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Annual Review of Neuroscience

Volume 45, 2022

Considering Organismal Physiology in Laboratory Studies of Rodent Behavior

Abstract

Any experiment conducted in a rodent laboratory is done so against the backdrop of each animal's physiological state at the time of the experiment. This physiological state can be the product of multiple factors, both internal (e.g., animal sex, strain, hormone cycles, or circadian rhythms) and external (e.g., housing conditions, social status, and light/dark phases). Each of these factors has the potential to influence experimental outcomes, either independently or via interactions with others, and yet there is little consistency across laboratories in terms of the weight with which they are considered in experimental design. Such discrepancies—both in practice and in reporting—likely contribute to the perception of a reproducibility crisis in the field of behavioral neuroscience. In this review, we discuss how several of these sources of variability can impact outcomes within the realm of common learning and memory paradigms.

Keyword(s): circadian rhythms, estrous cycle, learning and memory, rodent housing conditions, social learning
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2022-07-08
2024-04-28
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Literature Cited

  1. Ajayi AF, Akhigbe RE. 2020. Staging of the estrous cycle and induction of estrus in experimental rodents: an update. Fertil. Res. Pract. 6:15
     [Google Scholar]
  2. Akyazi I, Eraslan E. 2014. Transmission of stress between cagemates: a study in rats. Physiol. Behav. 123:114–18
     [Google Scholar]
  3. Anagnostaras SG, Gale GD, Fanselow MS. 2001. Hippocampus and contextual fear conditioning: recent controversies and advances. Hippocampus 11:18–17
     [Google Scholar]
  4. Bailey M, Silver R. 2014. Sex differences in circadian timing systems: implications for disease. Front. Neuroendocrinol. 35:1111
     [Google Scholar]
  5. Baker-Andresen D, Flavell CR, Li X, Bredy TW. 2013. Activation of BDNF signaling prevents the return of fear in female mice. Learn. Mem. 20:5237–40
     [Google Scholar]
  6. Becker JB, Prendergast BJ, Liang JW. 2016. Female rats are not more variable than male rats: a meta-analysis of neuroscience studies. Biol. Sex Differ. 7:134
     [Google Scholar]
  7. Beery AK, Zucker I. 2011. Sex bias in neuroscience and biomedical research. Neurosci. Biobehav. Rev. 35:3565–72
     [Google Scholar]
  8. Berry B, McMahan R, Gallagher M. 1997. Spatial learning and memory at defined points of the estrous cycle: effects on performance of a hippocampal-dependent task. Behav. Neurosci. 111:2267–74
     [Google Scholar]
  9. Bianchi M, Fone KFC, Azmi N, Heidbreder CA, Hagan JJ, Marsden CA. 2006. Isolation rearing induces recognition memory deficits accompanied by cytoskeletal alterations in rat hippocampus. Eur. J. Neurosci. 24:102894–902
     [Google Scholar]
  10. Blume SR, Freedberg M, Vantrease JE, Chan R, Padival M et al. 2017. Sex- and estrus-dependent differences in rat basolateral amygdala. J. Neurosci. 37:4410567
     [Google Scholar]
  11. Broadbent NJ, Gaskin S, Squire LR, Clark RE. 2010. Object recognition memory and the rodent hippocampus. Learn. Mem. 17:15–11
     [Google Scholar]
  12. Bruchey AK, Jones CE, Monfils M-H. 2010. Fear conditioning by proxy: social transmission of fear during memory retrieval. Behav. Brain Res. 214:180–84
     [Google Scholar]
  13. Burns ER. 2000. Biological time and in vivo research: a field guide to pitfalls. Anat. Rec. 261:141–52
     [Google Scholar]
  14. Caglioni CS. 2009. Assessing reproductive status/stages in mice. Curr. Protoc. Neurosci. 48:A.4I.1–8
     [Google Scholar]
  15. Chaudhury D, Colwell CS. 2002. Circadian modulation of learning and memory in fear-conditioned mice. Behav. Brain Res. 133:195–108
     [Google Scholar]
  16. Choleris E, Clipperton-Allen AE, Gray DG, Diaz-Gonzalez S, Welsman RG. 2011. Differential effects of dopamine receptor D1-type and D2-type antagonists and phase of the estrous cycle on social learning of food preferences, feeding, and social interactions in mice. Neuropsychopharmacology 36:81689–702
     [Google Scholar]
  17. Choleris E, Clipperton-Allen A, Phan A, Kavaliers M. 2009. Neuroendocrinology of social information processing in rats and mice. Front. Neuroendocrinol. 30:4442–59
     [Google Scholar]
  18. Chun LE, Woodruff ER, Morton S, Hinds LR, Spencer RL. 2015. Variations in phase and amplitude of rhythmic clock gene expression across prefrontal cortex, hippocampus, amygdala, and hypothalamic paraventricular and suprachiasmatic nuclei of male and female rats. J. Biol. Rhythms 30:5417–36
     [Google Scholar]
  19. Clayton JA, Collins FS. 2014. Policy: NIH to balance sex in cell and animal studies. Nature 509:7500282–83
     [Google Scholar]
  20. Cloutier CJ, Zevy DL, Kavaliers M, Ossenkopp KP. 2018. Conditioned disgust in rats (anticipatory nausea) to a context paired with the effects of the toxin LiCl: influence of sex and the estrous cycle. Pharmacol. Biochem. Behav. 173:51–57
     [Google Scholar]
  21. Cora MC, Kooistra L, Travlos G. 2015. Vaginal cytology of the laboratory rat and mouse: review and criteria for the staging of the estrous cycle using stained vaginal smears. Toxicol. Pathol. 43:6776–93
     [Google Scholar]
  22. Cordeira J, Kolluru S, Rosenblatt H, Kry J, Strecker R, McCarley R. 2018. Learning and memory are impaired in the object recognition task during metestrus/diestrus and after sleep deprivation. Behav. Brain Res. 339:124–29
     [Google Scholar]
  23. Cossio R, Carreira MB, Vásquez CE, Britton GB. 2016. Sex differences and estrous cycle effects on foreground contextual fear conditioning. Physiol. Behav. 163:305–11
     [Google Scholar]
  24. Davitz JR, Mason DJ. 1955. Socially facilitated reduction of a fear response in rats. J. Comp. Physiol. Psychol. 48:3149–51
     [Google Scholar]
  25. Frye CA. 1995. Estrus-associated decrements in a water maze task are limited to acquisition. Physiol. Behav. 57:15–14
     [Google Scholar]
  26. Galef BG, Giraldeau LA. 2001. Social influences on foraging in vertebrates: causal mechanisms and adaptive functions. Anim. Behav. 61:13–15
     [Google Scholar]
  27. Galef BG, Mason J, Preti G, Bean N. 1988. Carbon disulfide: a semiochemical mediating socially-induced diet choice in rats. Physiol. Behav. 42:2119–24
     [Google Scholar]
  28. Galef BG, Wigmore SW. 1983. Transfer of information concerning distant foods: a laboratory investigation of the ‘information-centre’ hypothesis. Anim. Behav. 31:3748–58
     [Google Scholar]
  29. Graham BM, Scott E. 2018. Effects of systemic estradiol on fear extinction in female rats are dependent on interactions between dose, estrous phase, and endogenous estradiol levels. Horm. Behav. 97:67–74
     [Google Scholar]
  30. Hall J, Thomas KL, Everitt BJ. 2000. Rapid and selective induction of BDNF expression in the hippocampus during contextual learning. Nat. Neurosci. 3:6533–35
     [Google Scholar]
  31. Haskell SG, Gordon KS, Mattocks K, Duggal M, Erdos J et al. 2010. Gender differences in rates of depression, PTSD, pain, obesity, and military sexual trauma among Connecticut War Veterans of Iraq and Afghanistan. J. Women's Health 19:2267–71
     [Google Scholar]
  32. Hellemans KGC, Benge LC, Olmstead MC. 2004. Adolescent enrichment partially reverses the social isolation syndrome. Dev. Brain Res. 150:2103–15
     [Google Scholar]
  33. Heyes C. 1994. Social learning in animals: categories and mechanisms. Biol. Rev. Camb. Philos. Soc. 69:2207–31
     [Google Scholar]
  34. Hullinger R, O'Riordan K, Burger C. 2015. Environmental enrichment improves learning and memory and long-term potentiation in young adult rats through a mechanism requiring mGluR5 signaling and sustained activation of p70s6k. Neurobiol. Learn. Mem. 125:126–34
     [Google Scholar]
  35. Hunter A. 2014. The effects of social housing on extinction of fear conditioning in rapid eye movement sleep-deprived rats. Exp. Brain Res. 232:51459–67
     [Google Scholar]
  36. Jarrard LE. 1993. On the role of the hippocampus in learning and memory in the rat. Behav. Neural Biol. 60:19–26
     [Google Scholar]
  37. Jones C, Riha P, Gore A, Monfils M. 2014. Social transmission of Pavlovian fear: fear-conditioning by-proxy in related female rats. Anim. Cogn. 17:3827–34
     [Google Scholar]
  38. Jones CA, Brown AM, Auer DP, Fone KCF. 2011. The mGluR2/3 agonist LY379268 reverses post-weaning social isolation-induced recognition memory deficits in the rat. Psychopharmacology 214:1269–83
     [Google Scholar]
  39. Jones CE, Monfils M-H. 2016. Dominance status predicts social fear transmission in laboratory rats. Anim. Cogn. 19:61051–69
     [Google Scholar]
  40. Kercmar J, Büdefeld T, Grgurevic N, Tobet SA, Majdic G. 2011. Adolescent social isolation changes social recognition in adult mice. Behav. Brain Res. 216:2647–51
     [Google Scholar]
  41. Kiyokawa Y, Honda A, Takeuchi Y, Mori Y. 2014. A familiar conspecific is more effective than an unfamiliar conspecific for social buffering of conditioned fear responses in male rats. Behav. Brain Res. 267:189–93
     [Google Scholar]
  42. Kiyokawa Y, Ishida A, Takeuchi Y, Mori Y. 2016. Sustained housing-type social buffering following social housing in male rats. Physiol. Behav. 158:85–89
     [Google Scholar]
  43. Kiyokawa Y, Kawai K, Takeuchi Y. 2018. The benefits of social buffering are maintained regardless of the stress level of the subject rat and enhanced by more conspecifics. Physiol. Behav. 194:177–83
     [Google Scholar]
  44. Kiyokawa Y, Kikusui T, Takeuchi Y, Mori Y. 2004. Partner's stress status influences social buffering effects in rats. Behav. Neurosci. 118:4798–804
     [Google Scholar]
  45. Kiyokawa Y, Takeuchi Y, Mori Y. 2007. Two types of social buffering differentially mitigate conditioned fear responses. Eur. J. Neurosci. 26:123606–13
     [Google Scholar]
  46. Kline A, Ciccone DS, Weiner M, Interian A, St Hill L et al. 2013. Gender differences in the risk and protective factors associated with PTSD: a prospective study of National Guard troops deployed to Iraq. Psychiatry 76:3256–72
     [Google Scholar]
  47. Knapska E, Mikosz M, Werka T, Maren S 2010. Social modulation of learning in rats. Learn. Mem. 17:135–42
     [Google Scholar]
  48. Kobayashi I, Hatcher M, Wilson C, Boadi L, Poindexter M et al. 2020. Impacts of sex and the estrous cycle on associations between post-fear conditioning sleep and fear memory recall. Behav. Brain Res. 378:112156
     [Google Scholar]
  49. Kogan JH, Frankland PW, Silva AJ. 2000. Long-term memory underlying hippocampus-dependent social recognition in mice. Hippocampus 10:147–56
     [Google Scholar]
  50. Langston RF, Wood ER. 2010. Associative recognition and the hippocampus: differential effects of hippocampal lesions on object-place, object-context and object-place-context memory. Hippocampus 20:101139–53
     [Google Scholar]
  51. Lapiz MDS, Fulford A, Muchimapura S, Mason R, Parker T, Marsden CA. 2003. Influence of postweaning social isolation in the rat on brain development, conditioned behavior, and neurotransmission. Neurosci. Behav. Physiol. 33:113–29
     [Google Scholar]
  52. Lapiz MDS, Mateo Y, Parker T, Marsden C. 2000. Effects of noradrenaline depletion in the brain on response to novelty in isolation-reared rats. Psychopharmacology 152:3312–20
     [Google Scholar]
  53. Lebron-Milad K, Milad MR. 2012. Sex differences, gonadal hormones and the fear extinction network: implications for anxiety disorders. Biol. Mood Anxiety Disord. 2:13
     [Google Scholar]
  54. Leser N, Wagner S. 2015. The effects of acute social isolation on long-term social recognition memory. Neurobiol. Learn. Mem. 124:97–103
     [Google Scholar]
  55. Maeng LY, Cover KK, Taha MB, Landau AJ, Milad MR, Lebrón-Milad K. 2017. Estradiol shifts interactions between the infralimbic cortex and central amygdala to enhance fear extinction memory in female rats. J. Neurosci. Res. 95:1–2163–75
     [Google Scholar]
  56. Maren S, Phan KL, Liberzon I. 2013. The contextual brain: implications for fear conditioning, extinction and psychopathology. Nat. Rev. Neurosci. 14:6417–28
     [Google Scholar]
  57. Markham JA, Juraska JM. 2007. Social recognition memory: influence of age, sex, and ovarian hormonal status. Physiol. Behav. 92:5881–88
     [Google Scholar]
  58. Markus EJ, Zecevic M. 1997. Sex differences and estrous cycle changes in hippocampus-dependent fear conditioning. Psychobiology 25:3246–52
     [Google Scholar]
  59. Marti AR, Pedersen TT, Wisor JP, Mrdalj J, Holmelid Ø et al. 2020. Cognitive function and brain plasticity in a rat model of shift work: role of daily rhythms, sleep and glucocorticoids. Sci. Rep. 10:113141
     [Google Scholar]
  60. McLean S, Grayson B, Harris M, Protheroe C, Woolley M, Neill J. 2010. Isolation rearing impairs novel object recognition and attentional set shifting performance in female rats. J. Psychopharmacol. 24:157–63
     [Google Scholar]
  61. Melo I, Ehrlich I. 2016. Sleep supports cued fear extinction memory consolidation independent of circadian phase. Neurobiol. Learn. Mem. 132:9–17
     [Google Scholar]
  62. Milad MR, Igoe SA, Lebron-Milad K, Novales JE. 2009. Estrous cycle phase and gonadal hormones influence conditioned fear extinction. Neuroscience 164:3887–95
     [Google Scholar]
  63. Moisan M-P. 2021. Sexual dimorphism in glucocorticoid stress response. Int. J. Mol. Sci. 22:63139
     [Google Scholar]
  64. Mora-Gallegos A, Fornaguera J 2019. The effects of environmental enrichment and social isolation and their reversion on anxiety and fear conditioning. Behav. Process. 158:59–69
     [Google Scholar]
  65. Morris RGM, Garrud P, Rawlins JNP, O'Keefe J. 1982. Place navigation impaired in rats with hippocampal lesions. Nature 297:5868681–83
     [Google Scholar]
  66. Nakayasu T, Ishii K. 2008. Effects of pair-housing after social defeat experience on elevated plus-maze behavior in rats. Behav. Process. 78:3477–80
     [Google Scholar]
  67. Ney LJ, Gogos A, Hsu C-MK, Felmingham KL. 2019. An alternative theory for hormone effects on sex differences in PTSD: the role of heightened sex hormones during trauma. Psychoneuroendocrinology 109:104416
     [Google Scholar]
  68. Peirson SN, Brown LA, Pothecary CA, Benson LA, Fisk AS. 2018. Light and the laboratory mouse. J. Neurosci. Methods 300:26–36
     [Google Scholar]
  69. Peirson SN, Foster RG. 2011. Bad light stops play. EMBO Rep. 12:5380
     [Google Scholar]
  70. Perry CJ, Ganella DE, Nguyen LD, Du X, Drummond KD et al. 2020a. Adolescent rats show estrous cycle-mediated sex-differences in extinction of conditioned fear. bioRxiv 2020.03.31.019273. https://doi.org/10.1101/2020.03.31.019273
    [Crossref]
  71. Perry CJ, Ganella DE, Nguyen LD, Du X, Drummond KD et al. 2020b. Assessment of conditioned fear extinction in male and female adolescent rats. Psychoneuroendocrinology 116:104670
     [Google Scholar]
  72. Pezük P, Mohawk JA, Wang LA, Menaker M. 2012. Glucocorticoids as entraining signals for peripheral circadian oscillators. Endocrinology 153:104775–83
     [Google Scholar]
  73. Popik P, van Ree JM. 1999. Neurohypophyseal peptides and social recognition in rats. Prog. Brain Res. 119:415–36
     [Google Scholar]
  74. Prendergast BJ, Onishi KG, Zucker I. 2014. Female mice liberated for inclusion in neuroscience and biomedical research. Neurosci. Biobehav. Rev. 40:1–5
     [Google Scholar]
  75. Robinson-Junker AL, O'hara BF, Gaskill BN 2018. Out like a light? The effects of a diurnal husbandry schedule on mouse sleep and behavior. J. Am. Assoc. Lab Anim. Sci. 57:2124–33
     [Google Scholar]
  76. Sánchez-Andrade G, James BM, Kendrick KM. 2005. Neural encoding of olfactory recognition memory. J. Reprod. Dev. 51:547–58
     [Google Scholar]
  77. Sánchez-Andrade G, Kendrick K 2011. Roles of α- and β-estrogen receptors in mouse social recognition memory: effects of gender and the estrous cycle. Horm. Behav. 59:1114–22
     [Google Scholar]
  78. Scharfman HE, Mercurio TC, Goodman JH, Wilson MA, MacLusky NJ. 2003. Behavioral/systems/cognitive hippocampal excitability increases during the estrous cycle in the rat: a potential role for brain-derived neurotrophic factor. J. Neurosci. 23:3711641–52
     [Google Scholar]
  79. Schrijver NCA, Bahr NI, Weiss IC, Würbel H. 2002. Dissociable effects of isolation rearing and environmental enrichment on exploration, spatial learning and HPA activity in adult rats. Pharmacol. Biochem. Behav. 73:1209–24
     [Google Scholar]
  80. Schrijver NCA, Pallier PN, Brown VJ, Würbel H. 2004. Double dissociation of social and environmental stimulation on spatial learning and reversal learning in rats. Behav. Brain Res. 152:2307–14
     [Google Scholar]
  81. Seligowski AV, Hurly J, Mellen E, Ressler KJ, Ramikie TS. 2020. Translational studies of estradiol and progesterone in fear and PTSD. Eur. J. Psychotraumatology 11:11723857
     [Google Scholar]
  82. Shahar-Gold H, Gur R, Wagner S. 2013. Rapid and reversible impairments of short- and long-term social recognition memory are caused by acute isolation of adult rats via distinct mechanisms. PLOS ONE 8:5e65085
     [Google Scholar]
  83. Shansky RM, Murphy AZ. 2021. Considering sex as a biological variable will require a global shift in science culture. Nat. Neurosci. 24:4457–64
     [Google Scholar]
  84. Smith IM, Pang KCH, Servatius RJ, Jiao X, Beck KD. 2016. Paired-housing selectively facilitates within-session extinction of avoidance behavior, and increases c-Fos expression in the medial prefrontal cortex, in anxiety vulnerable Wistar-Kyoto rats. Physiol. Behav. 164:198–206
     [Google Scholar]
  85. Sochat VV, Eisenberg IW, Enkavi AZ, Li J, Bissett PG, Poldrack RA. 2016. The experiment factory: standardizing behavioral experiments. Front. Psychol. 7:610
     [Google Scholar]
  86. Sun W, Li J, Cui S, Luo L, Huang P, Tang C, An L 2019. Sleep deprivation disrupts acquisition of contextual fear extinction by affecting circadian oscillation of hippocampal-infralimbic proBDNF. eNeuro 6:5ENEURO.0165-19.2019
     [Google Scholar]
  87. Tang S, Graham BM. 2020. Hormonal, reproductive, and behavioural predictors of fear extinction recall in female rats. Horm. Behav. 121:104693
     [Google Scholar]
  88. Thorsell A, Slawecki CJ, el Khoury A, Mathe AA, Ehlers CL. 2006. The effects of social isolation on neuropeptide Y levels, exploratory and anxiety-related behaviors in rats. Pharmacol. Biochem. Behav. 83:128–34
     [Google Scholar]
  89. Tóth M, Halász J, Mikics É, Barsy B, Haller J. 2008. Early social deprivation induces disturbed social communication and violent aggression in adulthood. Behav. Neurosci. 122:4849–54
     [Google Scholar]
  90. Toyoshima M, Yamada K, Sugita M, Ichitani Y. 2018. Social enrichment improves social recognition memory in male rats. Anim. Cogn. 21:3345–51
     [Google Scholar]
  91. Tribble J, Fanselow M. 2019. Pair-housing rats does not protect from behavioral consequences of an acute traumatic experience. Behav. Neurosci. 133:2232–39
     [Google Scholar]
  92. Tuscher J, Fortress A, Kim J, Frick K. 2015. Regulation of object recognition and object placement by ovarian sex steroid hormones. Behav. Brain Res. 285:140–57
     [Google Scholar]
  93. van Goethem NP, Rutten K, van der Staay FJ, Jans LAW, Akkerman S et al. 2012. Object recognition testing: rodent species, strains, housing conditions, and estrous cycle. Behav. Brain Res. 232:2323–34
     [Google Scholar]
  94. VanElzakker MB, Dahlgren MK, Davis FC, Dubois S, Shin LM. 2014. From Pavlov to PTSD: the extinction of conditioned fear in rodents, humans, and in anxiety disorders. Neurobiol. Learn. Mem. 113:3–18
     [Google Scholar]
  95. Verma P, Hellemans KGC, Choi FY, Yu W, Weinberg J 2010. Circadian phase and sex effects on depressive/anxiety-like behaviors and HPA axis responses to acute stress. Physiol. Behav. 99:3276–85
     [Google Scholar]
  96. Voulo ME, Parsons RG. 2019. Gonadal hormone fluctuations do not affect the expression or extinction of fear-potentiated startle in female rats. Behav. Neurosci. 133:517–26
     [Google Scholar]
  97. Wade SE, Maier SF. 1986. Effects of individual housing and stressor exposure upon the acquisition of watermaze escape. Learn. Motiv. 17:3287–310
     [Google Scholar]
  98. Wald C, Wu C. 2010. Of mice and women: the bias in animal models. Science 327:1571–72
     [Google Scholar]
  99. Walf A, Koonce C, Manley K, Frye C. 2009. Proestrous compared to diestrous wildtype, but not estrogen receptor beta knockout, mice have better performance in the spontaneous alternation and object recognition tasks and reduced anxiety-like behavior in the elevated plus and mirror maze. Behav. Brain Res. 196:2254–60
     [Google Scholar]
  100. Walf A, Rhodes M, Frye C. 2006. Ovarian steroids enhance object recognition in naturally cycling and ovariectomized, hormone-primed rats. Neurobiol. Learn. Mem. 86:135–46
     [Google Scholar]
  101. Wang L, Cao M, Pu T, Huang H, Marshall C, Xiao M 2018. Enriched physical environment attenuates spatial and social memory impairments of aged socially isolated mice. Int. J. Neuropsychopharmacol. 21:121114–27
     [Google Scholar]
  102. Warren SG, Juraska JM. 1997. Spatial and nonspatial learning across the rat estrous cycle. Behav. Neurosci. 111:2259–66
     [Google Scholar]
  103. Watson DJG, Marsden CA, Millan MJ, Fone KCF. 2012. Blockade of dopamine D3 but not D2 receptors reverses the novel object discrimination impairment produced by post-weaning social isolation: implications for schizophrenia and its treatment. Int. J. Neuropsychopharmacol. 15:4471–84
     [Google Scholar]
  104. Wegerer M, Kerschbaum H, Blechert J, Wilhelm FH. 2014. Low levels of estradiol are associated with elevated conditioned responding during fear extinction and with intrusive memories in daily life. Neurobiol. Learn. Mem. 116:145
     [Google Scholar]
  105. Woitowich NC, Beery A, Woodruff T 2020. A 10-year follow-up study of sex inclusion in the biological sciences. eLife 9:56344
     [Google Scholar]
  106. Wongwitdecha N, Marsden CA. 1996. Effects of social isolation rearing on learning in the morris water maze. Brain Res. 715:1–2119–24
     [Google Scholar]
  107. Woodruff ER, Greenwood BN, Chun LE, Fardi S, Hinds LR, Spencer RL. 2015. Adrenal-dependent diurnal modulation of conditioned fear extinction learning. Behav. Brain Res. 286:249–55
     [Google Scholar]
  108. Woolley CS, Gould E, Frankfurt M, McEwen BS. 1990. Naturally occurring fluctuation in dendritic spine density on adult hippocampal pyramidal neurons. J. Neurosci. 10:4035–39
     [Google Scholar]
  109. Woolley CS, McEwen BS. 1992. Estradiol mediates fluctuation in hippocampal synapse density during the estrous cycle in the adult rat. J. Neurosci. 12:2549–54
     [Google Scholar]
  110. Zhang YL, Zhang J, Lu H, Tang J, Luo JL et al. 2019. Group housing with young mice relieves Alzheimer's disease behaviors in aging mice. Eur. Rev. Med. Pharmacol. Sci. 23:188058–67
     [Google Scholar]
  111. Zhao X, Sun L, Jia H, Meng Q, Wu S, Li N, He S 2009. Isolation rearing induces social and emotional function abnormalities and alters glutamate and neurodevelopment-related gene expression in rats. Prog. Neuropsychopharmacol. Biol. Psychiatry 33:71173–77
     [Google Scholar]
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