Early experience of a novel-environment in isolation primes a fearful phenotype characterized by persistent amygdala activation

Psychoneuroendocrinology

Volumn 39, Issue 1, 2014, Pages 39-57

  Daskalakis, Nikolaos P ^a,b,c,d   Diamantopoulou, Anastasia ^a,e,f   Claessens, Sanne E F ^a   Remmers, Elisa ^a   Tjälve, Marika ^a   Oitzl, Melly S ^a   Champagne, Danielle L ^a   de Kloet, E Ronald ^a,b  

^a LEIDEN UNIVERSITY   (Netherlands)

^b LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^c MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^d VETERANS AFFAIRS MEDICAL CENTER   (United States)

^e UNIVERSITY OF ATHENS   (Greece)

^f Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

ACTH; Amygdala; C Fos; Corticosterone; Fear conditioning; Maternal separation; Novelty stress; Short term memory; Social play

Indexed keywords

CORTICOSTERONE; CORTICOTROPIN; PROTEIN C FOS;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; BASOLATERAL AMYGDALA; BRAIN FUNCTION; CENTRAL NUCLEUS (AMYGDALA); COGNITION; CONTROLLED STUDY; CORTICOSTERONE RELEASE; CORTICOTROPIN RELEASE; EXPERIMENTAL DESIGN; FEAR; FEMALE; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; MALE; MATERNAL DEPRIVATION; MEDIAL AMYGDALA; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RETROSPLENIAL CORTEX; SHORT TERM MEMORY; SOCIAL INTERACTION; SPATIAL MEMORY; STRESS; ADULT; ADULTHOOD; AMYGDALOID NUCLEUS; ANIMAL TISSUE; EARLY LIFE STRESS; HOME ENVIRONMENT; JUVENILE ANIMAL; PHENOTYPE; PLAY;

ACTH; AMYGDALA; C-FOS; CORTICOSTERONE; FEAR-CONDITIONING; MATERNAL SEPARATION; NOVELTY STRESS; SHORT-TERM MEMORY; SOCIAL PLAY;

AMYGDALA; ANIMALS; ANIMALS, NEWBORN; ENVIRONMENT; EXPLORATORY BEHAVIOR; FEAR; HOUSING, ANIMAL; MATERNAL DEPRIVATION; PLAY AND PLAYTHINGS; PROTO-ONCOGENE PROTEINS C-FOS; RATS; RATS, WISTAR; SOCIAL BEHAVIOR; STRESS, PSYCHOLOGICAL;

EID: 84888044971     PISSN: 03064530     EISSN: 18733360     Source Type: Journal    
DOI: 10.1016/j.psyneuen.2013.09.021     Document Type: Article

References (88)

1. Ahnert L., Gunnar M.R., Lamb M.E., Barthel M. Transition to child care: associations with infant-mother attachment, infant negative emotion, and cortisol elevations. Child Dev. 2004, 75:639-650.
2. Beery A.K., Francis D.D. Adaptive significance of natural variations in maternal care in rats: a translational perspective. Neurosci. Biobehav. Rev. 2011, 35:1552-1561.
3. Bohus B., de Kloet E.R. Adrenal steroids and extinction behavior: antagonism by progesterone, deoxycorticosterone and dexamethasone of a specific effect of corticosterone. Life Sci. 1981, 28:433-440.
4. Brinks V., de Kloet E.R., Oitzl M.S. Strain specific fear behaviour and glucocorticoid response to aversive events: modelling PTSD in mice. Prog. Brain Res. 2008, 167:257-261.
5. Cai W.H., Blundell J., Han J., Greene R.W., Powell C.M. Postreactivation glucocorticoids impair recall of established fear memory. J. Neurosci. 2006, 26:9560-9566.
6. Cavigelli S.A., Ragan C.M., Barrett C.E., Michael K.C. Within-litter variance in rat maternal behaviour. Behav. Process. 2010, 84:696-704.
7. Champagne D.L., Bagot R.C., van Hasselt F., Ramakers G., Meaney M.J., de Kloet E.R., Joels M., Krugers H. Maternal care and hippocampal plasticity: evidence for experience-dependent structural plasticity, altered synaptic functioning, and differential responsiveness to glucocorticoids and stress. J. Neurosci. 2008, 28:6037-6045.
8. Champagne F.A., Francis D.D., Mar A., Meaney M.J. Variations in maternal care in the rat as a mediating influence for the effects of environment on development. Physiol. Behav. 2003, 79:359-371.
9. Claessens S.E., Daskalakis N.P., Oitzl M.S., de Kloet E.R. Early handling modulates outcome of neonatal dexamethasone exposure. Horm. Behav. 2012, 62:433-441.
10. Claessens S.E., Daskalakis N.P., van der Veen R., Oitzl M.S., de Kloet E.R., Champagne D.L. Development of individual differences in stress responsiveness: an overview of factors mediating the outcome of early life experiences. Psychopharmacology (Berl.) 2011, 214:141-154.
11. D'Amato F.R., Cabib S., Puglisi-Allegra S., Patacchioli F.R., Cigliana G., Maccari S., Angelucci L. Effects of acute and repeated exposure to stress on the hypothalamo-pituitary-adrenocortical activity in mice during postnatal development. Horm. Behav. 1992, 26:474-485.
12. Daskalakis N.P., Claessens S.E., Laboyrie J.J., Enthoven L., Oitzl M.S., Champagne D.L., de Kloet E.R. 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. 2011, 60:165-176.
13. Daskalakis N.P., Kaperoni M., Koros C., de Kloet E.R., Kitraki E. Environmental and tactile stimulation modulates the neonatal handling effect on adult rat spatial memory. Int. J. Dev. Neurosci. 2009, 27:747-755.
14. Daskalakis N.P., Oitzl M.S., Schachinger H., Champagne D.L., de Kloet E.R. Testing the cumulative stress and mismatch hypotheses of psychopathology in a rat model of early-life adversity. Physiol. Behav. 2012, 106:707-721.
15. Daskalakis N.P., Bagot R.C., Parker K.J., Vinkers C.H., de Kloet E.R. The three-hit concept of vulnerability and resilience: Toward understanding adaptation to early-life adversity outcome. Psychoneuroendocrinology 2013, 38:1858-1873.
16. de Kloet E.R., Joels M., Holsboer F. Stress and the brain: from adaptation to disease. Nat. Rev. Neurosci. 2005, 6:463-475.
17. Deacon R.M. Burrowing in rodents: a sensitive method for detecting behavioral dysfunction. Nat. Protoc. 2006, 1:118-121.
18. Deacon R.M., Rawlins J.N. T-maze alternation in the rodent. Nat. Protoc. 2006, 1:7-12.
19. Diamantopoulou A., Stamatakis A., Panagiotaropoulos T., Stylianopoulou F. Reward or its denial during the neonatal period affects adult spatial memory and hippocampal phosphorylated cAMP response element-binding protein levels of both the neonatal and adult rat. Neuroscience 2011, 181:89-99.
20. Edelmann M.N., Demers C.H., Auger A.P. Maternal touch moderates sex differences in juvenile social play behavior. PLoS ONE 2013, 8:e57396.
21. Ellenbroek B.A., Cools A.R. The long-term effects of maternal deprivation depend on the genetic background. Neuropsychopharmacology 2000, 23:99-106.
22. Ellenbroek B.A., van den Kroonenberg P.T., Cools A.R. The effects of an early stressful life event on sensorimotor gating in adult rats. Schizophr. Res. 1998, 30:251-260.
23. Enthoven L., Oitzl M.S., Koning N., van der Mark M., de Kloet E.R. Hypothalamic-pituitary-adrenal axis activity of newborn mice rapidly desensitizes to repeated maternal absence but becomes highly responsive to novelty. Endocrinology 2008, 149:6366-6377.
24. Feinberg M.E., Neiderhiser J.M., Simmens S., Reiss D., Hetherington E.M. Sibling comparison of differential parental treatment in adolescence: gender, self-esteem, and emotionality as mediators of the parenting-adjustment association. Child Dev. 2000, 71:1611-1628.
25. Fenoglio K.A., Chen Y., Baram T.Z. Neuroplasticity of the hypothalamic-pituitary-adrenal axis early in life requires recurrent recruitment of stress-regulating brain regions. J. Neurosci. 2006, 26:2434-2442.
26. Fluttert M., Dalm S., Oitzl M.S. A refined method for sequential blood sampling by tail incision in rats. Lab. Anim. 2000, 34:372-378.
27. Gozzi A., Jain A., Giovannelli A., Bertollini C., Crestan V., Schwarz A.J., Tsetsenis T., Ragozzino D., Gross C.T., Bifone A. A neural switch for active and passive fear. Neuron 2010, 67:656-666.
28. Harrison F.E., Hosseini A.H., McDonald M.P. Endogenous anxiety and stress responses in water maze and Barnes maze spatial memory tasks. Behav. Brain Res. 2009, 198:247-251.
29. Huot R.L., Plotsky P.M., Lenox R.H., McNamara R.K. Neonatal maternal separation reduces hippocampal mossy fiber density in adult Long Evans rats. Brain Res. 2002, 950:52-63.
30. Karssen A.M., Meijer O.C., Berry A., Sanjuan Pinol R., de Kloet E.R. Low doses of dexamethasone can produce a hypocorticosteroid state in the brain. Endocrinology 2005, 146:5587-5595.
31. Knuth E.D., Etgen A.M. Corticosterone secretion induced by chronic isolation in neonatal rats is sexually dimorphic and accompanied by elevated ACTH. Horm. Behav. 2005, 47:65-75.
32. Levine S. Infantile experience and resistance to physiological stress. Science 1957, 126:405.
33. Levine S. Developmental determinants of sensitivity and resistance to stress. Psychoneuroendocrinology 2005, 30:939-946.
34. Levine S., Huchton D.M., Wiener S.G., Rosenfeld P. Time course of the effect of maternal deprivation on the hypothalamic-pituitary-adrenal axis in the infant rat. Dev. Psychobiol. 1991, 24:547-558.
35. Liu D., Diorio J., Day J.C., Francis D.D., Meaney M.J. Maternal care, hippocampal synaptogenesis and cognitive development in rats. Nat. Neurosci. 2000, 3:799-806.
36. Liu D., Diorio J., Tannenbaum B., Caldji C., Francis D., Freedman A., Sharma S., Pearson D., Plotsky P.M., Meaney M.J. Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress. Science 1997, 277:1659-1662.
37. Llorente R., Miguel-Blanco C., Aisa B., Lachize S., Borcel E., Meijer O.C., Ramirez M.J., De Kloet E.R., Viveros M.P. Long term sex-dependent psychoneuroendocrine effects of maternal deprivation and juvenile unpredictable stress in rats. J. Neuroendocrinol. 2011, 23:329-344.
38. Lukas M., Bredewold R., Landgraf R., Neumann I.D., Veenema A.H. Early life stress impairs social recognition due to a blunted response of vasopressin release within the septum of adult male rats. Psychoneuroendocrinology 2011, 36:843-853.
39. Lukas M., Bredewold R., Neumann I.D., Veenema A.H. Maternal separation interferes with developmental changes in brain vasopressin and oxytocin receptor binding in male rats. Neuropharmacology 2010, 58:78-87.
40. Macri S., Mason G.J., Wurbel H. Dissociation in the effects of neonatal maternal separations on maternal care and the offspring's HPA and fear responses in rats. Eur. J. Neurosci. 2004, 20:1017-1024.
41. Macri S., Wurbel H. Developmental plasticity of HPA and fear responses in rats: a critical review of the maternal mediation hypothesis. Horm. Behav. 2006, 50:667-680.
42. McClelland S., Korosi A., Cope J., Ivy A., Baram T.Z. Emerging roles of epigenetic mechanisms in the enduring effects of early-life stress and experience on learning and memory. Neurobiol. Learn. Mem. 2011, 96:79-88.
43. McCormick C.M., Kehoe P., Kovacs S. Corticosterone release in response to repeated, short episodes of neonatal isolation: evidence of sensitization. Int. J. Dev. Neurosci. 1998, 16:175-185.
44. Meaney M.J. Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Annu. Rev. Neurosci. 2001, 24:1161-1192.
45. Meaney M.J., Aitken D.H., van Berkel C., Bhatnagar S., Sapolsky R.M. Effect of neonatal handling on age-related impairments associated with the hippocampus. Science 1988, 239:766-768.
46. Moriceau S., Raineki C., Holman J.D., Holman J.G., Sullivan R.M. Enduring neurobehavioral effects of early life trauma mediated through learning and corticosterone suppression. Front. Behav. Neurosci. 2009, 3:22.
47. Moriceau S., Sullivan R.M. Maternal presence serves as a switch between learning fear and attraction in infancy. Nat. Neurosci. 2006, 9:1004-1006.
48. Moriceau S., Wilson D.A., Levine S., Sullivan R.M. Dual circuitry for odor-shock conditioning during infancy: corticosterone switches between fear and attraction via amygdala. J. Neurosci. 2006, 26:6737-6748.
49. Murgatroyd C., Patchev A.V., Wu Y., Micale V., Bockmuhl Y., Fischer D., Holsboer F., Wotjak C.T., Almeida O.F., Spengler D. Dynamic DNA methylation programs persistent adverse effects of early-life stress. Nat. Neurosci. 2009, 12:1559-1566.
50. Niesink R.J., Van Ree J.M. Involvement of opioid and dopaminergic systems in isolation-induced pinning and social grooming of young rats. Neuropharmacology 1989, 28:411-418.
51. Oitzl M.S., Champagne D.L., van der Veen R., de Kloet E.R. Brain development under stress: hypotheses of glucocorticoid actions revisited. Neurosci. Biobehav. Rev. 2010, 34:853-866.
52. Oomen C.A., Soeters H., Audureau N., Vermunt L., van Hasselt F.N., Manders E.M., Joels M., Lucassen P.J., Krugers H. Severe early life stress hampers spatial learning and neurogenesis, but improves hippocampal synaptic plasticity and emotional learning under high-stress conditions in adulthood. J. Neurosci. 2010, 30:6635-6645.
53. Ouellet-Morin I., Boivin M., Dionne G., Lupien S.J., Arseneault L., Barr R.G., Perusse D., Tremblay R.E. Variations in heritability of cortisol reactivity to stress as a function of early familial adversity among 19-month-old twins. Arch. Gen. Psychiatry 2008, 65:211-218.
54. Parent C.I., Meaney M.J. The influence of natural variations in maternal care on play fighting in the rat. Dev. Psychobiol. 2008, 50:767-776.
55. Paxinos G., Watson C. The Rat Brain in Stereotaxic Coordinates 2007, Elsevier Academic Press, San Diego. 6th edition.
56. Pellis S.M., Pellis V.C. Differential rates of attack, defense, and counterattack during the developmental decrease in play fighting by male and female rats. Dev. Psychobiol. 1990, 23:215-231.
57. Plotsky P.M., Thrivikraman K.V., Nemeroff C.B., Caldji C., Sharma S., Meaney M.J. Long-term consequences of neonatal rearing on central corticotropin-releasing factor systems in adult male rat offspring. Neuropsychopharmacology 2005, 30:2192-2204.
58. Pryce C.R., Bettschen D., Feldon J. Comparison of the effects of early handling and early deprivation on maternal care in the rat. Dev. Psychobiol. 2001, 38:239-251.
59. Raineki C., Moriceau S., Sullivan R.M. Developing a neurobehavioral animal model of infant attachment to an abusive caregiver. Biol. Psychiatry 2010, 67:1137-1145.
60. Roceri M., Cirulli F., Pessina C., Peretto P., Racagni G., Riva M.A. Postnatal repeated maternal deprivation produces age-dependent changes of brain-derived neurotrophic factor expression in selected rat brain regions. Biol. Psychiatry 2004, 55:708-714.
61. Roozendaal B., McEwen B.S., Chattarji S. Stress, memory and the amygdala. Nat. Rev. Neurosci. 2009, 10:423-433.
62. Rosenfeld P., Suchecki D., Levine S. Multifactorial regulation of the hypothalamic-pituitary-adrenal axis during development. Neurosci. Biobehav. Rev. 1992, 16:553-568.
63. Rosenfeld P., Wetmore J.B., Levine S. Effects of repeated maternal separations on the adrenocortical response to stress of preweanling rats. Physiol. Behav. 1992, 52:787-791.
64. Rots N.Y., Cools A.R., Oitzl M.S., de Jong J., Sutanto W., de Kloet E.R. Divergent prolactin and pituitary-adrenal activity in rats selectively bred for different dopamine responsiveness. Endocrinology 1996, 137:1678-1686.
65. Sandi C. The role and mechanisms of action of glucocorticoid involvement in memory storage. Neural Plast. 1998, 6:41-52.
66. Sapolsky R.M. Glucocorticoids and hippocampal atrophy in neuropsychiatric disorders. Arch. Gen. Psychiatry 2000, 57:925-935.
67. Sapolsky R.M., Meaney M.J. Maturation of the adrenocortical stress response: neuroendocrine control mechanisms and the stress hyporesponsive period. Brain Res. 1986, 396:64-76.
68. Schmidt M.V., Enthoven L., van der Mark M., Levine S., de Kloet E.R., Oitzl M.S. The postnatal development of the hypothalamic-pituitary-adrenal axis in the mouse. Int J Dev Neurosci. 2003, 21(May (3)):125-132.
69. Schmidt M., Enthoven L., van Woezik J.H., Levine S., de Kloet E.R., Oitzl M.S. The dynamics of the hypothalamic-pituitary-adrenal axis during maternal deprivation. J. Neuroendocrinol. 2004, 16:52-57.
70. Sevelinges Y., Moriceau S., Holman P., Miner C., Muzny K., Gervais R., Mouly A.M., Sullivan R.M. Enduring effects of infant memories: infant odor-shock conditioning attenuates amygdala activity and adult fear conditioning. Biol. Psychiatry 2007, 62:1070-1079.
71. Sevelinges Y., Mouly A.M., Raineki C., Moriceau S., Forest C., Sullivan R.M. Adult depression-like behavior, amygdala and olfactory cortex functions are restored by odor previously paired with shock during infant's sensitive period attachment learning. Dev. Cogn. Neurosci. 2011, 1:77-87.
72. Sevelinges Y., Sullivan R.M., Messaoudi B., Mouly A.M. Neonatal odor-shock conditioning alters the neural network involved in odor fear learning at adulthood. Learn. Mem. 2008, 15:649-656.
73. Sullivan R.M., Landers M., Yeaman B., Wilson D.A. Good memories of bad events in infancy. Nature 2000, 407:38-39.
74. Sullivan R.M., Stackenwalt G., Nasr F., Lemon C., Wilson D.A. Association of an odor with activation of olfactory bulb noradrenergic beta-receptors or locus coeruleus stimulation is sufficient to produce learned approach responses to that odor in neonatal rats. Behav. Neurosci. 2000, 114:957-962.
75. Tang A.C. Neonatal exposure to novel environment enhances hippocampal-dependent memory function during infancy and adulthood. Learn. Mem. 2001, 8:257-264.
76. Tang A.C., Akers K.G., Reeb B.C., Romeo R.D., McEwen B.S. Programming social, cognitive, and neuroendocrine development by early exposure to novelty. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:15716-15721.
77. Tang A.C., Reeb B.C., Romeo R.D., McEwen B.S. Modification of social memory, hypothalamic-pituitary-adrenal axis, and brain asymmetry by neonatal novelty exposure. J. Neurosci. 2003, 23:8254-8260.
78. Terranova M.L., Cirulli F., Laviola G. Behavioral and hormonal effects of partner familiarity in periadolescent rat pairs upon novelty exposure. Psychoneuroendocrinology 1999, 24:639-656.
79. van Hasselt F.N., Cornelisse S., Yuan Zhang T., Meaney M.J., Velzing E.H., Krugers H.J., Joels M. Adult hippocampal glucocorticoid receptor expression and dentate synaptic plasticity correlate with maternal care received by individuals early in life. Hippocampus 2012, 22:255-266.
80. Vanderschuren L.J., Niesink R.J., Spruijt B.M., Van Ree J.M. Effects of morphine on different aspects of social play in juvenile rats. Psychopharmacology (Berl.) 1995, 117:225-231.
81. Vanderschuren L.J., Niesink R.J., Van Ree J.M. The neurobiology of social play behavior in rats. Neurosci. Biobehav. Rev. 1997, 21:309-326.
82. Vanelzakker M.B., Zoladz P.R., Thompson V.M., Park C.R., Halonen J.D., Spencer R.L., Diamond D.M. Influence of pre-training predator stress on the expression of c-Fos mRNA in the hippocampus, amygdala, and striatum following long-term spatial memory retrieval. Front. Behav. Neurosci. 2011, 5:30.
83. Veenema A.H., Blume A., Niederle D., Buwalda B., Neumann I.D. Effects of early life stress on adult male aggression and hypothalamic vasopressin and serotonin. Eur. J. Neurosci. 2006, 24:1711-1720.
84. Veenema A.H., Neumann I.D. Maternal separation enhances offensive play-fighting, basal corticosterone and hypothalamic vasopressin mRNA expression in juvenile male rats. Psychoneuroendocrinology 2009, 34:463-467.
85. Vyas A., Bernal S., Chattarji S. Effects of chronic stress on dendritic arborization in the central and extended amygdala. Brain Res. 2003, 965:290-294.
86. Vyas A., Pillai A.G., Chattarji S. Recovery after chronic stress fails to reverse amygdaloid neuronal hypertrophy and enhanced anxiety-like behavior. Neuroscience 2004, 128:667-673.
87. Wiener S.G., Johnson D.F., Levine S. Influence of postnatal rearing conditions on the response of squirrel monkey infants to brief perturbations in mother-infant relationships. Physiol. Behav. 1987, 39:21-26.
88. Zhang T.Y., Chretien P., Meaney M.J., Gratton A. Influence of naturally occurring variations in maternal care on prepulse inhibition of acoustic startle and the medial prefrontal cortical dopamine response to stress in adult rats. J. Neurosci. 2005, 25:1493-1502.