Early maternal separation impacts cognitive flexibility at the age of first independence in mice

Developmental Cognitive Neuroscience

Volumn 18, Issue , 2016, Pages 49-56

  Thomas, A Wren ^a   Caporale, Natalia ^b   Wu, Claudia ^c   Wilbrecht, Linda ^b  

^a Helen Wills Neuroscience Graduate Program   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Development; Neglect; Perseveration; Prefrontal; Reversal; Stress

Indexed keywords

ALCOHOL;

ADULT; ALCOHOL ABUSE; ALCOHOL CONSUMPTION; ANIMAL MODEL; ARTICLE; BRAIN MATURATION; COGNITION; CONTROLLED STUDY; EARLY LIFE STRESS; FEMALE; INDEPENDENCE; JUVENILE ANIMAL; LEARNING; MALE; MATERNAL DEPRIVATION; MOUSE; NONHUMAN; OLFACTORY DISCRIMINATION; PRIORITY JOURNAL; SUBSTANCE ABUSE; TASK PERFORMANCE; WEANING; AGING; ANIMAL; C57BL MOUSE; DECISION MAKING; DRINKING BEHAVIOR; MENTAL STRESS; PHYSIOLOGY; PSYCHOLOGICAL MODEL; PSYCHOLOGY;

AGING; ALCOHOL DRINKING; ANIMALS; CHOICE BEHAVIOR; COGNITION; FEMALE; MALE; MATERNAL DEPRIVATION; MICE; MICE, INBRED C57BL; MODELS, ANIMAL; MODELS, PSYCHOLOGICAL; REVERSAL LEARNING; STRESS, PSYCHOLOGICAL; WEANING;

EID: 84961774369     PISSN: 18789293     EISSN: 18789307     Source Type: Journal    
DOI: 10.1016/j.dcn.2015.09.005     Document Type: Article

References (68)

1. B. Aisa, R. Tordera, B. Lasheras, J. Del Río, and M.J. Ramírez Cognitive impairment associated to HPA axis hyperactivity after maternal separation in rats Psychoneuroendocrinology 32 2007 256 266
2. K. Anier, K. Malinovskaja, K. Pruus, A. Aonurm-Helm, A. Zharkovsky, and A. Kalda Maternal separation is associated with DNA methylation and behavioural changes in adult rats. European Neuropsychopharmacology Eur. Neuropsychopharmacol. 24 2014 459 468
3. A. Baudin, K. Blot, C. Verney, L. Estevez, J. Santamaria, P. Gressens, and L. Naudon Maternal deprivation induces deficits in temporal memory and cognitive flexibility and exaggerates synaptic plasticity in the rat medial prefrontal cortex Neurobiol. Learn. Mem. 98 2012 207 214
4. J.M. Birrell, and V.J. Brown Medial frontal cortex mediates perceptual attentional set shifting in the rat J. Neurosci. 20 2000 4320 4324
5. G.B. Bissonette, G.J. Martins, T.M. Franz, E.S. Harper, G. Schoenbaum, and E.M. Powell Double dissociation of the effects of medial and orbital prefrontal cortical lesions on attentional and affective shifts in mice J. Neurosci. 28 2008 11124 11130
6. J. Bock, M. Gruss, S. Becker, and K. Braun Experience-induced changes of dendritic spine densities in the prefrontal and sensory cortex: Correlation with developmental time windows Cerebral Cortex 15 2005 802 808
7. J. Bowlby Attachment and loss: retrospect and prospect Am. J. Orthopsychiatry 52 1982 664 678
8. H.C. Brenhouse, and S.L. Andersen Nonsteroidal anti-inflammatory treatment prevents delayed effects of early life stress in rats Biol. Psychiatry 70 2011 434 440
9. H. Brenhouse, J. Lukkes, and S. Andersen Early life adversity alters the developmental profiles of addiction-related prefrontal cortex circuitry Brain Sci. 3 2013 143 158
10. B.L. Callaghan, and R. Richardson Maternal separation results in early emergence of adult-like fear and extinction learning in infant rats Behav. Neurosci. 125 2011 20 28
11. A. Chocyk, D. Dudys, A. Przyborowska, M. Maćkowiak, and K. Wȩdzony Impact of maternal separation on neural cell adhesion molecules expression in dopaminergic brain regions of juvenile, adolescent and adult rats Pharmacol. Rep 62 2010 1218 1224
12. F.C. Cruz, I.M. Quadros, C. Da, and K.A. Miczek Maternal separation stress in male mice: Long-term increases in alcohol intake Psychopharmacology 201 2008 459 468
13. R. Dalle Molle, a.K. Portella, M.Z. Goldani, F.P. Kapczinski, S. Leistner-Segal, S. Leistner-Segala, and P.P. Silveira Associations between parenting behavior and anxiety in a rodent model and a clinical sample: relationship to peripheral BDNF levels Transl. Psychiatry 2 2012 e195
14. M. Del Giudice, B.J. Ellis, and E.a. Shirtcliff The adaptive calibration model of stress responsivity Neurosci. Biobehav. Rev. 35 2011 1562 1592
15. S.R. Dube, R.F. Anda, V.J. Felitti, D.P. Chapman, D.F. Williamson, and W.H. Giles Childhood abuse, household dysfunction, and the risk of attempted suicide throughout the life span: findings from the Adverse Childhood Experiences Study JAMA 286 2001 3089 3096
16. M. Enoch The role of early life stress as a predictor for alcohol and drug dependence Psychopharmacology 214 2011 17 31
17. K. Fabricius, G. Wörtwein, and B. Pakkenberg The impact of maternal separation on adult mouse behaviour and on the total neuron number in the mouse hippocampus Brain Struct. Funct. 212 2008 403 416
18. V.J. Felitti, R.F. Anda, D. Nordenberg, D.F. Williamson, A.M. Spitz, V. Edwards, and J.S. Marks Relationship of childhood abuse and household dysfunction to many of the leading causes of death in adults Am. J. Prev. Med. 14 1998 245 258
19. D. Fishbein, T. Warner, C. Krebs, N. Trevarthen, B. Flannery, and J. Hammond Differential relationships between personal and community stressors and children's neurocognitive functioning Child Maltreatment 14 2009 299 315
20. D.D. Francis, J. Diorio, P.M. Plotsky, and M.J. Meaney Environmental enrichment reverses the effects of maternal separation on stress reactivity J. Neurosci. 22 2002 7840 7843
21. J.P. Garner, C.M. Thogerson, H. Würbel, J.D. Murray, and J.A. Mench Animal neuropsychology: validation of the Intra-Dimensional Extra-Dimensional set shifting task for mice Behav. Brain Res. 173 2006 53 61
22. D.G. Gee, L.J. Gabard-Durnam, J. Flannery, B. Goff, K.L. Humphreys, E.H. Telzer, and et al. Early developmental emergence of human amygdala-prefrontal connectivity after maternal deprivation Proc. Natl. Acad. Sci. USA 110 2013 15638 15643
23. R. Gilbert, C.S. Widom, K. Browne, D. Fergusson, E. Webb, and S. Janson Burden and consequences of child maltreatment in high-income countries Lancet 373 2009 68 81
24. E.E. Gilles, L. Schultz, and T.Z. Baram Abnormal corticosterone regulation in an immature rat model of continuous chronic stress Pediatr. Neurol. 15 1996 114 119
25. R.Z. Goldstein, and N.D. Volkow Dysfunction of the prefrontal cortex in addiction: neuroimaging findings and clinical implications Nat. Rev. Neurosci. 12 2011 652 669
26. J.G. Green, K.a. Mclaughlin, P.a Berglund, M.J. Gruber, N.a Sampson, A.M. Zaslavsky, and R.C. Kessler Childhood adversities and adult psychiatric disorders in the national comorbidity survey replication I Arch. Gen. Psychiatry 67 2010 113 123
27. C. Heim, and C.B. Nemeroff The role of childhood trauma in the neurobiology of mood and anxiety disorders: preclinical and clinical studies Biol. Psychiatry 49 2001 1023 1039
28. C. Helmeke, W. Ovtscharoff, G. Poeggel, and K. Braun Imbalance of immunohistochemically characterized interneuron populations in the adolescent and adult rodent medial prefrontal cortex after repeated exposure to neonatal separation stress Neuroscience 152 2008 18 28
29. C.E. Hostinar, and M.R. Gunnar The developmental effects of early life stress: an overview of current theoretical frameworks Curr. Dir. Psychol. Sci. 22 2013 400 406
30. R.L. Huot, P.M. Plotsky, R.H. Lenox, and R.K. McNamara Neonatal maternal separation reduces hippocampal mossy fiber density in adult Long Evans rats Brain Res. 950 2002 52 63
31. R.L. Huot, K.V. Thrivikraman, M.J. Meaney, and P.M. Plotsky Development of adult ethanol preference and anxiety as a consequence of neonatal maternal separation in Long Evans rats and reversal with antidepressant treatment Psychopharmacology 158 2001 366 373
32. A.S. Ivy, K.L. Brunson, C. Sandman, and T.Z. Baram Dysfunctional nurturing behavior in rat dams with limited access to nesting material: A clinically relevant model for early-life stress Neuroscience 154 2008 1132 1142
33. S.R. Jaffee, T.E. Moffitt, A. Caspi, E. Fombonne, R. Poulton, and J. Martin Differences in early childhood risk factors for juvenile-onset and adult-onset depression Arch. Gen. Psychiatry 59 2002 215 222
34. C. Johnson, and L. Wilbrecht Juvenile mice show greater flexibility in multiple choice reversal learning than adults Dev. Cogn. Neurosci. 1 2011 540 551
35. J. Kim, and M.E. Ragozzino The involvement of the orbitofrontal cortex in learning under changing task contingencies Neurobiol. Learn. Mem. 83 2005 125 133
36. C.O. Ladd, R.L. Huot, K.V. Thrivikraman, C.B. Nemeroff, and P.M. Plotsky Long-term adaptations in glucocorticoid receptor and mineralocorticoid receptor mRNA and negative feedback on the hypothalamo-pituitary-adrenal axis following neonatal maternal separation Biol. Psychiatry 55 2004 367 375
37. S. Levine The effects of infantile experience on adult behavior A.J. Bachrach, Experimental foundations of clinical psychology 1962 Basic Books New York 118 169
38. M. Lippmann, A. Bress, C.B. Nemeroff, P.M. Plotsky, and L.M. Monteggia Long-term behavioural and molecular alterations associated with maternal separation in rats Eur. J. Neurosci. 25 2007 3091 3098
39. C. Liston, M.M. Miller, D.S. Goldwater, J.J. Radley, A.B. Rocher, P.R. Hof, and B.S. McEwen Stress-induced alterations in prefrontal cortical dendritic morphology predict selective impairments in perceptual attentional set-shifting J. Neurosci. 26 2006 7840 7844
40. D. Liu, J. Diorio, B. Tannenbaum, C. Caldji, D. Francis, Freedman, and M.J. aMeaney Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress Science (New York, N.Y.) 277 1997 1659 1662
41. V. Lovic, and A.S. Fleming 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. 148 2004 209 219
42. H.L. Macmillan, J.E. Fleming, D.L. Streiner, E. Lin, M.H. Boyle, E. Jamieson, and W.R. Beardslee Childhood abuse and lifetime psychopathology in a community sample Am. J. Psychiatry 158 2001 1878 1883
43. S. Macri, F. Chiarotti, and H. Würbel Maternal separation and maternal care act independently on the development of HPA responses in male rats Behav. Brain Res. 191 2008 227 234
44. K. McAlonan, and V.J. Brown Orbital prefrontal cortex mediates reversal learning and not attentional set shifting in the rat Behav. Brain Res. 146 2003 97 103
45. B.S. McEwen, and E. Stellar Stress and the individual Mechanisms leading to disease Arch. Intern. Med. 153 1993 2093 2101
46. M. Mehta, and C. Schmauss Strain-specific cognitive deficits in adult mice exposed to early life stress Behav. Neurosci. 125 2011 29 36
47. M.C. Moffett, A. Vicentic, M. Kozel, P. Plotsky, D.D. Francis, and M.J. Kuhar Maternal separation alters drug intake patterns in adulthood in rats Biochem. Pharmacol. 73 2007 321 330
48. E. Monroy, E. Hernández-Torres, and G. Flores Maternal separation disrupts dendritic morphology of neurons in prefrontal cortex, hippocampus, and nucleus accumbens in male rat offspring J. Chem. Neuroanat. 40 2010 93 101
49. S. Moriceau, K. Shionoya, K. Jakubs, and R.M. Sullivan Early-Life stress disrupts attachment learning: the role of amygdala corticosterone, locus ceruleus corticotropin releasing hormone, and olfactory bulb norepinephrine J. Neurosci. 29 2009 15745 15755
50. A. Muhammad, and B. Kolb Maternal separation altered behavior and neuronal spine density without influencing amphetamine sensitization Behav. Brain Res. 223 2011 7 16
51. R. Pascual, and S.P. Zamora-León Effects of neonatal maternal deprivation and postweaning environmental complexity on dendritic morphology of prefrontal pyramidal neurons in the rat Acta Neurobiol. Exp. 67 2007 471 479
52. K. Ploj, E. Roman, and I. Nylander Long-term effects of maternal separation on ethanol intake and brain opioid and dopamine receptors in male wistar rats Neuroscience 121 2003 787 799
53. P.M. Plotsky, and M.J. Meaney Early, postnatal experience alters hypothalamic corticotropin-releasing factor (CRF) mRNA, median eminence CRF content and stress-induced release in adult rats Mol. Brain Res. 18 1993 195 200
54. C.R. Pryce, and J. Feldon Long-term neurobehavioural impact of the postnatal environment in rats: manipulations, effects and mediating mechanisms Neurosci. Biobehav. Rev. 27 2003 57 71
55. J.J. Radley, A.B. Rocher, A. Rodriguez, B. Douglas, M. Dammann, B.S. Mcewen, and P.R. Hof Repeated stress alters dendritic spine morphology J. Comp. Neurol. 507 2009 1141 1150
56. J.J. Radley, H.M. Sisti, J. Hao, a. Rocher, B. McCall, T. Hof, and P.R.J.H. Morrison Chronic behavioral stress induces apical dendritic reorganization in pyramidal neurons of the medial prefrontal cortex Neuroscience 125 2004 1 6
57. M.E. Ragozzino, J. Kim, D. Hassert, N. Minniti, and C. Kiang The contribution of the rat prelimbic-infralimbic areas to different forms of task switching Behav. Neurosci. 117 2003 1054 1065
58. M.E. Ragozzino, and S. Rozman The effect of rat anterior cingulate inactivation on cognitive flexibility Behav. Neurosci. 121 2007 698 706
59. J.S. Rhodes, K. Best, J.K. Belknap, D. Finn, and a.J.C. Crabbe Evaluation of a simple model of ethanol drinking to intoxication in C57BL/6J mice Physiol. Behav. 84 2005 53 63
60. M.M. Sánchez, C.O. Ladd, and P.M. Plotsky Early adverse experience as a developmental risk factor for later psychopathology: evidence from rodent and primate models Dev. Psychopathol. 13 2001 419 449
61. N.W. Simon, and B. Moghaddam Neural processing of reward in adolescent rodents Dev. Cogn. Neurosci. 11 2015 145 154
62. L.P. Spear The adolescent brain and age-related behavioral manifestations Neurosci. Biobehav. Rev. 24 2000 417 463
63. T.E. Thiele, and M. Navarro "Drinking in the dark" (DID) procedures: A model of binge-like ethanol drinking in non-dependent mice Alcohol 48 2014 235 241
64. S. Uchida, K. Hara, A. Kobayashi, H. Funato, T. Hobara, K. Otsuki, and Y. Watanabe Early life stress enhances behavioral vulnerability to stress through the activation of REST4-mediated gene transcription in the medial prefrontal cortex of rodents J. Neurosci. 30 2010 15007 15018
65. M.E. Van Der Schaaf, E. Warmerdam, E. Crone, and a.R. Cools Distinct linear and non-linear trajectories of reward and punishment reversal learning during development: Relevance for dopamine's role in adolescent decision making Dev. Cogn. Neurosci. 1 2011 578 590
66. L. Wang, J. Jiao, and S.C. Dulawa Infant maternal separation impairs adult cognitive performance in BALB/cJ mice Psychopharmacology 216 2011 207 218
67. Q. Wang, M. Li, W. Du, F. Shao, and W. Wang The different effects of maternal separation on spatial learning and reversal learning in rats Behav. Brain Res. 280 2015 16 23
68. X.-D. Yang, X.-M. Liao, A. Uribe-Mariño, R. Liu, X.-M. Xie, J. Jia, and T.-M. Si Stress during a Critical Postnatal Period Induces Region-Specific Structural Abnormalities and Dysfunction of the Prefrontal Cortex via CRF1 Neuropsychopharmacology 2015 1203 1215