Effects of Maternal Deprivation on Anxiety, Depression, and Empathy in Male and Female Offspring of Wistar Rats in the Face of Novel Objects
AbstractBackground: Early life stress (ELS) models such as maternal deprivation (MD) are used to in¬vestigate behavioral changes in rodents under stressful situations. MD is a situation in which rat pups are separated from the dam; MD has different paradigms. The purpose of this research is to evaluate the effects of maternal deprivation on anxiety, depression, and empathy in adult Wistar rats. Materials and Methods: MD was applied to pups as per specifically designed protocol to compare rats of the control group with maternal deprivation rats and also the group, which faced novel objects. Each group consisted of eight rats. In this study, separation started from postnatal day (PND) 14 for various periods up to PND 60. EPM test was undertaken to measure anxiety; moreover, FST was used to indicate levels of depression. Also, changes in the empathy ratio were also demonstrated. One-way analysis of variance (ANOVA), Tukey’s post hoc analysis, and t-test were applied to analyze the results. Results: MD-treated rats showed a significant decrease in anxiety and empathy indexes compared with those in the control group (P<0.05). However, MD significantly increased depression in both male and female rats (P<0.05). Final¬ly, exposure to novel objects decreased depression but did not have any effect on anxiety and empathy levels in MD rats (P<0.05). Conclusion: ELS may lead to various states of mood and behavior in adulthood. According to the findings of this study, depression increases due to MD, though both anxiety and empathy decrease in both male and female Wistar rats. Moreover, ex¬posure to novel objects decreases depression, while anxiety and empathy do not change signifi¬cantly with exposure to novel objects. [GMJ.2019;8:e1093]
Aleksic D, Aksic M, Radonjic NV, Jovanovic A, Markovic B, Petronijevic N, et al. Long-term Effects of Maternal Deprivation on the Volume, Number and Size of Neurons in the Amygdala and Nucleus Accumbens of Rats. Psychiatria Danubina. 2016;28(3):211-9.
Yin X, Chen L, Xia Y, Cheng Q, Yuan J, Yang Y, et al. Maternal Deprivation Influences Pup Ultrasonic Vocalizations of C57BL/6J Mice. PloS one. 2016;11(8):e0160409.
Zimmerberg B, Sageser KA. Comparison of two rodent models of maternal separation on juvenile social behavior. Frontiers in psychiatry. 2011;2:39.
Bouayed J, Rammal H, Soulimani R. Oxidative stress and anxiety: relationship and cellular pathways. Oxidative medicine and cellular longevity. 2009;2(2):63-7.
Daniel R. Weinberger MD. Anxiety at the Frontier of Molecular Medicine. N Engl J Med. 2001.
Etebary S, Nikseresht S, Sadeghipour HR, Zarrindast MR. Postpartum depression and role of serum trace elements. Iranian journal of psychiatry. 2010;5(2):40-6.
Lebedeva KA, Caruncho HJ, Kalynchuk LE. Cyclical corticosterone administration sensitizes depression-like behavior in rats. Neuroscience letters. 2017;650:45-51.
Carter GG, Wilkinson GS. Food sharing in vampire bats: reciprocal help predicts donations more than relatedness or harassment. Proceedings Biological sciences. 2013;280(1753):20122573.
Bradley ALBaCWELBJ. Communal nesting, kinship, and maternal success in a social primate. Behavioral Ecology and Sociobiology. 2013;67(12).
Clay Z, de Waal FB. Bonobos respond to distress in others: consolation across the age spectrum. PloS one. 2013;8(1):e55206.
BJ Hatchwell. ea. Ecological and demographic correlates of helping behaviour in cooperativly breeding bird. Journal of Animal Ecology. 2013;82(2):486-94.
Panksepp J, Panksepp JB. Toward a cross-species understanding of empathy. Trends in neurosciences. 2013;36(8):489-96.
Preston SD. The origins of altruism in offspring care. Psychological bulletin. 2013;139(6):1305-41.
Akyazi I, Eraslan E. Transmission of stress between cagemates: a study in rats. Physiology & behavior. 2014;123:114-8.
Chen J, Li Z, Lv YF, Li CL, Wang Y, Wang RR, et al. [Empathy for pain: A novel bio-psychosocial-behavioral laboratory animal model]. Sheng li xue bao : [Acta physiologica Sinica]. 2015;67(6):561-70.
Pellow S, File SE. Anxiolytic and anxiogenic drug effects on exploratory activity in an elevated plus-maze: a novel test of anxiety in the rat. Pharmacology, biochemistry, and behavior. 1986;24(3):525-9.
Walf AA, Frye CA. The use of the elevated plus maze as an assay of anxiety-related behavior in rodents. Nature protocols. 2007;2(2):322-8.
Zarrindast MR, Khalifeh S, Rezayof A, Rostami P, Aghamohammadi Sereshki A, Zahmatkesh M. Involvement of rat dopaminergic system of nucleus accumbens in nicotine-induced anxiogenic-like behaviors. Brain research. 2012;1460:25-32.
Yankelevitch-Yahav R, Franko M, Huly A, Doron R. The forced swim test as a model of depressive-like behavior. Journal of visualized experiments : JoVE. 2015(97).
Voiculescu SE, Rosca AE, Zeca V, Zagrean L, Zagrean AM. Impact of maternal melatonin suppression on forced swim and tail suspension behavioral despair tests in adult offspring. Journal of medicine and life. 2015;8(2):202-6.
Zare N, Khalifeh S, Khodagholi F, Shahamati SZ, Motamedi F, Maghsoudi N. Geldanamycin Reduces Abeta-Associated Anxiety and Depression, Concurrent with Autophagy Provocation. Journal of molecular neuroscience : MN. 2015;57(3):317-24.
Ben-Ami Bartal I, Shan H, Molasky NM, Murray TM, Williams JZ, Decety J, et al. Anxiolytic Treatment Impairs Helping Behavior in Rats. Frontiers in psychology. 2016;7:850.
Fedotova J, Pivina S, Sushko A. Effects of Chronic Vitamin D(3) Hormone Administration on Anxiety-Like Behavior in Adult Female Rats after Long-Term Ovariectomy. Nutrients. 2017;9(1).
Skripuletz T, Kruschinski C, Pabst R, von Horsten S, Stephan M. Postnatal experiences influence the behavior in adult male and female Fischer and Lewis rats. International journal of developmental neuroscience : the official journal of the International Society for Developmental Neuroscience. 2010;28(7):561-71.
Pascual R, Zamora-Leon SP. Effects of neonatal maternal deprivation and postweaning environmental complexity on dendritic morphology of prefrontal pyramidal neurons in the rat. Acta neurobiologiae experimentalis. 2007;67(4):471-9.
Porsolt RD, Anton G, Blavet N, Jalfre M. Behavioural despair in rats: a new model sensitive to antidepressant treatments. European journal of pharmacology. 1978;47(4):379-91.
Jenkins JA, Williams P, Kramer GL, Davis LL, Petty F. The influence of gender and the estrous cycle on learned helplessness in the rat. Biological psychology. 2001;58(2):147-58.
Mourlon V, Baudin A, Blanc O, Lauber A, Giros B, Naudon L, et al. Maternal deprivation induces depressive-like behaviours only in female rats. Behavioural brain research. 2010;213(2):278-87.
Decety J. The neuroevolution of empathy. Annals of the New York Academy of Sciences. 2011;1231:35-45.
Eisenberg N, Miller PA. The relation of empathy to prosocial and related behaviors. Psychological bulletin. 1987;101(1):91-119.
Decety J, Svetlova M. Putting together phylogenetic and ontogenetic perspectives on empathy. Developmental cognitive neuroscience. 2012;2(1):1-24.
Preston SD, de Waal FB. Empathy: Its ultimate and proximate bases. The Behavioral and brain sciences. 2002;25(1):1-20; discussion -71.
Langford DJ, Crager SE, Shehzad Z, Smith SB, Sotocinal SG, Levenstadt JS, et al. Social modulation of pain as evidence for empathy in mice. Science. 2006;312(5782):1967-70.
Chen Q, Panksepp JB, Lahvis GP. Empathy is moderated by genetic background in mice. PloS one. 2009;4(2):e4387.
Ben-Ami Bartal I, Rodgers DA, Bernardez Sarria MS, Decety J, Mason P. Pro-social behavior in rats is modulated by social experience. eLife. 2014;3:e01385.
C. Daniel Batson DAL, Jennifer Cook & Stacey Sawyer. Similarity and Nurturance: Two Possible Sources of Empathy for Strangers. Basic and Applied Social Psychology 2005;27(1):15-25.
Horner V, Carter JD, Suchak M, de Waal FB. Spontaneous prosocial choice by chimpanzees. Proceedings of the National Academy of Sciences of the United States of America. 2011;108(33):13847-51.
Xu X, Zuo X, Wang X, Han S. Do you feel my pain? Racial group membership modulates empathic neural responses. The Journal of neuroscience : the official journal of the Society for Neuroscience. 2009;29(26):8525-9.
Chiao JY, Iidaka T, Gordon HL, Nogawa J, Bar M, Aminoff E, et al. Cultural specificity in amygdala response to fear faces. Journal of cognitive neuroscience. 2008;20(12):2167-74.
Elfenbein HA, Ambady N. When familiarity breeds accuracy: cultural exposure and facial emotion recognition. Journal of personality and social psychology. 2003;85(2):276-90.
Madsen EA, Tunney RJ, Fieldman G, Plotkin HC, Dunbar RI, Richardson JM, et al. Kinship and altruism: a cross-cultural experimental study. British journal of psychology. 2007;98(Pt 2):339-59.
Telzer EH, Flannery J, Shapiro M, Humphreys KL, Goff B, Gabard-Durman L, et al. Early experience shapes amygdala sensitivity to race: an international adoption design. The Journal of neuroscience : the official journal of the Society for Neuroscience. 2013;33(33):13484-8.
Xiangyu Zuo SH. Cultural experiences reduce racial bias in neural responses to others' suffering. Culture and Brain. 2013;1(1):34-46.
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