Denial of reward in the neonate shapes sociability and serotonergic activity in the adult rat

PLoS ONE

Volumn 7, Issue 3, 2012, Pages

  Diamantopoulou, Anastasia ^a   Raftogianni, Androniki ^a   Stamatakis, Antonios ^a   Alikaridis, Filaretos ^b   Oitzl, Melly S ^c   Stylianopoulou, Fotini ^a  

^a UNIVERSITY OF ATHENS   (Greece)

^b UNIVERSITY OF ATHENS MEDICAL SCHOOL   (Greece)

^c LEIDEN UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

SEROTONIN; SEROTONIN 1A RECEPTOR; SEROTONIN TRANSPORTER;

ABNORMAL BEHAVIOR; AGGRESSION; AMYGDALOID NUCLEUS; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BODY POSTURE; BRAIN REGION; CONTROLLED STUDY; COPING BEHAVIOR; DENIAL; EXPERIMENTAL RAT; IMMUNOCOMPETENT CELL; MAZE TEST; NEONATAL STRESS; NEWBORN; NONHUMAN; PERINATAL PERIOD; PREFRONTAL CORTEX; PROTEIN EXPRESSION; RAT; REWARD; SEROTONIN BRAIN LEVEL; SEROTONINERGIC SYSTEM; SOCIAL BEHAVIOR;

ANIMALS; BEHAVIOR, ANIMAL; BRAIN; CORTICOSTERONE; DENIAL (PSYCHOLOGY); HUMANS; MALE; RATS; RATS, WISTAR; RECEPTOR, SEROTONIN, 5-HT1A; REWARD; SEROTONIN; SEROTONIN PLASMA MEMBRANE TRANSPORT PROTEINS; SOCIAL BEHAVIOR; STRESS, PSYCHOLOGICAL;

ANIMALIA; RATTUS; RATTUS NORVEGICUS;

EID: 84858957883     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0033793     Document Type: Article

References (99)

1. Sanchez MM, Ladd CO, Plotsky PM, (2001) Early adverse experience as a developmental risk factor for later psychopathology: evidence from rodent and primate models. Dev Psychopathol 13: 419-449.
2. McEwen BS, (2003) Early life influences on life-long patterns of behavior and health. Ment Retard Dev Disabil Res Rev 9: 149-154.
3. Nemeroff CB, (2004) Neurobiological consequences of childhood trauma. J Clin Psychiatry 65 (Suppl 1): 18-28.
4. Heim C, Nemeroff CB, (2001) The role of childhood trauma in the neurobiology of mood and anxiety disorders: preclinical and clinical studies. Biol Psychiatry 49: 1023-1039.
5. Panagiotaropoulos T, Diamantopoulou A, Stamatakis A, Dimitropoulou M, Stylianopoulou F, (2009) Learning of a T-maze by rat pups when contact with the mother is either permitted or denied. Neurobiol Learn Mem 91: 2-12.
6. Lipton SA, Kater SB, (1989) Neurotransmitter regulation of neuronal outgrowth, plasticity and survival. Trends Neurosci 12: 265-270.
7. Levitt P, Harvey JA, Friedman E, Simansky K, Murphy EH, (1997) New evidence for neurotransmitter influences on brain development. Trends Neurosci 20: 269-274.
8. Vitalis T, Parnavelas JG, (2003) The role of serotonin in early cortical development. Dev Neurosci 25: 245-256.
9. Lauder JM, Tamir H, Sadler TW, (1988) Serotonin and morphogenesis. I. Sites of serotonin uptake and-binding protein immunoreactivity in the midgestation mouse embryo. Development 102: 709-720.
10. Dori IE, Dinopoulos A, Parnavelas JG, (1998) The development of the synaptic organization of the serotonergic system differs in brain areas with different functions. Exp Neurol 154: 113-125.
11. Ziabreva I, Poeggel G, Schnabel R, Braun K, (2003) Separation-induced receptor changes in the hippocampus and amygdala of Octodon degus: influence of maternal vocalizations. J Neurosci 23: 5329-5336.
12. Vazquez DM, Lopez JF, Van Hoers H, Watson SJ, Levine S, (2000) Maternal deprivation regulates serotonin 1A and 2A receptors in the infant rat. Brain Res 855: 76-82.
13. Vicentic A, Francis D, Moffett M, Lakatos A, Rogge G, et al. (2006) Maternal separation alters serotonergic transporter densities and serotonergic 1A receptors in rat brain. Neuroscience 140: 355-365.
14. Gartside SE, Johnson DA, Leitch MM, Troakes C, Ingram CD, (2003) Early life adversity programs changes in central 5-HT neuronal function in adulthood. Eur J Neurosci 17: 2401-2408.
15. Arborelius L, Hawks BW, Owens MJ, Plotsky PM, Nemeroff CB, (2004) Increased responsiveness of presumed 5-HT cells to citalopram in adult rats subjected to prolonged maternal separation relative to brief separation. Psychopharmacology (Berl) 176: 248-255.
16. Lee JH, Kim HJ, Kim JG, Ryu V, Kim BT, et al. (2007) Depressive behaviors and decreased expression of serotonin reuptake transporter in rats that experienced neonatal maternal separation. Neurosci Res 58: 32-39.
17. Oler JA, Fox AS, Shelton SE, Christian BT, Murali D, et al. (2009) Serotonin transporter availability in the amygdala and bed nucleus of the stria terminalis predicts anxious temperament and brain glucose metabolic activity. J Neurosci 29: 9961-9966.
18. Lesch KP, Merschdorf U, (2000) Impulsivity, aggression, and serotonin: a molecular psychobiological perspective. Behav Sci Law 18: 581-604.
19. Lesch KP, Bengel D, Heils A, Sabol SZ, Greenberg BD, et al. (1996) Association of anxiety-related traits with a polymorphism in the serotonin transporter gene regulatory region. Science 274: 1527-1531.
20. Collier DA, Stober G, Li T, Heils A, Catalano M, et al. (1996) A novel functional polymorphism within the promoter of the serotonin transporter gene: possible role in susceptibility to affective disorders. Mol Psychiatry 1: 453-460.
21. Lesch KP, (2007) Linking emotion to the social brain. The role of the serotonin transporter in human social behaviour. EMBO Rep 8 Spec No: S24-29.
22. Homberg JR, Olivier JD, Smits BM, Mul JD, Mudde J, et al. (2007) Characterization of the serotonin transporter knockout rat: a selective change in the functioning of the serotonergic system. Neuroscience 146: 1662-1676.
23. Caspi A, Sugden K, Moffitt TE, Taylor A, Craig IW, et al. (2003) Influence of life stress on depression: moderation by a polymorphism in the 5-HTT gene. Science 301: 386-389.
24. Barr CS, Newman TK, Shannon C, Parker C, Dvoskin RL, et al. (2004) Rearing condition and rh5-HTTLPR interact to influence limbic-hypothalamic-pituitary-adrenal axis response to stress in infant macaques. Biol Psychiatry 55: 733-738.
25. Bartolomucci A, Carola V, Pascucci T, Puglisi-Allegra S, Cabib S, et al. (2010) Increased vulnerability to psychosocial stress in heterozygous serotonin transporter knockout mice. Dis Model Mech 3: 459-470.
26. Kalin NH, Shelton SE, Fox AS, Rogers J, Oakes TR, et al. (2008) The serotonin transporter genotype is associated with intermediate brain phenotypes that depend on the context of eliciting stressor. Mol Psychiatry 13: 1021-1027.
27. Wellman CL, Izquierdo A, Garrett JE, Martin KP, Carroll J, et al. (2007) Impaired stress-coping and fear extinction and abnormal corticolimbic morphology in serotonin transporter knock-out mice. J Neurosci 27: 684-691.
28. Cicchetti D, Rogosch FA, Sturge-Apple ML, (2007) Interactions of child maltreatment and serotonin transporter and monoamine oxidase A polymorphisms: depressive symptomatology among adolescents from low socioeconomic status backgrounds. Dev Psychopathol 19: 1161-1180.
29. Barr CS, Newman TK, Becker ML, Parker CC, Champoux M, et al. (2003) The utility of the non-human primate; model for studying gene by environment interactions in behavioral research. Genes Brain Behav 2: 336-340.
30. Akimova E, Lanzenberger R, Kasper S, (2009) The serotonin-1A receptor in anxiety disorders. Biol Psychiatry 66: 627-635.
31. Witte AV, Floel A, Stein P, Savli M, Mien LK, et al. (2009) Aggression is related to frontal serotonin-1A receptor distribution as revealed by PET in healthy subjects. Hum Brain Mapp 30: 2558-2570.
32. Kasper S, Tauscher J, Willeit M, Stamenkovic M, Neumeister A, et al. (2002) Receptor and transporter imaging studies in schizophrenia, depression, bulimia and Tourette's disorder-implications for psychopharmacology. World J Biol Psychiatry 3: 133-146.
33. Li Q, Wichems C, Heils A, Lesch KP, Murphy DL, (2000) Reduction in the density and expression, but not G-protein coupling, of serotonin receptors (5-HT1A) in 5-HT transporter knock-out mice: gender and brain region differences. J Neurosci 20: 7888-7895.
34. van der Vegt BJ, Lieuwes N, van de Wall EH, Kato K, Moya-Albiol L, et al. (2003) Activation of serotonergic neurotransmission during the performance of aggressive behavior in rats. Behav Neurosci 117: 667-674.
35. Veenema AH, Blume A, Niederle D, Buwalda B, Neumann ID, (2006) Effects of early life stress on adult male aggression and hypothalamic vasopressin and serotonin. Eur J Neurosci 24: 1711-1720.
36. Miczek KA, Fish EW, De Bold JF, De Almeida RM, (2002) Social and neural determinants of aggressive behavior: pharmacotherapeutic targets at serotonin, dopamine and gamma-aminobutyric acid systems. Psychopharmacology (Berl) 163: 434-458.
37. van der Vegt BJ, de Boer SF, Buwalda B, de Ruiter AJ, de Jong JG, et al. (2001) Enhanced sensitivity of postsynaptic serotonin-1A receptors in rats and mice with high trait aggression. Physiol Behav 74: 205-211.
38. Caramaschi D, de Boer SF, Koolhaas JM, (2007) Differential role of the 5-HT1A receptor in aggressive and non-aggressive mice: an across-strain comparison. Physiol Behav 90: 590-601.
39. Pellis SM, McKenna M, (1995) What do rats find rewarding in play fighting?-an analysis using drug-induced non-playful partners. Behav Brain Res 68: 65-73.
40. Pellis SM, Pellis VC, (1998) Play fighting of rats in comparative perspective: a schema for neurobehavioral analyses. Neurosci Biobehav Rev 23: 87-101.
41. Vanderschuren LJ, Niesink RJ, Van Ree JM, (1997) The neurobiology of social play behavior in rats. Neurosci Biobehav Rev 21: 309-326.
42. van den Berg CL, Hol T, Van Ree JM, Spruijt BM, Everts H, et al. (1999) Play is indispensable for an adequate development of coping with social challenges in the rat. Dev Psychobiol 34: 129-138.
43. Veenema AH, Neumann ID, (2009) Maternal separation enhances offensive play-fighting, basal corticosterone and hypothalamic vasopressin mRNA expression in juvenile male rats. Psychoneuroendocrinology 34: 463-467.
44. Arnold JL, Siviy SM, (2002) Effects of neonatal handling and maternal separation on rough-and-tumble play in the rat. Dev Psychobiol 41: 205-215.
45. Kotch JB, Lewis T, Hussey JM, English D, Thompson R, et al. (2008) Importance of early neglect for childhood aggression. Pediatrics 121: 725-731.
46. Beauregard M, Malkova L, Bachevalier J, (1995) Stereotypies and loss of social affiliation after early hippocampectomy in primates. Neuroreport 6: 2521-2526.
47. Machado CJ, Bachevalier J, (2006) The impact of selective amygdala, orbital frontal cortex, or hippocampal formation lesions on established social relationships in rhesus monkeys (Macaca mulatta). Behav Neurosci 120: 761-786.
48. Bachevalier J, Malkova L, (2006) The amygdala and development of social cognition: theoretical comment on Bauman, Toscano, Mason, Lavenex, and Amaral (2006). Behav Neurosci 120: 989-991.
49. Siever LJ, (2008) Neurobiology of aggression and violence. Am J Psychiatry 165: 429-442.
50. Venerosi A, Cirulli F, Capone F, Alleva E, (2003) Prolonged perinatal AZT administration and early maternal separation: effects on social and emotional behaviour of periadolescent mice. Pharmacol Biochem Behav 74: 671-681.
51. Toth M, Halasz J, Mikics E, Barsy B, Haller J, (2008) Early social deprivation induces disturbed social communication and violent aggression in adulthood. Behav Neurosci 122: 849-854.
52. Blanchard RJ, Blanchard DC, (1977) Aggressive behavior in the rat. Behav Biol 21: 197-224.
53. Vitiello B, Stoff DM, (1997) Subtypes of aggression and their relevance to child psychiatry. J Am Acad Child Adolesc Psychiatry 36: 307-315.
54. Dodge KA, Bates JE, Pettit GS, (1990) Mechanisms in the cycle of violence. Science 250: 1678-1683.
55. Ethier LS, Lemelin JP, Lacharite C, (2004) A longitudinal study of the effects of chronic maltreatment on children's behavioral and emotional problems. Child Abuse Negl 28: 1265-1278.
56. Fonagy P, (2004) Early-life trauma and the psychogenesis and prevention of violence. Ann N Y Acad Sci 1036: 181-200.
57. Lewis DO, (1992) From abuse to violence: psychophysiological consequences of maltreatment. J Am Acad Child Adolesc Psychiatry 31: 383-391.
58. Widom CS, (1989) Child abuse, neglect, and adult behavior: research design and findings on criminality, violence, and child abuse. Am J Orthopsychiatry 59: 355-367.
59. Higley JD, King ST Jr, Hasert MF, Champoux M, Suomi SJ, et al. (1996) Stability of interindividual differences in serotonin function and its relationship to severe aggression and competent social behavior in rhesus macaque females. Neuropsychopharmacology 14: 67-76.
60. Suomi SJ, (2005) Aggression and social behaviour in rhesus monkeys. Novartis Found Symp 268: 216-222; discussion 222-216, 242-253.
61. Sarchiapone M, Jaussent I, Roy A, Carli V, Guillaume S, et al. (2009) Childhood trauma as a correlative factor of suicidal behavior- via aggression traits. Similar results in an Italian and in a French sample. Eur Psychiatry 24: 57-62.
62. Bolhuis JE, Schouten WG, de Leeuw JA, Schrama JW, Wiegant VM, (2004) Individual coping characteristics, rearing conditions and behavioural flexibility in pigs. Behav Brain Res 152: 351-360.
63. Coppens CM, de Boer SF, Koolhaas JM, (2010) Coping styles and behavioural flexibility: towards underlying mechanisms. Philos Trans R Soc Lond B Biol Sci 365: 4021-4028.
64. Koolhaas JM, de Boer SF, Coppens CM, Buwalda B, Neuroendocrinology of coping styles: towards understanding the biology of individual variation. Front Neuroendocrinol 31: 307-321.
65. Koolhaas JM, de Boer SF, Coppens CM, Buwalda B, (2010) Neuroendocrinology of coping styles: towards understanding the biology of individual variation. Front Neuroendocrinol 31: 307-321.
66. van Erp AM, Miczek KA, (2000) Aggressive behavior, increased accumbal dopamine, and decreased cortical serotonin in rats. J Neurosci 20: 9320-9325.
67. Miczek KA, de Almeida RM, Kravitz EA, Rissman EF, de Boer SF, et al. (2007) Neurobiology of escalated aggression and violence. J Neurosci 27: 11803-11806.
68. de Boer SF, van der Vegt BJ, Koolhaas JM, (2003) Individual variation in aggression of feral rodent strains: a standard for the genetics of aggression and violence? Behav Genet 33: 485-501.
69. van Honk J, Harmon-Jones E, Morgan BE, Schutter DJ, (2010) Socially explosive minds: the triple imbalance hypothesis of reactive aggression. J Pers 78: 67-94.
70. Meerlo P, Horvath KM, Luiten PG, Angelucci L, Catalani A, et al. (2001) Increased maternal corticosterone levels in rats: effects on brain 5-HT1A receptors and behavioral coping with stress in adult offspring. Behav Neurosci 115: 1111-1117.
71. Stamatakis A, Mantelas A, Papaioannou A, Pondiki S, Fameli M, et al. (2006) Effect of neonatal handling on serotonin 1A sub-type receptors in the rat hippocampus. Neuroscience 140: 1-11.
72. Papaioannou A, Dafni U, Alikaridis F, Bolaris S, Stylianopoulou F, (2002) Effects of neonatal handling on basal and stress-induced monoamine levels in the male and female rat brain. Neuroscience 114: 195-206.
73. de Boer SF, Koolhaas JM, (2005) 5-HT1A and 5-HT1B receptor agonists and aggression: a pharmacological challenge of the serotonin deficiency hypothesis. Eur J Pharmacol 526: 125-139.
74. Homberg JR, Pattij T, Janssen MC, Ronken E, De Boer SF, et al. (2007) Serotonin transporter deficiency in rats improves inhibitory control but not behavioural flexibility. Eur J Neurosci 26: 2066-2073.
75. Roy A, (2002) Self-rated childhood emotional neglect and CSF monoamine indices in abstinent cocaine-abusing adults: possible implications for suicidal behavior. Psychiatry Res 112: 69-75.
76. Ichise M, Vines DC, Gura T, Anderson GM, Suomi SJ, et al. (2006) Effects of early life stress on [11C]DASB positron emission tomography imaging of serotonin transporters in adolescent peer- and mother-reared rhesus monkeys. J Neurosci 26: 4638-4643.
77. Veenema AH, (2009) Early life stress, the development of aggression and neuroendocrine and neurobiological correlates: what can we learn from animal models? Front Neuroendocrinol 30: 497-518.
78. Domes G, Heinrichs M, Glascher J, Buchel C, Braus DF, et al. (2007) Oxytocin attenuates amygdala responses to emotional faces regardless of valence. Biol Psychiatry 62: 1187-1190.
79. Morris JS, Ohman A, Dolan RJ, (1999) A subcortical pathway to the right amygdala mediating "unseen" fear. Proc Natl Acad Sci U S A 96: 1680-1685.
80. Cools R, Calder AJ, Lawrence AD, Clark L, Bullmore E, et al. (2005) Individual differences in threat sensitivity predict serotonergic modulation of amygdala response to fearful faces. Psychopharmacology (Berl) 180: 670-679.
81. Amat J, Matus-Amat P, Watkins LR, Maier SF, (1998) Escapable and inescapable stress differentially and selectively alter extracellular levels of 5-HT in the ventral hippocampus and dorsal periaqueductal gray of the rat. Brain Res 797: 12-22.
82. Linthorst AC, Flachskamm C, Barden N, Holsboer F, Reul JM, (2000) Glucocorticoid receptor impairment alters CNS responses to a psychological stressor: an in vivo microdialysis study in transgenic mice. Eur J Neurosci 12: 283-291.
83. Keeney A, Jessop DS, Harbuz MS, Marsden CA, Hogg S, et al. (2006) Differential effects of acute and chronic social defeat stress on hypothalamic-pituitary-adrenal axis function and hippocampal serotonin release in mice. J Neuroendocrinol 18: 330-338.
84. Huot RL, Thrivikraman KV, Meaney MJ, Plotsky PM, (2001) Development of adult ethanol preference and anxiety as a consequence of neonatal maternal separation in Long Evans rats and reversal with antidepressant treatment. Psychopharmacology (Berl) 158: 366-373.
85. Kalinichev M, Easterling KW, Plotsky PM, Holtzman SG, (2002) Long-lasting changes in stress-induced corticosterone response and anxiety-like behaviors as a consequence of neonatal maternal separation in Long-Evans rats. Pharmacol Biochem Behav 73: 131-140.
86. Wigger A, Neumann ID, (1999) Periodic maternal deprivation induces gender-dependent alterations in behavioral and neuroendocrine responses to emotional stress in adult rats. Physiol Behav 66: 293-302.
87. Ladd CO, Huot RL, Thrivikraman KV, Nemeroff CB, Meaney MJ, et al. (2000) Long-term behavioral and neuroendocrine adaptations to adverse early experience. Prog Brain Res 122: 81-103.
88. Homberg JR, Lesch KP, (2011) Looking on the bright side of serotonin transporter gene variation. Biol Psychiatry 69: 513-519.
89. Belsky J, Jonassaint C, Pluess M, Stanton M, Brummett B, et al. (2009) Vulnerability genes or plasticity genes? Mol Psychiatry 14: 746-754.
90. Belsky J, (1997) Theory testing, effect-size evaluation, and differential susceptibility to rearing influence: the case of mothering and attachment. Child Dev 68: 598-600.
91. Diamantopoulou A, Stamatakis A, Panagiotaropoulos T, Stylianopoulou F, (2010) 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 181: 89-99.
92. Pellis SM, Pellis VC, (1990) Differential rates of attack, defense, and counterattack during the developmental decrease in play fighting by male and female rats. Dev Psychobiol 23: 215-231.
93. Panksepp J, Beatty WW, (1980) Social deprivation and play in rats. Behav Neural Biol 30: 197-206.
94. Tornatzky W, Miczek KA, (1994) Behavioral and autonomic responses to intermittent social stress: differential protection by clonidine and metoprolol. Psychopharmacology (Berl) 116: 346-356.
95. Koolhaas JM, Korte SM, De Boer SF, Van Der Vegt BJ, Van Reenen CG, et al. (1999) Coping styles in animals: current status in behavior and stress-physiology. Neurosci Biobehav Rev 23: 925-935.
96. Miczek KA, Covington HE 3rd, Nikulina EM Jr, Hammer RP, (2004) Aggression and defeat: persistent effects on cocaine self-administration and gene expression in peptidergic and aminergic mesocorticolimbic circuits. Neurosci Biobehav Rev 27: 787-802.
97. Gardner KL, Thrivikraman KV, Lightman SL, Plotsky PM, Lowry CA, (2005) Early life experience alters behavior during social defeat: focus on serotonergic systems. Neuroscience 136: 181-191.
98. Panagiotaropoulos T, Pondiki S, Papaioannou A, Alikaridis F, Stamatakis A, et al. (2004) Neonatal handling and gender modulate brain monoamines and plasma corticosterone levels following repeated stressors in adulthood. Neuroendocrinology 80: 181-191.
99. Paxinos G, Watson C, (2005) The rat brain in stereotaxic coordinates Amsterdam; Boston Elsevier Academic Press pp. xliii [166].