Influence of environmental enrichment on the volume of brain regions sensitive to early life stress by maternal separation in rats

  1. Héctor González-Pardo 1
  2. Jorge Luis Arias Pérez 1
  3. Nélida María Conejo Jiménez 1
  1. 1 Universidad de Oviedo
    info

    Universidad de Oviedo

    Oviedo, España

    ROR https://ror.org/006gksa02

Revista:
Psicothema

ISSN: 0214-9915 1886-144X

Año de publicación: 2019

Volumen: 31

Número: 1

Páginas: 46-52

Tipo: Artículo

Otras publicaciones en: Psicothema

Resumen

Background: Exposure to maternal separation (MS) in rodents may have long-lasting consequences for the structure and function of several brain regions, eventually associated with alterations in cognition and emotion later in life. Post-weaning environmental enrichment (EE) has been reported to ameliorate the detrimental effects of exposure to early life stress mainly in the hippocampus. Method: In vivo magnetic resonance imaging (MRI) was applied to evaluate possible volumetric changes in the dorsal and ventral hippocampus, the medial prefrontal cortex and the dorsal striatum of 90-day-old male rats after daily MS for 240 min from postnatal days 2-21. Results: No signifi cant volume changes were found in the selected brain regions in MS animals as compared with an agematched control group. However, additional groups of control and MS animals with EE from days 21-60 showed signifi cant volume increases in the medial prefrontal cortex and the ventral hippocampus as compared to the groups without EE. In addition, general hemispheric asymmetry was found in the volume of the brain regions measured. Conclusions: Our results demonstrate that EE could have differential effects depending on previous exposure to MS and on the development of brain lateralization.

Referencias bibliográficas

  • Baker, L.M., Williams, L.M., Korgaonkar, M.S., Cohen, R.A., Heaps, J.M., & Paul, R.H. (2013). Impact of early vs. late childhood early life stress on brain morphometrics. Brain Imaging and Behavior, 7, 196203. doi:10.1007/s11682-012-9215-y
  • Banqueri, M., Méndez, M., & Arias, J.L. (2017a). Impact of stress in childhood: Psychobiological alterations. Psicothema, 29, 18-22. doi:10.7334/psicothema2016.264
  • Benjamini, Y., & Hochberg, Y. (1995). Controlling the false discovery rate: A practical and powerful approach to multiple testing. Journal of the Royal Statistical Society: Series B (Statistical Methodology), 57, 289-300. doi:10.1111/j.2517-6161.1995.tb02031.x
  • Banqueri, M., Méndez, M., & Arias, J.L. (2017b). Behavioral effects in adolescence and early adulthood in two length models of maternal separation in male rats. Behavioural Brain Research, 324, 77-86. doi:10.1016/j.bbr.2017.02.006
  • Bennett, E.L., Rosenzweig, M.R., & Diamond, M.C. (1969). Rat brain: Effects of environmental enrichment on wet and dry weights. Science, 163, 825-826. doi:10.1126/science.163.3869.825
  • Bremner, J.D., Vythilingam, M., Vermetten, E., Southwick, S.M., McGlashan, T., Nazeer, A., …. Charney, D.S. (2003). MRI and PET study of deficits in hippocampal structure and function in women with childhood sexual abuse and posttraumatic stress disorder. American Journal of Psychiatry, 160, 924-932. doi:10.1176/appi.ajp.160.5.924
  • Cohen, R.A., Grieve, S., Hoth ,K.F., Paul, R.H., Sweet. L., … Williams, L.M. (2006). Early life stress and morphometry of the adult anterior cingulate cortex and caudate nuclei. Biological Psychiatry, 59, 97582. doi:10.1016/j.biopsych.2005.12.016
  • Colomina, M,T., Sánchez-Santed, F., Conejo, N.M., Collado, P., Salvador, A., Gallo, M., Pinos, H., Salas, C., Navarro, J.F., Adán, A., Azpiroz, A., & Arias, J.L. (2018). The psychoexposome: a holistic perspective beyond health and disease. Psicothema, 30, 15-17. doi:10.7334/psicothema2017.244
  • Dannlowski, U., Stuhrmann, A., Beutelmann, V., Zwanzger P., Lenzen, T., Grotegerd, D., ... Kugel, H. (2012). Limbic scars: Long-term consequences of childhood maltreatment revealed by functional and structural magnetic resonance imaging. Biological Psychiatry, 71, 286-293. doi:10.1016/j.biopsych.2011.10.021
  • Diamond, M.C., Krech, D., & Rosenzweig, M.R. (1964). The effects of an enriched environment on the histology of the rat cerebral cortex. Journal of Comparative Neurology, 123, 111-120. doi:10.1002/cne.901230110
  • Gilmer, W.S., & McKinney, W.T. (2003). Early experience and depressive disorders: Human and non-human primate studies. Journal of Affective Disorders, 75, 97-113. doi:10.1016/s0165-0327(03)00046-6
  • González-Pardo, H., & Pérez Álvarez, M. (2013). Epigenetics and its implications for Psychology. Psicothema, 25, 3-12. doi:10.7334/psicothema2012.327
  • He, C., Tsipis, C.P., LaManna, J.C., & Xu, K. (2017). Environmental enrichment induces increased cerebral capillary density and improved cognitive function in mice. Advances in Experimental Medicine and Biology, 977, 175-181. doi:10.1007/978-3-319-55231-6_24
  • Hebb, D. O. (1947). The effects of early experience on problem solving at maturity. American Psychologist, 2, 206-307. doi:
  • Herpfer, I., Hezel, H., Reichardt, W., Clark, K., Geiger, J., Gross, C.M., ... Normann, C. (2012). Early life stress differentially modulates distinct forms of brain plasticity in young and adult mice. PLoS One, 7, e46004. doi:10.1371/journal.pone.0046004
  • Hirase, H., & Shinohara, Y. (2014). Transformation of cortical and hippocampal neural circuit by environmental enrichment. Neuroscience, 280, 282-298. doi:10.1016/j.neuroscience.2014.09.031
  • Hui, J.J., Zhang, Z.J., Liu, S.S., Xi, G.J., Zhang, X.R., Teng, G.J., … Reynolds, G.P. (2011). Hippocampal neurochemistry is involved in the behavioural effects of neonatal maternal separation and their reversal by post-weaning environmental enrichment: A magnetic resonance study. Behavioural Brain Research, 217, 122-127. doi:10.1016/j.bbr.2010.10.014
  • Konkle, A.T., Kentner, A.C., Baker, S.L., Stewart, A., & Bielajew, C. (2010). Environmental-enrichment-related variations in behavioral, biochemical, and physiologic responses of Sprague-Dawley and Long Evans rats. Journal of the American Association for Laboratory Animal Science, 49, 427-436. doi:10.30802/aalas-jaalas-17-000122
  • Leeb, R.T., Paulozzzi, L., Melanson, C., Simon, T., & Arias, I. (2008). Child Maltreatment Surveillance: Uniform definitions for Public Health and Recommended Data Elements. Atlanta: Centers for Disease Control and Prevention, USA. doi:10.1037/e587022010001
  • Lerch, J.P., Yiu, A.P., Martínez-Canabal, A., Pekar, T., Bohbot, V.D., Frankland, P.W., … Sled, J.G. (2011). Maze training in mice induces MRI-detectable brain shape changes specifi c to the type of learning. Neuroimage, 54, 2086-2095. doi:10.1016/j.neuroimage.2010.09.086
  • Luo, Y., Cao, Z., Wang, D., Wu, L., Li, Y., Sun, W., & Zhu, Y. (2014). Dynamic study of the hippocampal volume by structural MRI in a rat model of depression. Neurological Sciences, 35, 1777-1783. doi:10.1007/s10072-014-1837-y
  • Macrì, S., Chiarotti, F., & Würbel, H. (2008). Maternal separation and maternal care act independently on the development of HPA responses in male rats. Behavioural Brain Research, 191, 227-234. doi:10.1016/j.bbr.2008.03.031
  • Morley-Fletcher, S., Rea, M., Maccari, S., & Laviola, G. (2003). Environmental enrichment during adolescence reverses the effects of prenatal stress on play behaviour and HPA axis reactivity in rats. European Journal of Neuroscience, 18, 3367-3374. doi:10.1111/j.14609568.2003.03070.x
  • Nelson, C.A., Zeanah, C.H., Fox, N.A., Marshall, P.J., Smyke, A.T., & Guthrie, D., (2007). Cognitive recovery in socially deprived young children: The Bucharest Early Intervention Project. Science, 318, 1937-1940. doi:10.1016/s0084-3970(08)79223-5
  • O’Doherty, D.C., Chitty, K.M., Saddiqui, S., Bennett, M.R., & Lagopoulos, J.A., (2015). Systematic review and meta-analysis of magnetic resonance imaging measurement of structural volumes in posttraumatic stress disorder. Psychiatry Research, 232, 1-33. doi:10.1016/j.pscychresns.2015.01.002
  • Ryu, V., Yoo, S.B., Kang, D.W., Lee, J.H., & Jahng, J.W. (2009). Postweaning isolation promotes food intake and body weight gain in rats that experienced neonatal maternal separation. Brain Research, 1295, 127-134. doi:10.1016/j.brainres.2009.08.006
  • Saleh, A., Potter, G.G., McQuoid, D.R., Boyd, B., Turner, R., MacFall, J.R., & Taylor, W.D. (2017). Effects of early life stress on depression, cognitive performance and brain morphology. Psychological Medicine, 47, 171-181. doi:10.1017/s0033291716002403
  • Schiffer, W.K., Mirrione, M.M., Biegon, A., Alexoff, D.L., Patel, V., & Dewey, S.L. (2006.) Serial microPET measures of the metabolic reaction to a microdialysis probe implant. Journal of Neuroscience Methods, 155, 272-284. doi:10.1016/j.jneumeth.2006.01.027
  • Scholz, J., Allemang-Grand, R., Dazai, J., & Lerch, J.P. (2015). Environmental enrichment is associated with rapid volumetric brain changes in adult mice. Neuroimage, 109, 190-198. doi:10.1016/j.neuroimage.2015.01.027
  • Simpson, J., & Kelly, J.P. (2011). The impact of environmental enrichment in laboratory rats behavioural and neurochemical aspects. Behavioural Brain Research, 222, 246-264. doi:10.1016/j.bbr.2011.04.002
  • Sullivan, R.M. (2004). Hemispheric asymmetry in stress processing in rat prefrontal cortex and the role of mesocortical dopamine. Stress, 7, 131-143. doi:10.1080/102538900410001679310
  • Taylor, S.E., Way, B.M., & Seeman, T.E. (2011). Early adversity and adult health outcomes. Developmental Psychopathology, 23, 939-954. doi:10.1017/s0954579411000411
  • Teicher, M.H., & Samson, J.A. (2016). Annual research review: Enduring neurobiological effects of childhood abuse and neglect. Journal of Child Psychology and Psychiatry, and Allied Disciplines, 57, 241-266. doi:10.1111/jcpp.12507
  • Toth, L.A., Kregel, K., Leon, L., & Musch, T.I. (2011). Environmental enrichment of laboratory rodents: The answer depends on the question. Comparative Medicine, 61, 314-321. doi:10.2139/ssrn.3169603
  • van Bodegom, M., Homberg, J.R., & Henckens, M.J.A.G. (2017). Modulation of the Hypothalamic-Pituitary-Adrenal axis by early life stress exposure. Frontiers in Cellular Neuroscience, 11, 87-93. doi:10.3389/fncel.2017.00087
  • van Praag, H., Kempermann, G., & Gage, F.H. (2000). Neural consequences of environmental enrichment. Nature Reviews. Neuroscience, 1, 191198. doi:10.1038/35044558
  • Videbech, P., & Ravnkilde, B. (2004). Hippocampal volume and depression: A meta-analysis of MRI studies. American Journal of Psychiatry, 161, 1957-1966. doi:10.1176/appi.ajp.161.11.1957
  • Wang, Q., Li, M., Du, W., Shao, F., & Wang, W. (2015). The different effects of maternal separation on spatial learning and reversal learning in rats. Behavioural Brain Research, 280, 16-23. doi:10.1016/j. bbr.2014.11.040
  • Würbel, H. (2001). Ideal homes? Housing effects on rodent brain and behaviour. Trends in Neuroscience, 24, 207-211. doi:10.1016/s01662236(00)01718-5