Propagation of maternal behavior across generations is associated with changes in non-maternal cognitive and behavioral processes

Behavioural Processes

Volumn 117, Issue , 2015, Pages 42-47

  Lovic, Vedran ^a   Fleming, Alison S ^b  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

Attention; Deprivation; Impulsivity; Maternal; Rat; Rearing; Separation

Indexed keywords

ASSESSMENT METHOD; BEHAVIORAL ECOLOGY; COGNITION; ENDOCRINE DISRUPTOR; GENERATION TIME; MATERNAL EFFECT; RODENT; SOCIAL BEHAVIOR; WEANING;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ARTIFICIAL REARING; BEHAVIOR CHANGE; BIOMANIPULATION; CLINICAL ASSESSMENT; COGNITION; CONTROLLED STUDY; DOPAMINE BRAIN LEVEL; FEMALE; GROOMING; HUMAN; IMPULSIVENESS; LICKING; MATERNAL BEHAVIOR; MATERNAL CARE; MATERNAL DEPRIVATION; MOTHER CHILD RELATION; MOTHER REARING; NONHUMAN; PARENTAL BEHAVIOR; PERSONAL EXPERIENCE; PROGENY; RAT; REARING; SELECTIVE ATTENTION; SIBLING; SOCIAL ISOLATION; TIME MANAGEMENT; WEANING; ANIMAL; ANIMAL BEHAVIOR; EXECUTIVE FUNCTION; MALE; MOTIVATION; NEWBORN; PHYSIOLOGY; PSYCHOLOGY; SPRAGUE DAWLEY RAT;

RATTUS;

ANIMALS; ANIMALS, NEWBORN; BEHAVIOR, ANIMAL; COGNITION; EXECUTIVE FUNCTION; FEMALE; MALE; MATERNAL BEHAVIOR; MATERNAL DEPRIVATION; MOTIVATION; RATS; RATS, SPRAGUE-DAWLEY; SOCIAL ISOLATION;

EID: 84938749297     PISSN: 03766357     EISSN: 18728308     Source Type: Journal    
DOI: 10.1016/j.beproc.2015.02.016     Document Type: Article

References (60)

1. Afonso V.M., Sison M., Lovic V., Fleming A.S. Medial prefrontal cortex lesions in the female rat affect sexual and maternal behavior and their sequential organization. Behav. Neurosci. 2007, 121(3):515-526. 10.1037/0735-7044.121.3.515.
2. Afonso V.M., King S.J., Novakov M., Burton C.L., Fleming A.S. Accumbal dopamine function in postpartum rats that were raised without their mothers. Horm. Behav. 2011, 60:632-643. 10.1016/j.yhbeh.2011.08.016.
3. Alberts J.R. Huddling by rat pups: multisensory control of contact behavior. J. Comp. Physiol. Psychol. 1978, 92:220-230.
4. Arnsten A.F. Fundamentals of attention-deficit/hyperactivity disorder: circuits and pathways. J. Clin. Psychiatry 2006, 67(Suppl. 8):7-12.
5. Atkinson L., Leung E., Goldberg S., Benoit D., Poulton L., Myhal N., Kerr S. Attachment and selective attention: disorganization and emotional Stroop reaction time. Dev. Psychopathol. 2009, 21(1):99-126. 10.1017/s0954579409000078.
6. Bell R.W., Nitschke W., Gorry T.H., Zachman T.A. Infantile stimulation and ultrasonic signaling: a possible mediator of early handling phenomena. Dev. Psychobiol. 1971, 4(2):181-191. 10.1002/dev.420040209.
7. Birrell J.M., Brown V.J. Medial frontal cortex mediates perceptual attentional set shifting in the rat. J. Neurosci. 2000, 20(11):4320-4324.
8. Bos K.J., Fox N.A., Zeanah C.H., Nelson C.A. Effects of early psychosocial deprivation on the development of memory and executive function. Front. Behav. Neurosci. 2009, 3:1-7. 10.3389/neuro.08.016.2009.
9. Bridges R. Neurobiology of the Parental Brain 2008, Academic Press, Amsterdam.
10. Burton C.L., Lovic V., Fleming A.S. Early adversity alters attention and locomotion in adult Sprague-Dawley rats. Behav. Neurosci. 2006, 120:665-675. 10.1037/0735-7044.120.3.665.
11. Chatterjee D., Chatterjee-Chakraborty M., Rees S., Cauchi J., deMedeiros C.B., Fleming A.S. Maternal isolation alters the expression of neural proteins during development: 'Stroking' stimulation reverses these effects. Brain Res. 2007, 1158:11-27. 10.1016/j.brainres.2007.04.069.
12. Chico E., Gonzalez A., Ali N., Steiner M., Fleming A.S. Executive function and mothering: challenges faced by teenage mothers. Dev. Psychobiol. 2014, 10.1002/dev.21185.
13. De Bellis M.D. The psychobiology of neglect. Child Maltreat. 2005, 10(2):150-172. 10.1177/1077559505275116.
14. Fishbein D., Warner T., Krebs C., Trevarthen N., Flannery B., Hammond J. Differential relationships between personal and community stressors and children's neurocognitive functioning. Child Maltreat. 2009, 14(4):299-315. 10.1177/1077559508326355.
15. Fletcher P.J., Tenn C.C., Rizos Z., Lovic V., Kapur S. Sensitization to amphetamine, but not PCP, impairs attentional set shifting: reversal by a D1 receptor agonist injected into the medial prefrontal cortex. Psychopharmacol. (Berl.) 2005, 183(2):190-200. 10.1007/s00213-005-0157-6.
16. Fletcher P., Rizos Z., Noble K., Higgings G.A. Impulsive action induced by amphetamine, cocaine and MK801 is reduced by 5-HT(2C) receptor stimulation and 5-HT(2A) receptor blockade. Neuropharmacology 2011, 61(3):468-477. 10.1016/j.neuropharm.2011.02.0254.
17. Francis D., Diorio J., Liu D., Meaney M.J. Nongenomic transmission across generations of maternal behavior and stress responses in the rat. Science 1999, 286(5442):1155-1158.
18. Geier C.F., Terwilliger R., Teslovich T., Velanova K., Luna B. Immaturities in reward processing and its influence on inhibitory control in adolescence. Cereb. Cortex 2010, 20(7):1613-1629. 10.1093/cercor/bhp225.
19. Gonzalez A., Lovic V., Ward G.R., Wainwright P.E., Fleming A.S. Intergenerational effects of complete maternal deprivation and replacement stimulation on maternal behavior and emotionality in female rats. Dev. Psychobiol. 2001, 38:11-32. 10.1002/1098-2302.
20. Gonzalez A., Jenkins J.M., Steiner M., Fleming A.S. Maternal early life experiences and parenting: the mediating role of cortisol and executive function. J. Am. Acad. Child Adolesc. Psychiatry 2012, 51(7):673-682. 10.1016/j.jaac.2012.04.003.
21. Hall F.S., Wilkinson T.H., Robbins T.W. Maternal deprivation of neonatal rats produces enduring changes in dopamine function. Synapse 1999, 32:37-43.
22. Keverne E.B. Genomic imprinting and the maternal brain. Prog. Brain Res. 2001, 133:279-285.
23. Kinsley C.H., Amori-Meyer E. Why the maternal brain?. J. Neuroendocrin. 2011, 23:974-983.
24. Kreppner J., O'Connor T.G., Rutter M., The English and Romanian Adoptees Study Team Can inattention/overactivity be an institutional deprivation syndrome?. J. Abnormal Child Psychol. 2001, 29(29):513-528. 10.1023/A:1012229209190.
25. Levine S., Chevalier J.A., Korchin S.J. The effects of shock and handling in infancy on later avoidance learning. J. Pers. 1956, 24:475-493.
26. Levine S. Psychosocial factors in growth and development. Society, Stress and Disease 1975, 43-50. Oxford University Press, London. L. Levi (Ed.).
27. Levy F., Melo A.I., Galef G.B.J., Madden M., Fleming A.S. Complete maternal deprivation affects social, but not spatial, learning in adult rats. Dev. Psychobiol. 2003, 43:177-191. 10.1002/dev.10131.
28. Li M., Fleming A.S. The nucleus accumbens shell is critical for normal expression of pup-retrieval in postpartum female rats. Behav. Brain Res. 2003, 145(1-2):99-111.
29. Li M., Fleming A.S. Differential involvement of nucleus accumbens shell and core subregions in maternal memory in postpartum female rats. Behav. Neurosci. 2003, 117(3):426-445.
30. Liu D., Diorio J., Tannenbaum B., Caldji C., Francis D., Freedman A., Meaney M.J. Maternal care, hippocampal glucocorticoid receptors, and hypothalamic - pituitary - adrenal responses to stress. Science 1997, 277:1659-1662. 10.1126/science.277.5332.1659.
31. Lomanowska A.M., Lovic V., Rankine M.J., Mooney S.J., Robinson T.E., Kraemer G.W. Inadequate early social experience increases the incentive salience of reward-related cues in adulthood. Behav. Brain Res. 2011, 220(1):91-99.
32. Lovic V., Gonzalez A., Fleming A.S. Maternally separated rats show deficits in maternal care in adulthood. Dev. Psychobiol. 2001, 39(1):19-33.
33. Lovic V., Fleming A.S. Artificially-reared female rats show reduced prepulse inhibition and deficits in the attentional set shifting task-reversal of effects with maternal-like licking stimulation. Behav. Brain Res. 2004, 148(1-2):209-219.
34. Lovic V., Fleming A.S., Fletcher P.J. Early life tactile stimulation changes adult rat responsiveness to amphetamine. Pharmacol. Biochem. Behav. 2006, 84:497-503. 10.1016/j.pbb.2006.06.013.
35. Lovic V., Keen D., Fletcher P., Fleming A. Early life maternal separation and social isolation produce an increase in impulsive action but not impulsive choice. Behav. Neurosci. 2011, 12:481-491. 10.1037/a0024367.
36. Lovic V., Palombo D.J., Fleming A.S. Impulsive rats are less maternal. Dev. Psychobiol. 2011, 53(1):13-22. 10.1002/dev.20481.
37. Mann P.E., Bridges R. Lactogenic hormone control of maternal behaivor. Prog. Brain Res. 2001, 133:251-262.
38. Mansbach R.S., Geyer M.A., Braff D.L. Dopaminergic stimulation disrupts sensorimotor gating in the rat. Psychopharmacology 1988, 94:507-514.
39. McAnarney E.R. Adolescent brain development: forging new links?. J. Adolesc. Health 2008, 42(4):321-323. 10.1016/j.jadohealth.2007.10.012.
40. Meaney M.J., Diorio J., Francis D., Widdowson J., LaPlante P., Caldji C., Plotsky Early environmental regulation of forebrain glucocorticoid receptor gene expression: Implications for adrenocortical responses to stress. Dev. Neurosci. 1996, 18:49-72. 10.1159/000111396.
41. Meaney M.J., Diorio J., Francis D., Weaver S., Yau J., Chapman K., Seckl J.R. Postnatal handling increases the expression of cAMP-inducible transcription factors in the rat hippocampus: The effects of thyroid hormone and serotonin. J. Neurosci. 2000, 20:3935-3936.
42. Meaney M.J. Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Ann. Rev. Neurosci. 2001, 24:1161-1192.
43. Meaney M.J., Brake W., Gratton A. Environmental regulation of the development of mesolimbic dopamine systems: a neurobiological mechanism for vulnerability to drug abuse?. Psychoneuroendocrinology 2002, 138:40-43. 10.1016/S0306-4530(01).
44. Nolin P., Ethier L. Using neuropsychological profiles to classify neglected children with or without physical abuse. Child Abuse Negl. 2007, 31(6):631-643. 10.1016/j.chiabu.2006.12.009.
45. Novakov M., Fleming A.S. The effects of early rearing environment on the hormonal induction of maternal behavior in virgin rats. Horm. Behav. 2005, 48:528-536. 10.1016/j.yhbeh.2005.04.011.
46. Numan M. Medial preoptic area and maternal behavior in the female rat. J. Comp. Physiol. Psychol. 1974, 87(4):746-759. 10.1037/h0036974.
47. Numan M., Insel T.R. The Neurobiology of Parental Behavior 2003, Springer, New York.
48. Orpen B.G., Fleming A.S. Experience with pups sustains maternal responding in postpartum rats. Physiol. Behav. 1987, 40(1):47-54.
49. Palombo D.J., Nowoslawski M., Fleming A.S. Motherless rats show deficits in maternal behavior towards fostered pups. Dev. Psychobiol. 2010, 52(2):142-148. 10.1002/dev.20422.
50. Parada M., King S., Li M., Fleming A.S. The roles of accumbal dopamine D1 and D2 receptors in maternal memory in rats. Behav. Neurosci. 2008, 122(2):368-376. 10.1037/0735-7044.122.2.368.
51. Pears K., Fisher P.A. Developmental, cognitive, and neuropsychological functioning in preschool-aged foster children: associations with prior maltreatment and placement history. J. Dev. Behav. Pediatr. 2005, 26(2):112-122.
52. Pears K.C., Fisher P.A. Emotion understanding and theory of mind among maltreated children in foster care: evidence of deficits. Dev. Psychopathol. 2005, 17(1):47-65.
53. Pears K.C., Kim H.K., Fisher P.A. Psychosocial and cognitive functioning of children with specific profiles of maltreatment. Child Abuse Negl. 2008, 32(10):958-971. 10.1016/j.chiabu.2007.12.009.
54. Robinson T.E., Berridge K.C. The neural basis of drug craving: an incentive-sensitization theory of addiction. Brain Res. Brain Res. Rev. 1993, 18(3):247-291.
55. Rosenblatt, J.S., Snowdon, C.T., 1996, Parental Care: Evolution, Mechanisms, and AdaptiveSignificance. In, Advances in the Study of Behavior (Vol., 25, pp. iii-xix, 3 -712). San Diego: A P.
56. Rubia K., Hyde Z., Halari R., Giampietro V., Smith A. Effects of age and sex on developmental neural networks of visual-spatial attention allocation. Neuroimage 2010, 51(2):817-827. 10.1016/j.neuroimage.2010.02.058.
57. Steinhauer A., Villani V., Pereira J., Leung E., Atkinson L. Attention allocation and maternal responsivity to infant signals. Poster presented at the American Psychological Association Conference 2009.
58. Stern J.M., Lonstein J.S. Neural mediation of nursing and related maternal behaviors. Prog. Brain Res. 2001, 133:263-278.
59. Sturman D.A., Moghaddam B. The neurobiology of adolescence: changes in brain architecture, functional dynamics, and behavioral tendencies. Neurosci. Biobehav. Rev. 2011, 35(8):1704-1712. 10.1016/j.neubiorev.2011.04.003.
60. Van Leijenhorst L., Gunther Moor B., Op de Macks Z.A., Rombouts S.A., Westenberg P.M., Crone E.A. Adolescent risky decision-making: neurocognitive development of reward and control regions. Neuroimage 2010, 51(1):345-355. 10.1016/j.neuroimage.2010.02.038.