DOI: 10.3724/SP.J.1042.2018.00454

Advances in Psychological Science (心理科学进展) 2018/26:3 PP.454-466

Effects of maternal behavior on offspring's psychology and behavior:Based on animal studies

Maternal behavior is a kind of instinctive behavior with strong motivation and regularity, reflected in a series of care and protection for their pups. Previous studies have shown that maternal behavior does not only affect the emotions, the cognitive and learning abilities of offspring, but also relates to the incidence of cardiovascular diseases. Therefore, the influence of maternal behavior on offspring's psychological functions and behavior has received more and more attention in recent years. A lot of researches have explored the influence of maternal behavior on offspring's psychological functions and behavior and tried to elucidate the mechanisms underlying it. While there is no review to discuss the issues above in details. In the present review, we deeply discussed the effects of maternal behavior on the psychological functions and behavior of offspring. Furthermore, we also tried to explainthe limitations of the previous studies. Lastly, in view of these deficiencies, we put forward some suggestions that might improve the future study work in this field.

Key words:maternal behavior,psychological development,behavior development

ReleaseDate:2018-03-29 16:57:02

邝满元, 邓鹏程, 徐松. (2009). 母爱剥夺对子代鼠前额叶皮质c-fos蛋白表达的影响. 解剖科学进展, 15(2), 199-201.

赵晓莲, 齐淑芳, 贾秀月. (2010). 母性行为的研究进展. 黑龙江医药科学, 33(5), 90-91.

Albers, E. M., Riksen-Walraven, J. M., Sweep, F. C. G. J., & de Weerth, C. (2008). Maternal behavior predicts infant cortisol recovery from a mild everyday stressor. Journal of Child Psychology and Psychiatry, 49(1), 97-103.

Anda, R. F., Felitti, V. J., Bremner, J. D., Walker, J. D., Whitfield, C., Perry, B. D., … Giles, W. H. (2006). The enduring effects of abuse and related adverse experiences in childhood. A convergence of evidence from neurobiology and epidemiology. European Archives of Psychiatry and Clinical Neuroscience, 256(3), 174-186.

Baram, T. Z., Davis, E. P., Obenaus, A., Sandman, C. A., Small, S. L., Solodkin, A., & Stern, H. (2012). Fragmentation and unpredictability of early-life experience in mental disorders. The American Journal of Psychiatry, 169(9), 907-915.

Barha, C. K., Pawluski, J. L., & Galea, L. A. M. (2007). Maternal care affects male and female offspring working memory and stress reactivity. Physiology and Behavior, 92(5), 939-950.

Batten, S. V., Aslan, M., Maciejewski, P. K., & Mazure, C. M. (2004). Childhood maltreatment as a risk factor for adult cardiovascular disease and depression. Journal of Clinical Psychiatry, 65(2), 249-254.

Baydar, N., & Brooks-Gunn, J. (1991). Effects of maternal employment and child-care arrangements on preschoolers' cognitive and behavioral outcomes:Evidence from the children of the national longitudinal survey of abuth. Developmental Psychology, 27(6), 932-945.

Bhatnagar, S., & Meaney, M. J. (1995). Hypothalamic-pituitary-adrenal function in chronic intermittently cold-stressed neonatally handled and non handled rats. Journal of Neuroendocrinology, 7(2), 97-108.

Bosch, O. J., Müsch, W., Bredewold, R., Slattery, D. A., & Neumann, I. D. (2007). Prenatal stress increases HPA axis activity and impairs maternal care in lactating female offspring:Implications for postpartum mood disorder. Psychoneuroendocrinology, 32(3), 267-278.

Bredy, T. W., Lee, A. W., Meaney, M. J., & Brown, R. E. (2004). Effect of neonatal handling and paternal care on offspring cognitive development in the monogamous California mouse (Peromyscus californicus). Hormones and Behavior, 46(1), 30-38.

Buijs, R. M., van Eden, C. G., Goncharuk, V. D., & Kalsbeek, A. (2003). The biological clock tunes the organs of the body:Timing by hormones and the autonomic nervous system. Journal of Endocrinology, 177(1), 17-26.

Champagne, F. A., Francis, D. D., Mar, A., & Meaney, M. J. (2003). Variations in maternal care in the rat as a mediating influence for the effects of environment on development. Physiology & Behavior, 79(3), 359-371.

Champagne, F. A., Weaver, I. C. G., Diorio, J., Dymov, S., Szyf, M., & Meaney, M. J. (2006). Maternal care associated with methylation of the estrogen receptor-α1b promoter and estrogen receptor-α expression in the medial preoptic area of female offspring. Endocrinology, 147(6), 2909-2915.

Champagne, F. A. (2008). Epigenetic mechanisms and the transgenerational effects of maternal care. Frontiers in Neuroendocrinology, 29(3), 386-397.

Champagne, F. A., & Curley, J. P. (2009). Epigenetic mechanisms mediating the long-term effects of maternal care on development. Neuroscience & Biobehavioral Reviews, 33(4), 593-600.

Chen, W. H., Zhang, Q., Su, W. X., Zhang, H. R., Yang, Y., Qiao, J., … Li, M. (2014). Effects of 5-hydroxytryptamine 2C receptor agonist MK212 and 2A receptor antagonist MDL100907 on maternal behavior in postpartum female rats. Pharmacology Biochemistry and Behavior, 117, 25-33.

Cirulli, F., Berry, A., & Alleva, E. (2003). Early disruption of the mother-infant relationship:Effects on brain plasticity and implications for psychopathology. Neuroscience & Biobehavioral Reviews, 27(1-2), 73-82.

Cittaro, D., Lampis, V., Luchetti, A., Coccurello, R., Guffanti, A., Felsani, A., … Battaglia, M. (2016). Histone modifications in a mouse model of early adversities and panic disorder:Role for Asic1 and neurodevelopmental genes. Scientific Reports, 6, 25131.

De Azeredo, L. A., Wearick-Silva, L. E., Viola, T. W., Tractenberg, S. G., Centeno-Silva, A., Orso, R.,... Grassi-Oliveira, R. (2017). Maternal separation induces hippocampal changes in cadherin-1 (CDH-1) mRNA and recognition memory impairment in adolescent mice. Neurobiology of Learning and Memory, 141, 157-167.

De Kloet, E. R., Vreugdenhil, E., Oitzl, M. S., & Joëls, M. (1998). Brain corticosteroid receptor balance in health and disease. Endocrine Reviews, 19(3), 269-301.

Dettling, A. C., Feldon, J., & Pryce, C. R. (2002). Repeated parental deprivation in the infant common marmoset (Callithrix jacchus, primates) and analysis of its effects on early development. Biological Psychiatry, 52(11), 1037-1046

Do Prado, C. H., Narahari, T., Holland, F. H., Lee, H. N., Murthy, S. K., & Brenhouse, H. C. (2016). Effects of early adolescent environmental enrichment on cognitive dysfunction, prefrontal cortex development, and inflammatory cytokines after early life stress. Developmental Psychobiology, 58(4), 482-491.

Fairbanks, L. A. (1989). Early experience and cross-generational continuity of mother-infant contact in vervet monkeys. Developmental Psychobiology, 22(7), 669-681.

Farrington, D. P., Gallagher, B., Morley, L., St Ledger, R. J., & West, D. J. (1988). Are there any successful men from criminogenic backgrounds? Psychiatry, 51(2), 116-130.

Francis, D. D., Champagne, F. A., Liu, D., & Meaney, M. J. (1999). Maternal care, gene expression, and the development of individual differences in stress reactivity. Annals of the New York Academic of Sciences, 896(1), 66-84.

Gammie, S. C. (2005). Current models and future directions for understanding the neural circuitries of maternal behaviors in rodents. Behaviroal and Cognitive Neuroscience Review, 4(2), 119-135.

Garner, B., Wood, S. J., Pantelis, C., & van den Buuse, M. (2007). Early maternal deprivation reduces prepulse inhibition and impairs spatial learning ability in adulthood:No further effect of post-pubertal chronic corticosterone treatment. Behavioral Brain Research, 176(2), 323-332.

Grace, S. L., Evindar, A., & Stewart, D. E. (2003). The effect of postpartum depression on child cognitive development and behavior:A review and critical analysis of the literature. Archives of Women's Mental Health, 6(4), 263-274.

Grassi-Oliveira, R., Honeycutt, J. A., Holland, F. H., Ganguly, P., & Brenhouse, H. C. (2016). Cognitive impairment effects of early life stress in adolescents can be predicted with early biomarkers:Impacts of sex, experience, and cytokines. Psychoneuroendocrinology, 71, 19-30.

Hane, A. A., & Fox, N. A. (2006). Ordinary variations in maternal caregiving influence human infants' stress reactivity. Psychological Science, 17(6), 550-556.

Harlow, H. F., & Suomi, S. J. (1971). Social recovery by isolation-reared monkeys. Proceedings of the National Academy of Sciences of the United States of America, 68(7), 1534-1538.

Ho, T. C., Sanders, S. J., Gotlib, I. H., & Hoeft, F. (2016). Intergenerational neuroimaging of human brain circuitry. Trends in Neurosciences, 39(10), 644-648.

Hodges, H. (1996). Maze procedures:The radial-arm and water maze compared. Cognitive Brain Research, 3(3-4), 167-181.

Ichise, M., Vines, D. C., Gura, T., Anderson, G. M., Suomi, S. J., Higley, J. D., & Innis, R. B. (2006). Effects of early life stress on[11C]DASB positron emission tomography imaging of serotonin transporters in adolescent peer-and mother-reared rhesus monkeys. Journal of Neuroscience, 26(17), 4638-4643.

Kaplan, L. A., Evans, L., & Monk, C. (2008). Effects of mothers' prenatal psychiatric status and postnatal caregiving on infant biobehavioral regulation:Can prenatal programming be modified? Early Human Development, 84(4), 249-256.

Katz, M., Liu, C., Schaer, M., Parker, K. J., Ottet, M. C., Epps, A., … Lyons, D. M. (2009). Prefrontal plasticity and stress inoculation-induced resilience. Developmental Neuroscience, 31(4), 293-299.

Knudsen, E. I. (2004). Sensitive periods in the development of the brain and behavior. Journal of Cognitive Neuroscience, 16(8), 1412-1425.

Kuroda, K. O., Tachikawa, K., Yoshida, S., Tsuneoka, Y., & Numan, M. (2011). Neuromolecular basis of parental behavior in laboratory mice and rats:With special emphasis on technical issues of using mouse genetics. Progress in Neuro-Psychopharmacology and Biological Psychiatry, 35(5), 1205-1231.

Lau, C. (2001). Effects of stress on lactation. Pediatric Clinics of North America, 48(1), 221-234

Lau, C., & Simpson, C. (2004). Animal models for the study of the effect of prolonged stress on lactation in rats. Physiology and Behavior, 82(2-3), 193-197.

Law, A. J., Pei, Q., Walker, M., Gordon-Andrews, H., Weickert, C. S., Feldon, J., … Harrison, P. J. (2009). Early parental deprivation in the marmoset monkey produces long-term changes in hippocampal expression of genes involved in synaptic plasticity and implicated in mood disorder. Neuropsychopharmacology, 34(6), 1381-1394.

Leckman, J. F., & Herman, A. E. (2002). Maternal behavior and developmental psychopathology. Biological Psychiatry, 51(1), 27-43.

Levine, S. (2000). Influence of psychological variables on the activity of the hypothalamic-pituitary-adrenal axis. European Journal of Pharmacology, 405(1-3), 149-160.

Li, M. (2015). Antipsychotic drugs on maternal behavior in rats. Behavioral Pharmacology, 26(6), 616-626.

Liu, D., Diorio, J., Day, J. C., Francis, D. D., & Meaney, M. J. (2000). Maternal care, hippocampal synaptogenesis and cognitive development in rats. Nature Neuroscience, 3(8), 799-806.

Luchetti, A., Oddi, D., Lampis, V., Centofante, E., Felsani, A., Battaglia, M., & D'Amato, F. R. (2015). Early handling and repeated cross-fostering have opposite effect on mouse emotionality. Frontiers in Behavioral Neuroscience, 9, 93.

Lyons, D. M., & Parker, K. J. (2007). Stress inoculation-induced indications of resilience in monkeys. Journal of Traumatic Stress, 20(4), 423-433.

Macrí, S., Mason, G. J., & Würbel, H. (2004). Dissociation in the effects of neonatal maternal separations on maternal care and the offspring's HPA and fear responses in rats. European Journal of Neuroscience, 20(4), 1017-1024.

Macrì, S., & Würbel, H. (2006). Developmental plasticity of HPA and fear responses in rats:A critical review of the maternal mediation hypothesis. Hormones and Behavior, 50(5), 667-680.

Maestripieri, D., Badiani, A., & Puglisi-Allegra, S. (1991). Prepartal chronic stress increases anxiety and decreases aggression in lactating female mice. Behavioral Neuroscience, 105(5), 663-668.

Maestripieri, D., Lindell, S. G., Ayala, A., Gold, P. W., & Higley, J. D. (2005). Neurobiological characteristics of rhesus macaque abusive mothers and their relation to social and maternal behavior. Neuroscience & Biobehavioral Reviews, 29(1), 51-57.

Masís-Calvo, M., Sequeira-Cordero, A., Mora-Gallegos, A., & Fornaguera-Trías, J. (2013). Behavioral and neurochemical characterization of maternal care effects on juvenile Sprague-Dawley rats. Physiology & Behavior, 118, 212-217.

Mattson, B. J., Williams, S., Rosenblatt, J. S., & Morrell, J. I. (2001). Comparison of two positive reinforcing stimuli:Pups and cocaine throughout the postpartum period. Behavioral Neuroscience, 115(3), 683-694.

Meaney, M. J., Aitken, D. H., Bhatnagar, S., & Sapolsky, R. M. (1991). Postnatal handling attenuates certain neuroendocrine, anatomical, and cognitive dysfunctions associated with aging in female rats. Neurobiology of Aging, 12(1), 31-38.

Meaney, M. J. (2001). Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Annual of Review Neuroscience, 24, 1161-1192.

Moore, C. L., Wong, L., Daum, M. C., & Leclair, O. U. (1997). Mother-infant interactions in two strains of rats:Implications for dissociating mechanism and function of a maternal pattern. Developmental Psychobiology, 30(4), 301-312.

Moriceau, S., & Sullivan, R. M. (2006). Maternal presence serves as a switch between learning fear and attraction in infancy. Nature Neuroscience, 9(8), 1004-1006.

Murphy, K. M., Berg, K. D., & Eshleman, J. R. (2005). Sequencing of genomic DNA by combined amplification and cycle sequencing reaction. Clinical Chemistry, 51(1), 35-39.

Nephew, B. C., & Bridges, R. S. (2011). Effects of chronic social stress during lactation on maternal behavior and growth in rats. Stress, 14(6), 677-684.

Numan, M., & Young, L. J. (2016). Neural mechanisms of mother-infant bonding and pair bonding:Similarities, differences, and broader implications. Hormones and Behavior, 77, 98-112.

Ohiwa, N., Saito, T., Chang, H., Nakamura, T., & Soya, H. (2006). Differential responsiveness of c-Fos expression in the rat medulla oblongata to different treadmill running speeds. Neurosciende Research, 54(2), 124-132.

Park, M. K., Hoang, T. A., Belluzzi, J. D., & Leslie, F. M. (2003). Gender specific effect of neonatal handling on stress reactivity of adolescent rats. Journal of Neuroendocrinology, 15(3), 289-295

Parker, K. J., & Maestripieri, D. (2011). Identifying key features of early stressful experiences that produce stress vulnerability and resilience in primates. Neuroscience & Biobehavioral Reviews, 35(7), 1466-1483.

Penza, K. M., Heim, C., & Nemeroff, C. B. (2003). Neurobiological effects of childhood abuse:Implications for the pathophysiology of depression and anxiety. Archives of Women's Mental Health, 6(1), 15-22.

Phillips, N. K., Hammen, C. L., Brennan, P. A., Najman, J. M., & Bor, W. (2005). Early adversity and the prospective prediction of depressive and anxiety disorders in adolescents. Journal of Abnormal Child Psychology, 33(1), 13-24.

Read, J., van Os, J., Morrison, A. P., & Ross, C. A. (2005). Childhood trauma, psychosis and schizophrenia:A literature review with theoretical and clinical implications. Acta Psychiatrica Scandinavica, 112(5), 330-350.

Reincke, S. A. J., & Hanganu-Opatz, I. L. (2017). Early-life stress impairs recognition memory and perturbs the functional maturation of prefrontal-hippocampal-perirhinal networks. Scientific Reports, 7, 42042.

Roy, P., Rutter, M., & Pickles, A. (2004). Institutional care:Associations between overactivity and lack of selectivity in social relationships. Journal of Child Psychology Psychiatry, 45(4), 866-873.

Ruddy, M. G., & Bornstein, M. H. (1982). Cognitive correlates of infant attention and maternal stimulation over the first year of life. Child Development, 53(1), 183-188

Sachser, N., Hennessy, M. B., & Kaiser, S. (2011). Adaptive modulation of behavioural profiles by social stress during early phases of life and adolescence. Neuroscience and Biobehavioral Reviews, 35(7), 1518-1533.

Sale, A., Putignano, E., Cancedda, L., Landi, S., Cirulli, F., Berardi, N., Maffei, L. (2004). Enriched environment and acceleration of visual system development. Neuropharmacology, 47(5), 649-660.

Shumake, J., Barrett, D., & Gonzalez-Lima, F. (2005). Behavioral characteristics of rats predisposed to learned helplessness:Reduced reward sensitivity, increased novelty seeking, and persistent fear memories. Behavioural Brain Research, 164(2), 222-230.

Smith, J., & Prior, M. (1995). Temperament and stress resilience in school-age children:A within-families study. Journal of the American Academy Child & Adolescent Psychiatry, 34(2), 168-179.

Smith, J. W., Seckl, J. R., Evans, A. T., Costall, B., & Smythe, J. W. (2004). Gestational stress induces post-partum depression-like behaviour and alters maternal care in rats. Psychoneuroendocrinology, 29(2), 227-244.

Stevens, H. E., Leckman, J. F., Coplan, J. D., & Suomi, S. J. (2009). Risk and resilience:Early manipulation of macaque social experience and persistent behavioral and neurophysiological outcomes. Journal of the American Academy Child & Adolescent Psychiatry, 48(2), 114-127.

Suomi, S. J., Harlow, H. F., & Kimball, S. D. (1971). Behavioral effects of prolonged partial social isolation in the rhesus monkey. Psychological Reports, 29(3), 1171-1177.

Thomas, A. W., Caporale, N., Wu, C., & Wilbrecht, L. (2016). Early maternal separation impacts cognitive flexibility at the age of first independence in mice. Developmental Cognitive Neuroscience, 18, 49-56.

Uriarte, N., Breigeiron, M. K., Benetti, F., Rosa, X. F., & Lucion, A. B. (2007). Effects of maternal care on the development, emotionality, and reproductive functions in male and female rats. Developmental Psychobiology, 49(5), 451-462.

Walker, C. D. (2010). Maternal touch and feed as critical regulators of behavioral and stress responses in the offspring. Developmental Psychobiology, 52(7), 638-650.

Wan, M. W., & Green, J. (2010). Negative and atypical story content themes depicted by children with behaviour problems. Journal of Child Psychology and Psychiatry, 51(10), 1125-1131.

Weaver, I. C. G., Cervoni, N., Champagne, F. A., D'Alessio, A. C., Sharma, S., Seckl, J. R., … Meaney, M. J. (2004). Epigenetic programming by maternal behavior. Nature Neuroscience, 7(8), 847-854.