Share This Article:

Qualitative Differences in Pup-Retrieval Strategies in a Maternal Separation Paradigm

Full-Text HTML XML Download Download as PDF (Size:818KB) PP. 603-616
DOI: 10.4236/jbbs.2013.38064    3,768 Downloads   5,029 Views   Citations


The rodent maternal separation (MS) paradigm is frequently used to investigate the impact of early-life conditions in the offspring. One critical issue is whether the effects seen in the offspring are a result of maternal contact deprivation and/or altered pup-directed maternal behavior. To address this question we used an innovative approach with a qualitative analysis of pup-retrieval strategies in a test situation related to risk for the pups. The dams were separated from their litters for 0 (MS0) or 360 (MS360) min, respectively. The pups were placed in a risk area in the multivariate concentric square field? test at two test occasions and the pup-retrieval strategies were recorded. No significant evident differences between MS0 and MS360 dams were found. However, there were clearly two different strategies, either removing the pups out of potential danger or into safety, and these strategies were represented in both MS groups. As compared to the MS0 dams, the MS360 dams did not change their strategies and left more pups in the risk area in both pup-retrieval tests. This implies different pup-retrieval strategies depending on early-life conditions.


Conflicts of Interest

The authors declare no conflicts of interest.

Cite this paper

L. Daoura, I. Nylander and E. Roman, "Qualitative Differences in Pup-Retrieval Strategies in a Maternal Separation Paradigm," Journal of Behavioral and Brain Science, Vol. 3 No. 8, 2013, pp. 603-616. doi: 10.4236/jbbs.2013.38064.


[1] P. D. Gluckman, M. A. Hanson and A. S. Beedle, “Early Life Events and Their Consequences for Later Disease: A Life History and Evolutionary Perspective,” American Journal of Human Biology, Vol. 19, No. 1, 2007, pp. 1-19.
[2] E. McCrory, S. A. De Brito and E. Viding, “The Impact of Childhood Maltreatment: A Review of Neurobiological and Genetic Factors,” Front Psychiatry, Vol. 2, 2011, pp. 1-14.
[3] F. Crews, J. He and C. Hodge, “Adolescent Cortical Development: A Critical Period of Vulnerability for Addiction,” Pharmacology Biochemistry and Behavior, Vol. 86, No. 2, 2007, pp. 189-199.
[4] R. K. Lenroot and J. N. Giedd, “The Changing Impact of Genes and Environment on Brain Development during Childhood and Adolescence: Initial Findings from a Neuroimaging Study of Pediatric Twins,” Developmental Psychobiology, Vol. 20, No. 4, 2008, pp. 1161-1175.
[5] R. D. Romeo and B. S. McEwen, “Stress and the Adolescent Brain,” Annals of the New York Academy of Sciences, Vol. 1094, 2006, pp. 202-214.
[6] A. Feder, E. J. Nestler and D. S. Charney, “Psychobiology and Molecular Genetics of Resilience,” Nature Reviews Neuroscience, Vol. 10, No. 6, 2009, pp. 446-457.
[7] J. Kim-Cohen, “Resilience and Developmental Psychopathology,” Child & Adolescent Psychiatric Clinics of North America, Vol. 16, No. 2, 2007, pp. 271-283.
[8] C. B. Nemeroff, “Neurobiological Consequences of Childhood Trauma,” Journal of Clinical Psychiatry, Vol. 65, Suppl. 1, 2004, pp. 18-28.
[9] R. Sinha, “Chronic Stress, Drug Use, and Vulnerability to Addiction,” Annals of the New York Academy of Sciences, Vol. 1141, 2008, pp. 105-130.
[10] U. Ehlert, “Enduring Psychobiological Effects of Childhood Adversity,” Psychoneuroendocrinology, Vol. 38, No. 9, 2013, pp. 1850-1857.
[11] J. Murray and L. Murray, “Parental Incarceration, Attachment and Child Psychopathology,” Attachment & Human Development, Vol. 12, No. 4, 2010, pp. 289-309.
[12] C. Heim, M. Shugart, W. E. Craighead and C. B. Nemeroff, “Neurobiological and Psychiatric Consequences of Child Abuse and Neglect,” Developmental Psychobiology, Vol. 52, No. 7, 2010, pp. 671-690.
[13] M. D. De Bellis, “Developmental Traumatology: A Contributory Mechanism for Alcohol and Substance Use Disorders,” Psychoneuroendocrinology, Vol. 27, No. 1-2, 2002, pp. 155-170.
[14] W. Langeland, N. Draijer and W. van den Brink, “Psychiatric Comorbidity in Treatment-Seeking Alcoholics: The Role of Childhood Trauma and Perceived Parental Dysfunction,” Alcoholism: Clinical and Experimental Research, Vol. 28, No. 3, 2004, pp. 441-447.
[15] E. R. de Kloet, R. M. Sibug, F. M. Helmerhorst and M. V. Schmidt, “Stress, Genes and the Mechanism of Programming the Brain for Later Life,” Neuroscience & Biobehavioral Reviews, Vol. 29, No. 2, 2005, pp. 271-281.
[16] C. R. Pryce, D. Ruedi-Bettschen, A. C. Dettling, A. Weston, H. Russig, B. Ferger and J. Feldon, “Long-Term Effects of Early-Life Environmental Manipulations in Rodents and Primates: Potential Animal Models in Depression Research,” Neuroscience & Biobehavioral Reviews, Vol. 29, No. 4-5, 2005, pp. 649-674.
[17] I. Nylander and E. Roman, “Neuropeptides as Mediators of the Early-Life Impact on the Brain; Implications for alcohol Use Disorders,” Frontiers in Molecular Neuroscience, Vol. 5, 2012, pp. 1-19.
[18] A. Holmes, A. M. le Guisquet, E. Vogel, R. A. Millstein, S. Leman and C. Belzung, “Early Life Genetic, Epigenetic and Environmental Factors Shaping Emotionality in Rodents,” Neuroscience & Biobehavioral Reviews, Vol. 29, No. 8, 2005, pp. 1335-1346.
[19] I. Nylander and E. Roman, “Is the Rodent Maternal Separation Model a Valid and Effective Model for Studies on the Early-Life Impact on Ethanol Consumption?” Psychopharmacology (Berl), Vol. 229, No. 4, 2013, pp. 555-569.
[20] H. C. Becker, M. F. Lopez and T. L. Doremus-Fitzwater, “Effects of Stress on Alcohol Drinking: A Review of Animal Studies,” Psychopharmacology (Berl), Vol. 218, No. 1, 2011, pp. 131-156.
[21] C. O. Ladd, R. L. Huot, K. V. Thrivikraman, C. B. Nemeroff, M. J. Meaney and P. M. Plotsky, “Long-Term Behavioral and Neuroendocrine Adaptations to Adverse Early Experience,” Progress in Brain Research, Vol. 122, 2000, pp. 81-103.
[22] S. Macri and H. Wurbel, “Developmental Plasticity of HPA and Fear Responses in Rats: A Critical Review of the Maternal Mediation Hypothesis,” Hormones and Behavior, Vol. 50, No. 5, 2006, pp. 667-680.
[23] C. R. Pryce, D. Bettschen and J. Feldon, “Comparison of the Effects of Early Handling and Early Deprivation on Maternal Care in the Rat,” Developmental Psychobiology, Vol. 38, No. 4, 2001, pp. 239-251.
[24] M. L. Boccia, M. Razzoli, S. P. Vadlamudi, W. Trumbull, C. Caleffie and C. A. Pedersen, “Repeated Long Separations from Pups Produce Depression-Like Behavior in Rat Mothers,” Psychoneuroendocrinology, Vol. 32, No. 1, 2007, pp. 65-71.
[25] R. M. Sapolsky and M. J. Meaney, “Maturation of the Adrenocortical Stress Response: Neuroendocrine Control Mechanisms and the Stress Hyporesponsive Period,” Brain Research, Vol. 396, No. 1, 1986, pp. 64-76.
[26] A. S. Fleming, D. H. O’Day and G. W. Kraemer, “Neurobiology of Mother-Infant Interactions: Experience and Central Nervous System Plasticity Across Development and Generations,” Neuroscience & Biobehavioral Reviews, Vol. 23, No. 5, 1999, pp. 673-685.
[27] B. J. Meyerson, H. Augustsson, M. Berg and E. Roman, “The Concentric Square Field: A Multivariate Test Arena for Analysis of Explorative Strategies,” Behavioural Brain Research, Vol. 168, No. 1, 2006, pp. 100-113.
[28] E. Roman and G. Colombo, “Lower Risk Taking and Exploratory Behavior in Alcohol-Preferring sP Rats than in Alcohol Non-Preferring sNP Rats in the Multivariate Concentric Square Field (MCSF) Test,” Behavioural Brain Research, Vol. 205, No. 1, 2009, pp. 249-258.
[29] E. Roman, L. Gustafsson, M. Berg and I. Nylander, “Behavioral Profiles and Stress-Induced Corticosteroid Secretion in Male Wistar Rats Subjected to Short and Prolonged Periods of Maternal Separation,” Hormones and Behavior, Vol. 50, No. 5, 2006, pp. 736-747.
[30] L. Daoura, M. Hjalmarsson, S. Oreland, I. Nylander and E. Roman, “Postpartum Behavioral Profiles in Wistar Rats Following Maternal Separation—Altered Exploration and Risk-Assessment Behavior in MS15 Dams,” Frontiers in Behavioral Neuroscience, Vol. 4, 2010, pp. 1-7.
[31] K. Ploj, E. Roman and I. Nylander, “Long-Term Effects of Short and Long Periods of Maternal Separation on Brain Opioid Peptide Levels in Male Wistar Rats,” Neuropeptides, Vol. 37, No. 3, 2003, pp. 149-156.
[32] B. J. Meyerson, B. Jurek and E. Roman, “A Rank-Order Procedure Applied to an Ethoexperimental Behavior Model—The Multivariate Concentric Square FieldTM (MCSF) Test,” Journal of Behavioral and Brain Science, Vol. 3, No. 4, 2013, pp. 350-361.
[33] L. Daoura, J. Haaker and I. Nylander, “Early Environmental Factors Differentially Affect Voluntary Ethanol Consumption in Adolescent and Adult Male Rats,” Alcoholism: Clinical and Experimental Research, Vol. 35, No. 3, 2010.
[34] J. T. Allin and E. M. Banks, “Functional Aspects of Ultrasound Production by Infant Albino Rats (Rattus norvegicus),” Animal Behaviour, Vol. 20, No. 1, 1972, pp. 175-185.
[35] R. L. Huot, C. O. Ladd and P. M. Plotsky, “Maternal Deprivation,” Elsevier Inc., Amsterdam , 2000.
[36] M. Marmendal, E. Roman, C. J. Eriksson, I. Nylander and C. Fahlke, “Maternal Separation Alters Maternal Care, But Has Minor Effects on Behavior and Brain Opioid Peptides in Adult Offspring,” Developmental Psychobiology, Vol. 45, No. 3, 2004, pp. 140-152.
[37] J. P. Aguggia, M. M. Suarez and M. A. Rivarola, “Early Maternal Separation: Neurobehavioral Consequences in Mother Rats,” Behavioural Brain Research, Vol. 248, 2013, pp. 25-31.
[38] J. Maniam and M. J. Morris, “Long-Term Postpartum Anxiety and Depression-Like Behavior in Mother Rats Subjected to Maternal Separation are Ameliorated by Palatable High Fat Diet,” Behavioural Brain Research, Vol. 208, No. 1, 2010, pp. 72-79.
[39] N. P. Daskalakis, S. E. Claessens, J. J. Laboyrie, L. Enthoven, M. S. Oitzl, D. L. Champagne and E. R. de Kloet, “The Newborn Rat’s Stress System Readily Habituates to Repeated and Prolonged Maternal Separation, While Continuing to Respond to Stressors in Context Dependent Fashion,” Horm Behav, Vol. 60, No. 2, 2011, pp. 165-176.
[40] D. Liu, J. Diorio, B. Tannenbaum, C. Caldji, D. Francis, A. Freedman, S. Sharma, D. Pearson, P. M. Plotsky and M. J. Meaney, “Maternal Care, Hippocampal Glucocorticoid Receptors, and Hypothalamic-Pituitary-Adrenal Responses to Stress,” Science, Vol. 277, No. 5332, 1997, pp. 1659-1662.
[41] S. Macri, G. J. Mason and H. Wurbel, “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, Vol. 20, No. 4, 2004, pp. 1017-1024.
[42] A. Wallen-Mackenzie, K. Nordenankar, K. Fejgin, M. C. Lagerstrom, L. Emilsson, R. Fredriksson, C. Wass, D. Andersson, E. Egecioglu, M. Andersson, J. Strandberg, O. Lindhe, H. B. Schioth, K. Chergui, E. Hanse, B. Langstrom, A. Fredriksson, L. Svensson, E. Roman and K. Kullander, “Restricted Cortical and Amygdaloid Removal of Vesicular Glutamate Transporter 2 in Preadolescent Mice Impacts Dopaminergic Activity and Neuronal Circuitry of Higher Brain Function,” The Journal of Neuroscience, Vol. 29, No. 7, 2009, pp. 2238-2251.
[43] E. Roman, B. J. Meyerson, P. Hyytia and I. Nylander, “The Multivariate Concentric Square Field Test Reveals Different Behavioural Profiles in Male AA and ANA Rats with Regard to Risk Taking and Environmental Reactivity,” Behavioural Brain Research, Vol. 183, No. 2, 2007, pp. 195-205.
[44] W. P. Smotherman, R. W. Bell, J. Starzec, J. Elias and T. A. Zachman, “Maternal Responses to Infant Vocalizations and Olfactory Cues in Rats and Mice,” Behavioral Biology, Vol. 12, No. 1, 1974, pp. 55-66.
[45] F. A. Champagne, D. D. Francis, A. Mar and M. J. Meaney, “Variations in Maternal Care in the rat as a Mediating Influence for the Effects of Environment on Development,” Physiology & Behavior, Vol. 79, No. 3, 2003, pp. 359-371.
[46] D. C. Blanchard and R. J. Blanchard, “Ethoexperimental Approaches to the Biology of Emotion,” Annual Review of Psychology, Vol. 39, 1988, pp. 43-68.
[47] A. H. Macbeth, C. Gautreaux and V. N. Luine, “Pregnant Rats Show Enhanced Spatial Memory, Decreased Anxiety, and Altered Levels of Monoaminergic Neurotransmitters,” Brain Research, Vol. 1241, 2008, pp. 136-147.
[48] I. D. Neumann, “Alterations in Behavioral and Neuroendocrine Stress Coping Strategies in Pregnant, Parturient and Lactating Rats,” Progress in Brain Research, Vol. 133, 2001, pp. 143-152.
[49] S. Palm, E. Roman and I. Nylander, “Differences in Voluntary Ethanol Consumption in Wistar Rats from Five Different Suppliers,” Alcohol, Vol. 45, No. 6, 2011, pp. 607-614.

comments powered by Disqus

Copyright © 2018 by authors and Scientific Research Publishing Inc.

Creative Commons License

This work and the related PDF file are licensed under a Creative Commons Attribution 4.0 International License.