Maternal separation and early social enrichment increase anxiety-related behaviours of adolescent rats in the elevated plus maze
La separación materna y el enriquecimiento social temprano aumentan los comportamientos relacionados con ansiedad de ratas adolescentes en el laberinto en cruz elevado
Javier L. Rico , Karen Paola Chaverra-Rodríguez , Natalia Garzón-Barbosa , Leonardo A. Ortega
Suma Psicológica, (2024), 31(2), pp. 28-33.
Received 25 September 2023
Accepted 10 September 2024
Introducción: Las condiciones de crianza adversas o favorables en etapas tempranas de la vida afectan la respuesta emocional durante la adolescencia. Para estudiar el efecto de la crianza temprana sobre la respuesta emocional, han sido útiles modelos animales como la separación materna (SM) y el enriquecimiento social (ES) mediante anidamiento comunitario. Sin embargo, se desconoce la comparación del efecto de la SM y el ES sobre las conductas relacionadas con la ansiedad en ratas adolescentes. Objetivo: Este estudio pretende evaluar los efectos de la SM y el ES sobre la respuesta emocional de ratas adolescentes expuestas al test del laberinto en cruz elevado (EPM). Método: Las ratas Wistar preñadas se distribuyeron aleatoriamente en tres grupos según la condición de crianza. En el grupo SM, las crías fueron separadas diariamente de sus madres durante 180 minutos, desde el día postnatal (P) 2 hasta el 14. En el grupo ES, dos hembras que parieron de forma sincronizada se alojaron en una caja con una camada de ocho crías. Las hembras del alojamiento estándar de control (SH) se alojaron individualmente y se mantuvieron con sus crías hasta el destete (P23). En P32, se evaluaron las medidas relacionadas con la ansiedad mediante un EPM. Resultados: La SM y el ES aumentan las conductas relacionadas con la ansiedad y la locomoción en las ratas expuestas al EPM. El ES tuvo efectos dependientes del sexo en las medidas relacionadas con ansiedad, aumentando la actividad vertical en las hembras y la actividad horizontal en los machos. La sm, pero no el ES, incrementó la ganancia de peso corporal en las ratas hembra. Conclusiones: Condiciones de crianza adversas o favorables en etapas tempranas de la vida pueden dar lugar a un fenotipo de ansiedad aumentado en el EPM durante la adolescencia. Es probable que el efecto favorable del ES dependa del número de hembras por nido comunitario.
Palabras clave:
Ansiedad, separación materna, enriquecimiento social, laberinto en cruz elevado, ratas adolescentes.
Introduction: Adverse or favourable rearing conditions early in life affect emotional response during adolescence. To study the effect of early rearing on emotional response, animal models such as maternal separation (MS) and social enrichment (SE) by community nesting have been useful. However, the comparison of the effect of MS and SE on anxiety-related behaviours in adolescent rats is unknown. Objective: This study aimed to assess the effects of MS and SE on the emotional response of adolescent rats exposed to the elevated plus-maze test (EPM). Method: Pregnant Wistar rats were randomly distributed into three groups according to the rearing condition. In the MS group, pups were separated daily from their dams for 180 minutes, from postnatal day (P) 2 to 14. In the SE group, two females that gave birth synchronously were housed in a cage with a litter of eight pups. Females from control standard housing (SH) were individually housed and kept with their offspring until weaning (P23). On P32, anxiety-related measures were evaluated using an EPM. Results: MS and SE increase anxiety-related behaviours and locomotion in rats exposed to the EPM. SE had sex-dependent effects on anxiety-related measures, increasing vertical activity in females and horizontal activity in males. MS but not SE increased body weight gain in female rats. Conclusion: Adverse or favourable rearing conditions early in life may result in an increased anxiety phenotype in the EPM during adolescence. It is likely that the favourable effect of SE depends on the number of dams per communal nest.
Keywords:
Anxiety, maternal separation, social enrichment, elevated plus-maze, adolescent rats.
Arellano, J. I., Duque, A., & Rakic, P. (2024). A coming-of-age story: Adult neurogenesis or adolescent neurogenesis in rodents? Frontiers in Neuroscience, 18. https://doi.org/10.3389/fnins.2024.1383728
Branchi, I., & Alleva, E. (2006). Communal nesting, an early social enrichment, increases the adult anxiety-like response and shapes the role of social context in modulating the emotional behavior. Behavioural Brain Research, 172(2), 299-306. https://doi.org/10.1016/j.bbr.2006.05.019
Bratzu, J., Ciscato, M., Pisanu, A., Talani, G., Frau, R., Porcu, P., Diana, M., Fumagalli, F., Romualdi, P., Rullo, L., Trezza, V., Ciccocioppo, R., Sanna, F., & Fattore, L. (2023). Communal nesting differentially attenuates the impact of pre-weaning social isolation on behavior in male and female rats during adolescence and adulthood. Frontiers in Behavioral Neuroscience, 17. https://doi.org/10.3389/fnbeh.2023.1257417
Carobrez, A. P., & Bertoglio, L. J. (2005). Ethological and temporal analyses of anxiety-like behavior: The elevated plus-maze model 20 years on. Neuroscience & Biobehavioral Reviews, 29(8), 1193-1205. https://doi.org/10.1016/j.neubiorev.2005.04.017
Connors, E. J., Migliore, M. M., Pillsbury, S. L., Shaik, A. N., & Kentner, A. C. (2015). Environmental enrichment models a naturalistic form of maternal separation and shapes the anxiety response patterns of offspring. Psychoneuroendocrinology, 52, 153-167. https://doi.org/10.1016/j.psyneuen.2014.10.021
D’Andrea, I., Gracci, F., Alleva, E., & Branchi, I. (2010). Early social enrichment provided by communal nest increases resilience to depression-like behavior more in female than in male mice. Behavioural Brain Research, 215(1), 71-76. https://doi.org/10.1016/j.bbr.2010.06.030
Eskandari, F., Salimi, M., Binayi, F., Abdollahifar, M.-A., Eftekhary, M., Hedayati, M., Ghanbarian, H., & Zardooz, H. (2023). Investigating the effects of maternal separation on hypothalamic-pituitary-adrenal axis and glucose homeostasis under chronic social defeat stress in young adult male rat offspring. Neuroendocrinology, 113(3), 361–380. https://doi.org/10.1159/000526989
Halladay, L. R., & Herron, S. M. (2023). Lasting impact of postnatal maternal separation on the developing BNST: Lifelong socioemotional consequences. Neuropharmacology, 225, 109404. https://doi.org/10.1016/j.neuropharm.2022.109404
Heiderstadt, K. M., & Blizard, D. A. (2011). Increased juvenile and adult body weights in BALB/cByJ mice reared in a communal nest. Journal of the American Association for Laboratory Animal Science: JAALAS, 50(4), 484-487.
Holly, K. S., Orndorff, C. O., & Murray, T. A. (2016). MATSAP: An automated analysis of stretch-attend posture in rodent behavioral experiments. Scientific Reports, 6, 31286. https://doi.org/10.1038/srep31286
Kraeuter, A.-K., Guest, P. C., & Sarnyai, Z. (2019). The Elevated Plus Maze Test for Measuring Anxiety-Like Behavior in Rodents. En P. C. Guest (Ed.), Pre-Clinical Models: Techniques and Protocols (pp. 69-74). Springer. https://doi.org/10.1007/978-1-4939-8994-2_4
Kuniishi, H., Ichisaka, S., Yamamoto, M., Ikubo, N., Matsuda, S., Futora, E., Harada, R., Ishihara, K., & Hata, Y. (2017). Early deprivation increases high-leaning behavior, a novel anxiety-like behavior, in the open field test in rats. Neuroscience Research, 123, 27-35. https://doi.org/10.1016/j.neures.2017.04.012
Machado, A. G., Silva Silveira, A. C., Peres, A. M., de Sá Couto-Pereira, N., Trindade, A. A., Lúcio, J. A., Lampert, C., August, P. M., Schild Lobo, P. M., Jorge, R. O., Matté, C., Moreira, J. C., Dalmaz, C., & Krolow, R. (2022). Olive oil-rich diet during pregnancy/lactation attenuated the early life stress effects on depressive-like behavior and altered energy metabolism in the dorsal hippocampus in a sex-specific manner. Nutritional Neuroscience, 25(10), 2033-2050. https://doi.org/10.1080/1028415X.2021.1929766
Martinez, A. R., Brunelli, S. A., & Zimmerberg, B. (2015). Communal nesting exerts epigenetic influences on affective and social behaviors in rats selectively bred for an infantile trait. Physiology & Behavior, 139, 97-103. https://doi.org/10.1016/j.physbeh.2014.11.007
Nelson, C. A., Fox, N. A., & Zeanah, C. H. (2023). Romania’s abandoned children: The effects of early profound psychosocial deprivation on the course of human development. Current Directions in Psychological Science, 32(6), 515-521. https://doi.org/10.1177/09637214231201079
Nishi, M. (2020). Effects of early-life stress on the brain and behaviors: Implications of Early maternal separation in rodents. International Journal of Molecular Sciences, 21(19), 7212. https://doi.org/10.3390/ijms21197212
Rico, J. L., Hurtado Parrado, C., Vásquez Sepúlveda, J., Fonseca, J., & Cardona, Á. (2016). Time in the central area of the elevated plus-maze correlates with impulsivity-related measures during an operant task. Universitas Psychologica, 15(5), 14. https://revistas.javeriana.edu.co/index.php/revPsycho/article/view/17054
Ruiz, R., Roque, A., Pineda, E., Licona-Limón, P., José Valdéz-Alarcón, J., & Lajud, N. (2018). Early life stress accelerates age-induced effects on neurogenesis, depression, and metabolic risk. Psychoneuroendocrinology, 96, 203-211. https://doi.org/10.1016/j.psyneuen.2018.07.012
Smith, K. E., & Pollak, S. D. (2020). Early life stress and development: Potential mechanisms for adverse outcomes. Journal of Neurodevelopmental Disorders, 12(34), Article 1. https://doi.org/10.1186/s11689-020-09337-y
Sun, X., Zhang, Y., Li, X., Liu, X., & Qin, C. (2021). Early-life neglect alters emotional and cognitive behavior in a sex-dependent manner and reduces glutamatergic neuronal excitability in the prefrontal cortex. Frontiers in Psychiatry, 11, 572224. https://doi.org/10.3389/fpsyt.2020.572224
Tejada, J., Chaim, K. T., & Morato, S. (2017). X-PloRat: A software for scoring animal behavior in enclosed spaces. Psicologia: Teoria e Pesquisa, 33. https://doi.org/10.1590/0102.3772e3322
Wang, D., Levine, J. L. S., Avila-Quintero, V., Bloch, M., & Kaffman, A. (2020). Systematic review and meta-analysis: Effects of maternal separation on anxiety-like behavior in rodents. Translational Psychiatry, 10(1), 174. https://doi.org/10.1038/s41398-020-0856-0
