemur (Microcebus murinus). Biology of Reproduction, 49(1), 58-65. https://doi.org/10.1095/biolreprod49.1.58
Schilling, A., Perret, M., & Predine, J. (1984). Sexual inhibition in a prosimian primate: A pheromone-like effect. Journal of Endocrinology, 102(2), 143-151. https://doi.org/10.1677/joe.0.1020143
Schmidtke, D. (2021). Age affects procedural paired-associates learning in the grey mouse lemur (Microcebus murinus). Scientific Reports, 11(1), 1252. https://doi.org/10.1038/s41598-021-80960-y
Schmidtke, D., Ammersdörfer, S., Joly, M., & Zimmermann, E. (2018). First comparative approach to touchscreen-based visual object-location paired-associates learning in humans (Homo sapiens) and a nonhuman primate (Microcebus murinus). Journal of Comparative Psychology, 132(3), 315-325. https://doi.org/10.1037/com0000116
Schmidtke, D., Zimmermann, E., Trouche, S. G., Fontès, P., Verdier, J. M., & Mestre-Francés, N. (2020). Linking cognition to age and amyloid-β burden in the brain of a nonhuman primate (Microcebus murinus). Neurobiology of Aging, 94, 207-216. https://doi.org/10.1016/j.neurobiolaging.2020.03.025
Schoenbaum, G., Nugent, S., Saddoris, M. P., & Gallagher, M. (2002). Teaching old rats new tricks: Age-related impairments in olfactory reversal learning. Neurobiology of Aging, 23(4), 555-564. https://doi.org/10.1016/S0197-4580(01)00343-8
Schoenbaum, G., Setlow, B., Saddoris, M. P., & Gallagher, M. (2006). Encoding changes in orbitofrontal cortex in reversal-impaired aged rats. Journal of Neurophysiology, 95(3), 1509-1517. https://doi.org/10.1152/jn.01052.2005
Schopf, C., Zimmermann, E., Tünsmeyer, J., Kästner, S. B. R., Hubka, P., & Kral, A. (2014). Hearing and age-related changes in the gray mouse lemur. Journal of the Association for Research in Otolaryngology, 15(6), 993-1005. https://doi.org/10.1007/s10162-014-0478-4
Seddon, J., Fong, D., West, S. K., & Valmadrid, C. T. (1995). Epidemiology of risk factors for age-related cataract. Survey of Ophthalmology, 39(4), 323-334. https://doi.org/10.1016/S0039-6257(05)80110-9
Shamy, J. L., Habeck, C., Hof, P. R., Amaral, D. G., Fong, S. G., Buonocore, M. H., Stern, Y., Barnes, C. A., & Rapp, P. R. (2011). Volumetric correlates of spatiotemporal working and recognition memory impairment in aged rhesus monkeys. Cerebral Cortex, 21(7), 1559-1573. 1537. https://doi.org/10.1093/cercor/bhq210
Smith, T. D., Bhatnagar, K. P., Rossie, J. B., Docherty, B. A., Burrows, A. M., Cooper, G. M., Mooney, M. P., & Siegel, M. I. (2007). Scaling of the first ethmoturbinal in nocturnal strepsirrhines: Olfactory and respiratory surfaces. Anatomical Record, 290(3), 215-237. https://doi.org/10.1002/ar.20428
Souza, A. A. (2003). Male behavioral response to the urine odor of females in lesser mouse lemur (Microcebus murinus Miller, 1777)(Cheirogaleidae Primates). Revista Brasileira de Zoociências, 5(1), 55-77.
Spindler, S. R. (2010). Caloric restriction: From soup to nuts. Ageing Research Reviews, 9(3), 324-353. https://doi.org/10.1016/j.arr.2009.10.003
Squire, L. R. (1992). Memory and the hippocampuss: A synthesis from findings with rats, monkeys, and humans. Psychological Review, 99(2), 195-231. https://doi.org/10.1037/0033-295X.99.2.195
Squire, L. R., Stark, C. E. L., & Clark, R. E. (2004). The medial temporal lobe. Annual Review of Neuroscience, 27, 279-306. https://doi.org/10.1146/annurev.neuro.27.070203.144130
Stenholm, S., Head, J., Aalto, V., Kivimäki, M., Kawachi, I., Zins, M., Goldberg, M., Platts, L. G., Zaninotto, P., Magnusson Hanson, L. L., Westerlund, H., & Vahtera, J. (2017). Body mass index as a predictor of healthy and disease-free life expectancy between ages 50 and 75: A multicohort study. International Journal of Obesity, 41(5), 769-775. https://doi.org/10.1038/ijo.2017.29
Stieler, J. T., Bullmann, T., Kohl, F., Tøien, O., Brückner, M. K., Härtig, W., Barnes, B. M., & Arendt, T. (2011). The physiological link between metabolic rate depression and tau phosphorylation in mammalian hibernation. PLoS One, 6(1), 14530. https://doi.org/10.1371/journal.pone.0014530
Takeuchi, T., Iwanaga, M., & Harada, E. (2003). Possible regulatory mechanism of DHA-induced anti-stress reaction in rats. Brain Research, 964(1), 136-143.
Thomas, P., Pouydebat, E., Le Brazidec, M., Aujard, F., & Herrel, A. (2016). Determinants of pull strength in captive grey mouse lemurs (Microcebus murinus). Journal of Zoology, 298(2), 77-81.
Touron, D. R. (2006). Are item-level strategy shifts abrupt and collective? Age differences in cognitive skill acquisition. Psychonomic Bulletin and Review, 13(5), 781-786. https://doi.org/10.3758/BF03193997
Trouche, S. G., Maurice, T., Rouland, S., Verdier, J. -M., & Mestre-Francés, N. (2010). The three-panel runway maze adapted to Microcebus murinus reveals age-related differences in memory and perseverance performances. Neurobiology of Learning and Memory, 94(1), 100-106. https://doi.org/10.1016/j.nlm.2010.04.006
Ullman, M. T. (2004). Contributions of memory circuits to language: The declarative/procedural model. Cognition, 92(1-2), 231-270. https://doi.org/10.1016/j.cognition.2003.10.008
Valdois, S., Joanette, Y., Poissant, A., Ska, B., & Dehaut, F. (1990). Heterogeneity in the cognitive profile of normal elderly. Journal of Clinical and Experimental Neuropsychology, 12(4), 587-596. https://doi.org/10.1080/01688639008401003
Verduci, E., Banderali, G., Barberi, S., Radaelli, G., Lops, A., Betti, F., Riva, E., & Giovannini, M. (2014). Epigenetic effects of human breast milk. Nutrients, 6(4), 1711-1724. https://doi.org/10.3390/nu6041711
Villain, N., Picq, J.-L., Aujard, F., & Pifferi, F. (2016). Body mass loss correlates with cognitive performance in primates under acute caloric restriction conditions. Behavioural Brain Research, 305, 157-163. https://doi.org/10.1016/j.bbr.2016.02.037
Vinot, N., Jouin, M., Lhomme-Duchadeuil, A., Guesnet, P., Alessandri, J.-M., Aujard, F., & Pifferi, F. (2011). Omega-3 fatty acids from fish oil lower anxiety, improve cognitive functions and reduce spontaneous locomotor activity in a non-human primate. PLoS One, 6(6), e20491. https://doi.org/10.1371/journal.pone.0020491
Voytko, M. L. (1999). Impairments in acquisition and reversals of two-choice discriminations by aged rhesus monkeys. Neurobiology of Aging, 20(6), 617-627. https://doi.org/10.1016/S0197-4580(99)00097-4
Walker, L. C., Kitt, C. A., Struble, R. G., Wagster, M. V., Price, D. L., & Cork, L. C. (1988). The neural basis of memory decline in aged monkeys. Neurobiology of Aging, 9, 657-666. https://doi.org/10.1016/S0197-4580(88)80130-1
Watanabe, Y., & Tatsuno, I. (2020). Prevention of cardiovascular events with omega-3 polyunsaturated fatty acids and the mechanism involved. Journal of Atherosclerosis and Thrombosis, 27(3), 183-198. https://doi.org/10.5551/jat.50658
Weiler, J. A., Bellebaum, C., & Daum, I. (2008). Aging affects acquisition and reversal of reward-based associative learning. Learning and Memory, 15(4), 190-197. https://doi.org/10.1101/lm.890408
Weinstein, G., Maillard, P., Himali, J. J., Beiser, A. S., Au, R., Wolf, P. A., Seshadri, S., & DeCarli, C. (2015). Glucose indices are associated with cognitive and structural brain measures in young adults. Neurology, 84(23), 2329-2337. https://doi.org/10.1212/WNL.0000000000001655
Weiser, M. J., Butt, C. M., & Mohajeri, M. H. (2016). Docosahexaenoic acid and cognition throughout the lifespan. Nutrients, 8(2), 99. https://doi.org/10.3390/nu8020099
WHO. (2014). Diet, nutrition and the prevention of chronic diseases. Report of the joint WHO/FAO expert consultation. WHO.
WHO. (2021). Obesity and overweight. http://www.who.int/mediacentre/factsheets/fs311/en/
Wittkowski, J., Fritz, R. G., Meier, M., & Schmidtke, D. (2021). Conditioning learning in an attentional task relates to age and ventricular expansion in a nonhuman primate (Microcebus murinus). Behavioural Brain Research, 399, 113053. https://doi.org/10.1016/j.bbr.2020.113053
Won, S. J., Yoo, B. H., Kauppinen, T. M., Choi, B. Y., Kim, J. H., Jang, B. G., Lee, M. W., Sohn, M., Liu, J., Swanson, R. A., & Suh, S. W. (2012). Recurrent/moderate hypoglycemia induces hippocampal dendritic injury, microglial activation, and cognitive impairment in diabetic rats. Journal of Neuroinflammation, 9, 182. https://doi.org/10.1186/1742-2094-9-182
Ximenes da Silva, A., Lavialle, F., Gendrot, G., Guesnet, P., Alessandri, J.-M., & Lavialle, M. (2002). Glucose transport and utilization are altered in the brain of rats deficient in n-3 polyunsaturated fatty acids. Journal of Neurochemistry, 81(6), 1328-1337.
Yamada, Y., Kemnitz, J. W., Weindruch, R., Anderson, R. M., Schoeller, D. A., & Colman, R. J. (2018). Caloric restriction and healthy life span: Frail phenotype of nonhuman primates in the Wisconsin National Primate Research Center caloric restriction study. The Journals of Gerontology: Series A, Biological Sciences and Medical Sciences, 73(3), 273-278. https://doi.org/10.1093/gerona/glx059
Yanai, S., Okaichi, Y., & Okaichi, H. (2004). Long-term dietary restriction causes negative effects on cognitive functions in rats. Neurobiology of Aging, 25(3), 325-332. https://doi.org/10.1016/S0197-4580(03)00115-5
Ylikoski, R. (1999). Heterogeneity of cognitive profiles in aging: Successful aging, normal aging, and individuals at risk for cognitive decline. European Journal of Neurology, 6(6), 645-652. https://doi.org/10.1046/j.1468-1331.1999.660645.x
Yoder, A. D., Chan, L. M., Dos Reis, M., Larsen, P. A., Campbell, C. R., Rasoloarison, R., Barrett, M., Roos, C., Kappeler, P., Bielawski, J., & Yang, Z. (2014). Molecular evolutionary characterization of a V1R subfamily unique to strepsirrhine primates. Genome Biology and Evolution, 6(1), 213-227. https://doi.org/10.1093/gbe/evu006
Zablocki-Thomas, P. B., Herrel, A., Hardy, I., Rabardel, L., Perret, M., Aujard, F., & Pouydebat, E. (2018). Personality and performance are affected by age and early life parameters in a small primate. Ecology and Evolution, 8(9), 4598-4605. https://doi.org/10.1002/ece3.3833
Zablocki-Thomas, P. B., Herrel, A., Karanewsky, C. J., Aujard, F., & Pouydebat, E. (2019). Heritability and genetic correlations of personality, life history and morphology in the grey mouse lemur (Microcebus murinus). Royal Society Open Science, 6(10), 190632. https://doi.org/10.1098/rsos.190632
Zimmermann, E., Radespiel, U., Mestre-Francés, N., & Verdier, J. M. (2016). Life history variation in mouse lemurs (Microcebus murinus, M. lehilahytsara): The effect of environmental and phylogenetic determinants. In S. M. Lehman, N. Mestre-Francés, & J.-M. Verdier (Eds.), The dwarf and mouse lemurs of madagascar: Biology, behavior and conservation biogeography of the cheirogaleidae (pp. 174-194). Cambridge University Press. https://doi.org/10.1017/CBO9781139871822.009
Zohdy, S., Gerber, B. D., Tecot, S., Blanco, M. B., Winchester, J. M., Wright, P. C., & Jernvall, J. (2014). Teeth, sex, and testosterone: Aging in the world's smallest primate. PLoS One, 9(10), 109528. https://doi.org/10.1371/journal.pone.0109528