in

Effects of weaning age and housing conditions on phenotypic differences in mice

  • 1.

    Baker, M. 1,500 scientists lift the lid on reproducibility. Nature 533, 452–454 (2016).

    ADS  CAS  PubMed  Google Scholar 

  • 2.

    Begley, C. G. & Ellis, L. M. Drug development: Raise standards for preclinical cancer research. Nature 483, 531–533 (2012).

    ADS  CAS  Google Scholar 

  • 3.

    Prinz, F., Schlange, T. & Asadullah, K. Believe it or not: How much can we rely on published data on potential drug targets?. Nat. Rev. Drug Discov. 10, 712 (2011).

    CAS  PubMed  Google Scholar 

  • 4.

    Bailoo, J. D., Reichlin, T. S. & Würbel, H. Refinement of experimental design and conduct in laboratory animal research. ILAR J. 55, 383–391 (2014).

    CAS  PubMed  Google Scholar 

  • 5.

    Richter, S. H., Garner, J. P. & Würbel, H. Environmental standardization: Cure or cause of poor reproducibility in animal experiments?. Nat. Methods 6, 257–261 (2009).

    CAS  PubMed  Google Scholar 

  • 6.

    Voelkl, B., Vogt, L., Sena, E. S. & Würbel, H. Reproducibility of preclinical animal research improves with heterogeneity of study samples. PLoS Biol. 16, e2003693 (2018).

    PubMed  PubMed Central  Google Scholar 

  • 7.

    Amrhein, V., Trafimow, D. & Greenland, S. Inferential statistics as descriptive statistics: There is no replication crisis if we don’t expect replication. Am. Stat. 73(sup1), 262–270 (2019).

    MathSciNet  Google Scholar 

  • 8.

    Bohlen, M. et al. Experimenter effects on behavioral test scores of eight inbred mouse strains under the influence of ethanol. Behav. Brain Res. 272, 46–54 (2014).

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  • 9.

    Corrigan, J. K. et al. A big-data approach to understanding metabolic rate and response to obesity in laboratory mice. bioRxiv https://doi.org/10.1101/839076 (2019).

    Article  Google Scholar 

  • 10.

    Crabbe, J. C., Wahlsten, D. L. & Dudek, B. C. Genetics of mouse behavior: Interactions with laboratory environment. Science (80-). 284, 1670–1672 (1999).

    ADS  CAS  Google Scholar 

  • 11.

    Wahlsten, D. et al. Different data from different labs: Lessons from studies of gene-environment interaction. J. Neurobiol. 54, 283–311 (2003).

    PubMed  Google Scholar 

  • 12.

    Richter, S. H. et al. Effect of population heterogenization on the reproducibility of mouse behavior: A multi-laboratory study. PLoS ONE 6, e16461 (2011).

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  • 13.

    Voelkl, B. & Würbel, H. Reproducibility crisis: Are we ignoring reaction norms?. Trends Pharmacol. Sci. 37(7), 509–510 (2016).

    CAS  PubMed  Google Scholar 

  • 14.

    Terranova, M. L. & Laviola, G. Delta opioid modulation of social interactions in juvenile mice weaned at different ages. Physiol. Behav. 73, 393–400 (2001).

    CAS  PubMed  Google Scholar 

  • 15.

    Ladd, C. O., Owens, M. J. & Nemeroff, C. B. Persistent changes in corticotropin-releasing factor neuronal systems induced by maternal deprivation. Endocrinology 137, 1212–1218 (1996).

    CAS  PubMed  Google Scholar 

  • 16.

    Berry, A. et al. Social deprivation stress is a triggering factor for the emergence of anxiety- and depression-like behaviours and leads to reduced brain BDNF levels in C57BL/6J mice. Psychoneuroendocrinology 37, 762–772 (2012).

    CAS  PubMed  Google Scholar 

  • 17.

    Kanari, K., Kikusui, T., Takeuchi, Y. & Mori, Y. Multidimensional structure of anxiety-related behavior in early-weaned rats. Behav. Brain Res. 156, 45–52 (2005).

    PubMed  Google Scholar 

  • 18.

    Kikusui, T., Nakamura, K., Kakuma, Y. & Mori, Y. Early weaning augments neuroendocrine stress responses in mice. Behav. Brain Res. 175, 96–103 (2006).

    CAS  PubMed  Google Scholar 

  • 19.

    Francis, D. D., Champagne, F. A., Liu, D. & Meaney, M. J. Maternal care, gene expression, and the development of individual differences in stress reactivity. Ann. N. Y. Acad. Sci. 896, 66–84 (1999).

    ADS  CAS  PubMed  Google Scholar 

  • 20.

    Bailoo, J. D., Jordan, R. L., Garza, X. J. & Tyler, A. N. Brief and long periods of maternal separation affect maternal behavior and offspring behavioral development in C57BL/6 mice. Dev. Psychobiol. 56, 674–685 (2013).

    PubMed  Google Scholar 

  • 21.

    Bailoo, J. D., Varholick, J. A., Garza, X. J., Jordan, R. L. & Hintze, S. Maternal separation followed by isolation-housing differentially affects prepulse inhibition of the acoustic startle response in C57BL/6 mice. Dev. Psychobiol. 58, 937–944 (2016).

    PubMed  Google Scholar 

  • 22.

    Macrí, S., Mason, G. J. & Würbel, H. Dissociation in the effects of neonatal maternal separations on maternal care and the offspring’s HPA and fear responses in rats. Eur. J. Neurosci. 20, 1017–1024 (2004).

    PubMed  Google Scholar 

  • 23.

    Krackow, S. & Hoeck, H. N. Sex ratio manipulation, maternal investment and behaviour during concurrent pregnancy and lactation in house mice. Anim. Behav. 37, 177–186 (1989).

    Google Scholar 

  • 24.

    König, B. & Markl, H. Maternal care in house mice. Behav. Ecol. Sociobiol. 20, 1–9 (1987).

    Google Scholar 

  • 25.

    König, B. Components of lifetime reproductive success in communally and solitarily nursing house mice: A laboratory study. Behav. Ecol. Sociobiol. 34, 275–283 (1994).

    Google Scholar 

  • 26.

    Hall, F. S. Social deprivation of neonatal, adolescent, and adult rats has distinct neurochemical and behavioral consequences. Crit. Rev. Neurobiol. 12, 129–162 (1998).

    CAS  PubMed  Google Scholar 

  • 27.

    Richter, S. H. et al. A time to wean? Impact of weaning age on anxiety-like behaviour and stability of behavioural traits in full adulthood. PLoS ONE 11, e0167652 (2016).

    PubMed  PubMed Central  Google Scholar 

  • 28.

    Curley, J. P. et al. The meaning of weaning: Influence of the weaning period on behavioral development in mice. Dev. Neurosci. 31, 318–331 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  • 29.

    Bechard, A. & Mason, G. Leaving home: A study of laboratory mouse pup independence. Appl. Anim. Behav. Sci. 125, 181–188 (2010).

    Google Scholar 

  • 30.

    Kikusui, T. & Mori, Y. Behavioural and neurochemical consequences of early weaning in rodents. J. Neuroendocrinol. 21, 427–431 (2009).

    CAS  PubMed  Google Scholar 

  • 31.

    Kikusui, T., Kiyokawa, Y. & Mori, Y. Deprivation of mother-pup interaction by early weaning alters myelin formation in male, but not female, ICR mice. Brain Res. 1133, 115–122 (2007).

    CAS  PubMed  Google Scholar 

  • 32.

    Nakamura, K., Kikusui, T., Takeuchi, Y. & Mori, Y. Changes in social instigation- and food restriction-induced aggressive behaviors and hippocampal 5HT1B mRNA receptor expression in male mice from early weaning. Behav. Brain Res. 187, 442–448 (2008).

    CAS  PubMed  Google Scholar 

  • 33.

    Nakamura, K., Kikusui, T., Takeuchi, Y. & Mori, Y. The influence of early weaning on aggressive behavior in mice. J. Vet. Med. Sci. 65, 1347–1349 (2003).

    PubMed  Google Scholar 

  • 34.

    Würbel, H. & Stauffacher, M. Age and weight at weaning affect corticosterone level and development of stereotypies in ICR-mice. Anim. Behav. 53, 891–900 (1997).

    Google Scholar 

  • 35.

    Latham, N. R. & Mason, G. J. Maternal deprivation and the development of stereotypic behaviour. Appl. Anim. Behav. Sci. 110, 84–108 (2008).

    Google Scholar 

  • 36.

    Kikusui, T., Ichikawa, S. & Mori, Y. Maternal deprivation by early weaning increases corticosterone and decreases hippocampal BDNF and neurogenesis in mice. Psychoneuroendocrinology 34, 762–772 (2009).

    CAS  PubMed  Google Scholar 

  • 37.

    Franklin, T. B. et al. Epigenetic transmission of the impact of early stress across generations. Biol. Psychiatry 68, 408–415 (2010).

    PubMed  Google Scholar 

  • 38.

    Olsson, I. A. S. & Westlund, K. More than numbers matter: The effect of social factors on behaviour and welfare of laboratory rodents and non-human primates. Appl. Anim. Behav. Sci. 103, 229–254 (2007).

    Google Scholar 

  • 39.

    Cacioppo, S., Capitanio, J. P. & Cacioppo, J. T. Toward a neurology of loneliness. Psychol. Bull. 140, 1464–1504 (2014).

    PubMed  PubMed Central  Google Scholar 

  • 40.

    Krohn, T. C., Sorensen, D. B., Ottesen, J. L. & Hansen, A. K. The effects of individual housing on mice and rats: A review. Anim. Welf. 15, 343–352 (2006).

    CAS  Google Scholar 

  • 41.

    Brain, P. What does individual housing mean to a mouse?. Life Sci. 16, 187–200 (1975).

    CAS  PubMed  Google Scholar 

  • 42.

    Valzelli, L. The ‘isolation syndrome’ in mice. Psychopharmacologia 31, 305–320 (1973).

    CAS  PubMed  Google Scholar 

  • 43.

    Albin, R. L., Young, A. B. & Penney, J. B. The functional anatomy of basal ganglia disorders. Trends Neurosci. 12, 366–375 (1989).

    CAS  PubMed  Google Scholar 

  • 44.

    Deroche, V., Piazza, P. V., Moal, M. L. & Simon, H. Social isolation-induced enhancement of the psychomotor effects of morphine depends on corticosterone secretion. Brain Res. 640, 136–139 (1994).

    CAS  PubMed  Google Scholar 

  • 45.

    Piazza, P. V. et al. Suppression of glucocorticoid secretion and antipsychotic drugs have similar effects on the mesolimbic dopaminergic transmission. Proc. Natl. Acad. Sci. 93, 15445–15450 (2002).

    Google Scholar 

  • 46.

    Van Loo, P. L. P. P., Van Zutphen, L. F. M. M. & Baumans, V. Male management: Coping with aggression problems in male laboratory mice. Lab. Anim. 37, 300–313 (2003).

    PubMed  Google Scholar 

  • 47.

    Gerlach, G. Dispersal mechanisms in a captive wild house mouse population (Mus domesticus Rutty). Biol. J. Linn. Soc. 41, 271–277 (1990).

    Google Scholar 

  • 48.

    Gerlach, G. Emigration mechanisms in fetal house mice: A laboratory investigation of the influence of social structure, population density, and aggression. Behav. Ecol. Sociobiol. 39, 159–170 (1996).

    Google Scholar 

  • 49.

    Berry, R. J. & Bronson, F. H. Life history and bioeconomy of the house mouse. Biol. Rev. Camb. Philos. Soc. 67, 519–550 (1992).

    CAS  PubMed  Google Scholar 

  • 50.

    Jansen, R. G., Wiertz, L., Meyer, E. S. & Noldus, L. P. J. J. Reliability analysis of observational data: Problems, solutions, and software implementation. Behav. Res. Methods Instrum. Comput. 35, 391–399 (2003).

    PubMed  Google Scholar 

  • 51.

    Pellow, S., Chopin, P., File, S. & Briley, M. Validation of open: Closed arm entries in an elevated plus-maze as a measure of anxiety in the rat. J. Neurosci. Methods 14, 149–167 (1985).

    CAS  PubMed  Google Scholar 

  • 52.

    File, S. E. & Seth, P. A review of 25 years of the social interaction test. Eur. J. Pharmacol. 463, 35–53 (2003).

    CAS  PubMed  Google Scholar 

  • 53.

    Bailoo, J. D., Bohlen, M. O. & Wahlsten, D. L. The precision of video and photocell tracking systems and the elimination of tracking errors with infrared backlighting. J. Neurosci. Methods 188, 45–52 (2010).

    PubMed  PubMed Central  Google Scholar 

  • 54.

    Möstl, E. & Palme, R. Hormones as indicators of stress. Domest. Anim. Endocrinol. 23, 67–74 (2002).

    PubMed  Google Scholar 

  • 55.

    Touma, C. & Palme, R. Measuring Fecal glucocorticoid metabolites in mammals and birds: The importance of validation. Ann. N. Y. Acad. Sci. 1046, 54–74 (2005).

    ADS  CAS  PubMed  Google Scholar 

  • 56.

    Palme, R. Non-invasive measurement of glucocorticoids: Advances and problems. Physiol. Behav. 199, 229–243 (2019).

    CAS  PubMed  Google Scholar 

  • 57.

    Touma, C., Sachser, N., Möstl, E. & Palme, R. Effects of sex and time of day on metabolism and excretion of corticosterone in urine and feces of mice. Gen. Comp. Endocrinol. 130, 267–278 (2003).

    CAS  PubMed  Google Scholar 

  • 58.

    Touma, C., Palme, R. & Sachser, N. Analyzing corticosterone metabolites in fecal samples of mice: A noninvasive technique to monitor stress hormones. Horm. Behav. 45, 10–22 (2004).

    CAS  PubMed  Google Scholar 

  • 59.

    Kikusui, T., Takeuchi, Y. & Mori, Y. Early weaning induces anxiety and aggression in adult mice. Physiol. Behav. 81, 37–42 (2004).

    CAS  PubMed  Google Scholar 

  • 60.

    Iwata, E., Kikusui, T., Takeuchi, Y. & Mori, Y. Fostering and environmental enrichment ameliorate anxious behavior induced by early weaning in Balb/c mice. Physiol. Behav. 91, 318–324 (2007).

    CAS  PubMed  Google Scholar 

  • 61.

    Benton, D. & Brain, P. F. Behavioral and adrenocortical reactivity in female mice following individual or group housing. Dev. Psychobiol. 14, 101–107 (1981).

    CAS  PubMed  Google Scholar 

  • 62.

    Goldsmith, J. F., Brain, P. F. & Benton, D. Effects of the duration of individual or group housing on behavioural and adrenocortical reactivity in male mice. Physiol. Behav. 21, 757–760 (1978).

    CAS  PubMed  Google Scholar 

  • 63.

    Faggin, B. M. & Palermo-Neto, J. Differential alterations in brain sensitivity to amphetamine and pentylenetetrazol in socially deprived mice. Gen. Pharmacol. 16, 299–302 (1985).

    CAS  PubMed  Google Scholar 

  • 64.

    Cairns, R. B., Hood, K. E. & Midlam, J. On fighting in mice: Is there a sensitive period for isolation effects?. Anim. Behav. 33, 166–180 (1985).

    Google Scholar 

  • 65.

    de Catanzaro, D. & Gorzalka, B. B. Sexual arousal in male mice: Effects of brief periods of isolation or grouping. Behav. Neural Biol. 28, 442–453 (1980).

    PubMed  Google Scholar 

  • 66.

    Einon, D. F., Humphreys, A. P., Chivers, S. M., Field, S. & Naylor, V. Isolation has permanent effects upon the behavior of the rat, but not the mouse, gerbil, or guinea pig. Dev. Psychobiol. 14, 343–355 (1981).

    CAS  PubMed  Google Scholar 

  • 67.

    Misslin, R., Herzog, F., Koch, B. & Ropartz, P. Effects of isolation, handling and novelty on the pituitary-adrenal response in the mouse. Psychoneuroendocrinology 7, 217–221 (1982).

    CAS  PubMed  Google Scholar 

  • 68.

    Rodgers, R. J. & Cole, J. C. Influence of social isolation, gender, strain, and prior novelty on plus-maze behaviour in mice. Physiol. Behav. 54, 729–736 (1993).

    CAS  PubMed  Google Scholar 

  • 69.

    Kikusui, T., Nakamura, K. & Mori, Y. A review of the behavioral and neurochemical consequences of early weaning in rodents. Appl. Anim. Behav. Sci. 110, 73–83 (2008).

    Google Scholar 

  • 70.

    Kikusui, T. et al. Early weaning increases anxiety via brain-derived neurotrophic factor signaling in the mouse prefrontal cortex. Sci. Rep. 9, 3991 (2019).

    ADS  PubMed  PubMed Central  Google Scholar 

  • 71.

    Weinstock, M. The long-term behavioural consequences of prenatal stress. Neurosci. Biobehav. Rev. 32, 1073–1086 (2008).

    CAS  PubMed  Google Scholar 

  • 72.

    Archer, J. E. & Blackman, D. E. Prenatal psychological stress and offspring behavior in rats and mice. Dev. Psychobiol. 4, 193–248 (1971).

    CAS  PubMed  Google Scholar 


  • Source: Ecology - nature.com

    Public health is moot without water security

    Decarbonize and diversify