Individual variations in maternal care early in life correlate with later life decision-making and c-Fos expression in prefrontal subregions of rats

PLoS ONE

Volumn 7, Issue 5, 2012, Pages

  van Hasselt, Felisa N ^a   de Visser, Leonie ^b   Tieskens, Jacintha M ^a   Cornelisse, Sandra ^b   Baars, Annemarie M ^b   Lavrijsen, Marla ^b   Krugers, Harm J ^a   van den Bos, Ruud ^b   Joëls, Marian ^b  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN C FOS;

ADULTHOOD; ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANXIETY; ARTICLE; COHORT ANALYSIS; DECISION MAKING; DENDRITE; FEMALE; GROOMING; INFRALIMBIC CORTEX; INSULA; LICKING; LIFE; LIMBIC CORTEX; MALE; MATERNAL CARE; MAZE TEST; MENTAL TASK; NONHUMAN; ORBITAL CORTEX; PATHOLOGICAL GAMBLING; PERINATAL PERIOD; PREFRONTAL CORTEX; PRELIMBIC CORTEX; PROTEIN EXPRESSION; PYRAMIDAL NERVE CELL; RAT; TASK PERFORMANCE; ANIMAL; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; IMMEDIATE EARLY GENE; MATERNAL BEHAVIOR; METABOLISM;

ANIMALIA; RATTUS; RODENTIA;

ANIMALS; BEHAVIOR, ANIMAL; DECISION MAKING; FEMALE; GAMBLING; GENE EXPRESSION REGULATION; GENES, IMMEDIATE-EARLY; MALE; MATERNAL BEHAVIOR; PREFRONTAL CORTEX; PROTO-ONCOGENE PROTEINS C-FOS; RATS;

EID: 84861676253     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0037820     Document Type: Article

References (98)

1. Fossati P, Amar G, Raoux N, Ergis AM, Allilaire JF, (1999) Executive functioning and verbal memory in young patients with unipolar depression and schizophrenia. Psychiatry Res 89: 171-187.
2. Rogers MA, Kasai K, Koji M, Fukuda R, Iwanami A, et al. (2004) Executive and prefrontal dysfunction in unipolar depression: a review of neuropsychological and imaging evidence. Neurosci Res 50: 1-11.
3. Bremner JD, (2002) Neuroimaging studies in post-traumatic stress disorder. Curr Psychiatry Rep 4: 254-263.
4. Mann JJ, McBride PA, Malone KM, DeMeo M, Keilp J, (1995) Blunted serotonergic responsivity in depressed inpatients. Neuropsychopharmacology 13: 53-64.
5. Nikolaus S, Antke C, Beu M, Muller HW, (2010) Cortical GABA, striatal dopamine and midbrain serotonin as the key players in compulsive and anxiety disorders-results from in vivo imaging studies. Rev Neurosci 21: 119-139.
6. Nutt DJ, (2001) Neurobiological mechanisms in generalized anxiety disorder. J Clin Psychiatry 62 Suppl 11: 22-27; discussion 28.
7. Olvera-Cortes ME, Anguiano-Rodriguez P, Lopez-Vazquez MA, Alfaro JM, (2008) Serotonin/dopamine interaction in learning. Prog Brain Res 172: 567-602.
8. Shansky RM, Morrison JH, (2009) Stress-induced dendritic remodeling in the medial prefrontal cortex: effects of circuit, hormones and rest. Brain Res 1293: 108-113.
9. Diorio D, Viau V, Meaney MJ, (1993) The role of the medial prefrontal cortex (cingulate gyrus) in the regulation of hypothalamic-pituitary-adrenal responses to stress. J Neurosci 13: 3839-3847.
10. Arnsten AF, (2009) Stress signalling pathways that impair prefrontal cortex structure and function. Nat Rev Neurosci 10: 410-422.
11. Sullivan RM, Gratton A, (2002) Prefrontal cortical regulation of hypothalamic-pituitary-adrenal function in the rat and implications for psychopathology: side matters. Psychoneuroendocrinology 27: 99-114.
12. Agid O, Shapira B, Zislin J, Ritsner M, Hanin B, et al. (1999) Environment and vulnerability to major psychiatric illness: a case control study of early parental loss in major depression, bipolar disorder and schizophrenia. Mol Psychiatry 4: 163-172.
13. Breier A, Kelsoe JR, Jr, Kirwin PD, Beller SA, Wolkowitz OM, et al. (1988) Early parental loss and development of adult psychopathology. Arch Gen Psychiatry 45: 987-993.
14. Niwa M, Matsumoto Y, Mouri A, Ozaki N, Nabeshima T, (2010) Vulnerability in early life to changes in the rearing environment plays a crucial role in the aetiopathology of psychiatric disorders. Int J Neuropsychopharmacol pp. 1-19.
15. Pechtel P, Pizzagalli DA, (2010) Effects of early life stress on cognitive and affective function: an integrated review of human literature. Psychopharmacology (Berl).
16. Bock J, Gruss M, Becker S, Braun K, (2005) Experience-induced changes of dendritic spine densities in the prefrontal and sensory cortex: correlation with developmental time windows. Cereb Cortex 15: 802-808.
17. Monroy E, Hernandez-Torres E, Flores G, (2010) Maternal separation disrupts dendritic morphology of neurons in prefrontal cortex, hippocampus, and nucleus accumbens in male rat offspring. J Chem Neuroanat 40: 93-101.
18. Pascual R, Zamora-Leon SP, (2007) Effects of neonatal maternal deprivation and postweaning environmental complexity on dendritic morphology of prefrontal pyramidal neurons in the rat. Acta Neurobiol Exp (Wars) 67: 471-479.
19. Liu D, Diorio J, Tannenbaum B, Caldji C, Francis D, et al. (1997) Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress. Science 277: 1659-1662.
20. Weaver IC, Meaney MJ, Szyf M, (2006) Maternal care effects on the hippocampal transcriptome and anxiety-mediated behaviors in the offspring that are reversible in adulthood. Proc Natl Acad Sci U S A 103: 3480-3485.
21. Champagne DL, Bagot RC, van Hasselt F, Ramakers G, Meaney MJ, et al. (2008) Maternal care and hippocampal plasticity: evidence for experience-dependent structural plasticity, altered synaptic functioning, and differential responsiveness to glucocorticoids and stress. J Neurosci 28: 6037-6045.
22. Liu D, Diorio J, Day JC, Francis DD, Meaney MJ, (2000) Maternal care, hippocampal synaptogenesis and cognitive development in rats. Nat Neurosci 3: 799-806.
23. Bagot RC, van Hasselt FN, Champagne DL, Meaney MJ, Krugers HJ, et al. (2009) Maternal care determines rapid effects of stress mediators on synaptic plasticity in adult rat hippocampal dentate gyrus. Neurobiol Learn Mem 92: 292-300.
24. Chudasama Y, Robbins TW, (2006) Functions of frontostriatal systems in cognition: comparative neuropsychopharmacological studies in rats, monkeys and humans. Biol Psychol 73: 19-38.
25. Claessens SE, Daskalakis NP, van der Veen R, Oitzl MS, de Kloet ER,et al. Development of individual differences in stress responsiveness: an overview of factors mediating the outcome of early life experiences. Psychopharmacology (Berl) 214: 141-154.
26. van Hasselt FN, Boudewijns ZS, van der Knaap NJ, Krugers HJ, Joels M, (2012) Maternal care received by individual pups correlates with adult CA1 dendritic morphology and synaptic plasticity in a sex-dependent manner. J Neuroendocrinol 24: 331-340.
27. van Hasselt FN, Cornelisse S, Zhang TY, Meaney MJ, Velzing EH, et al. (2012) Adult hippocampal glucocorticoid receptor expression and dentate synaptic plasticity correlate with maternal care received by individuals early in life. Hippocampus 22: 255-266.
28. van Hasselt FN, Tieskens JM, Trezza V, Krugers HJ, Vanderschuren LJ, et al. (2012) Within-litter variation in maternal care received by individual pups correlates with adolescent social play behavior in male rats. Physiol Behav.
29. Van den Bos R, Lasthuis W, Den Heijer E, Van der Harst J, Spruijt B, (2006) Toward a rodent model of the Iowa gambling task. Behav Res Methods 38: 470-478.
30. De Visser L, Baars AM, Lavrijsen M, van der Weerd CM, van den Bos R, (2011) Decision-making performance is related to levels of anxiety and differential recruitment of frontostriatal areas in male rats. Neuroscience 184: 97-106.
31. Champagne FA, Francis DD, Mar A, Meaney MJ, (2003) Variations in maternal care in the rat as a mediating influence for the effects of environment on development. Physiol Behav 79: 359-371.
32. Pryce CR, Bettschen D, Feldon J, (2001) Comparison of the effects of early handling and early deprivation on maternal care in the rat. Dev Psychobiol 38: 239-251.
33. Moore CL, Morelli GA, (1979) Mother rats interact differently with male and female offspring. J Comp Physiol Psychol 93: 677-684.
34. De Visser L, Baars AM, Van 't Klooster J, Van den Bos R, (2011) Transient inactivation of the medial prefrontal cortex affects both anxiety and decision-making in male wistar rats. Front Neurosci 5: 102.
35. de Visser L, Homberg JR, Mitsogiannis M, Zeeb FD, Rivalan M, et al. (2011) Rodent versions of the iowa gambling task: opportunities and challenges for the understanding of decision-making. Front Neurosci 5: 109.
36. Homberg JR, van den Bos R, den Heijer E, Suer R, Cuppen E, (2008) Serotonin transporter dosage modulates long-term decision-making in rat and human. Neuropharmacology 55: 80-84.
37. Bechara A, Damasio AR, Damasio H, Anderson SW, (1994) Insensitivity to future consequences following damage to human prefrontal cortex. Cognition 50: 7-15.
38. Van den Bos R, Houx BB, Spruijt BM, (2006) The effect of reward magnitude differences on choosing disadvantageous decks in the Iowa Gambling Task. Biol Psychol 71: 155-161.
39. Paxinos G, Watson C, (2005) The rat brain in stereotaxic coordinates: Elsevier Academic Press.
40. Boekhoorn K, Terwel D, Biemans B, Borghgraef P, Wiegert O, et al. (2006) Improved long-term potentiation and memory in young tau-P301L transgenic mice before onset of hyperphosphorylation and tauopathy. J Neurosci 26: 3514-3523.
41. Overman WH, (2004) Sex differences in early childhood, adolescence, and adulthood on cognitive tasks that rely on orbital prefrontal cortex. Brain Cogn 55: 134-147.
42. Meaney MJ, (2001) Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Annu Rev Neurosci 24: 1161-1192.
43. Caldji C, Tannenbaum B, Sharma S, Francis D, Plotsky PM, et al. (1998) Maternal care during infancy regulates the development of neural systems mediating the expression of fearfulness in the rat. Proc Natl Acad Sci U S A 95: 5335-5340.
44. Fernandes C, Gonzalez MI, Wilson CA, File SE, (1999) Factor analysis shows that female rat behaviour is characterized primarily by activity, male rats are driven by sex and anxiety. Pharmacol Biochem Behav 64: 731-738.
45. De Visser L, Van der Knaap LJ, Van de Loo AJ, Van der Weerd CM, Ohl F, et al. (2010) Trait anxiety affects decision-making differently in healthy men and women: towards gender-specific endophenotypes of anxiety. Neuropsychologia 48: 1598-1606.
46. Miu AC, Heilman RM, Houser D, (2008) Anxiety impairs decision-making: psychophysiological evidence from an Iowa Gambling Task. Biol Psychol 77: 353-358.
47. Van den Bos R, De Visser L, Van de Loo AJAE, Mets MAJ, Van Willigenburg GM, et al. (2012) Sex differences in decision-making in adult normal volunteers are related to differences in the interaction of emotion and cognitive control. In: Moore KO, Gonzalez NP, editors. Handbook on Psychology of Decision-making: Nova Science Publisher Inc.
48. Overman W, Graham L, Redmond A, Eubank R, Boettcher L, et al. (2006) Contemplation of moral dilemmas eliminates sex differences on the Iowa gambling task. Behav Neurosci 120: 817-825.
49. Reavis R, Overman WH, (2001) Adult sex differences on a decision-making task previously shown to depend on the orbital prefrontal cortex. Behav Neurosci 115: 196-206.
50. van den Bos R, Harteveld M, Stoop H, (2009) Stress and decision-making in humans: performance is related to cortisol reactivity, albeit differently in men and women. Psychoneuroendocrinology 34: 1449-1458.
51. Reynolds SM, Zahm DS, (2005) Specificity in the projections of prefrontal and insular cortex to ventral striatopallidum and the extended amygdala. J Neurosci 25: 11757-11767.
52. Berridge KC, Kringelbach ML, (2008) Affective neuroscience of pleasure: reward in humans and animals. Psychopharmacology (Berl) 199: 457-480.
53. Ragozzino ME, Kesner RP, (1999) The role of the agranular insular cortex in working memory for food reward value and allocentric space in rats. Behav Brain Res 98: 103-112.
54. Salamone JD, (1996) The behavioral neurochemistry of motivation: methodological and conceptual issues in studies of the dynamic activity of nucleus accumbens dopamine. J Neurosci Methods 64: 137-149.
55. Todtenkopf MS, Parsegian A, Naydenov A, Neve RL, Konradi C, et al. (2006) Brain reward regulated by AMPA receptor subunits in nucleus accumbens shell. J Neurosci 26: 11665-11669.
56. Bechara A, Damasio H, Damasio AR, Lee GP, (1999) Different contributions of the human amygdala and ventromedial prefrontal cortex to decision-making. J Neurosci 19: 5473-5481.
57. Bolla KI, Eldreth DA, Matochik JA, Cadet JL, (2004) Sex-related differences in a gambling task and its neurological correlates. Cereb Cortex 14: 1226-1232.
58. Bishop S, Duncan J, Brett M, Lawrence AD, (2004) Prefrontal cortical function and anxiety: controlling attention to threat-related stimuli. Nat Neurosci 7: 184-188.
59. Brand M, Labudda K, Markowitsch HJ, (2006) Neuropsychological correlates of decision-making in ambiguous and risky situations. Neural Netw 19: 1266-1276.
60. Ernst M, Bolla K, Mouratidis M, Contoreggi C, Matochik JA, et al. (2002) Decision-making in a risk-taking task: a PET study. Neuropsychopharmacology 26: 682-691.
61. Grachev ID, Apkarian AV, (2000) Anxiety in healthy humans is associated with orbital frontal chemistry. Mol Psychiatry 5: 482-488.
62. Lawrence NS, Jollant F, O'Daly O, Zelaya F, Phillips ML, (2009) Distinct roles of prefrontal cortical subregions in the Iowa Gambling Task. Cereb Cortex 19: 1134-1143.
63. Li X, Lu ZL, D'Argembeau A, Ng M, Bechara A The Iowa Gambling Task in fMRI images. Hum Brain Mapp 31: 410-423.
64. Rivalan M, Coutureau E, Fitoussi A, Dellu-Hagedorn F, (2011) Inter-individual decision-making differences in the effects of cingulate, orbitofrontal, and prelimbic cortex lesions in a rat gambling task. Front Behav Neurosci 5: 22.
65. Zeeb FD, Winstanley CA, (2011) Lesions of the basolateral amygdala and orbitofrontal cortex differentially affect acquisition and performance of a rodent gambling task. J Neurosci 31: 2197-2204.
66. Balleine BW, O'Doherty JP, (2010) Human and rodent homologies in action control: corticostriatal determinants of goal-directed and habitual action. Neuropsychopharmacology 35: 48-69.
67. Birrell JM, Brown VJ, (2000) Medial frontal cortex mediates perceptual attentional set shifting in the rat. J Neurosci 20: 4320-4324.
68. Dias R, Robbins TW, Roberts AC, (1996) Dissociation in prefrontal cortex of affective and attentional shifts. Nature 380: 69-72.
69. Floresco SB, Block AE, Tse MT, (2008) Inactivation of the medial prefrontal cortex of the rat impairs strategy set-shifting, but not reversal learning, using a novel, automated procedure. Behav Brain Res 190: 85-96.
70. Ragozzino ME, Detrick S, Kesner RP, (1999) Involvement of the prelimbic-infralimbic areas of the rodent prefrontal cortex in behavioral flexibility for place and response learning. J Neurosci 19: 4585-4594.
71. Sul JH, Kim H, Huh N, Lee D, Jung MW, (2010) Distinct roles of rodent orbitofrontal and medial prefrontal cortex in decision making. Neuron 66: 449-460.
72. Tran-Tu-Yen DA, Marchand AR, Pape JR, Di Scala G, Coutureau E, (2009) Transient role of the rat prelimbic cortex in goal-directed behaviour. Eur J Neurosci 30: 464-471.
73. Young JJ, Shapiro ML, (2009) Double dissociation and hierarchical organization of strategy switches and reversals in the rat PFC. Behav Neurosci 123: 1028-1035.
74. Lin CH, Chiu YC, Cheng CM, Hsieh JC, (2008) Brain maps of Iowa gambling task. BMC Neurosci 9: 72.
75. Fukui H, Murai T, Fukuyama H, Hayashi T, Hanakawa T, (2005) Functional activity related to risk anticipation during performance of the Iowa Gambling Task. Neuroimage 24: 253-259.
76. McClure SM, Laibson DI, Loewenstein G, Cohen JD, (2004) Separate neural systems value immediate and delayed monetary rewards. Science 306: 503-507.
77. Tanaka SC, Doya K, Okada G, Ueda K, Okamoto Y, et al. (2004) Prediction of immediate and future rewards differentially recruits cortico-basal ganglia loops. Nat Neurosci 7: 887-893.
78. Pais-Vieira M, Lima D, Galhardo V, (2007) Orbitofrontal cortex lesions disrupt risk assessment in a novel serial decision-making task for rats. Neuroscience 145: 225-231.
79. Hsu M, Bhatt M, Adolphs R, Tranel D, Camerer CF, (2005) Neural systems responding to degrees of uncertainty in human decision-making. Science 310: 1680-1683.
80. Ongur D, Price JL, (2000) The organization of networks within the orbital and medial prefrontal cortex of rats, monkeys and humans. Cereb Cortex 10: 206-219.
81. Mainen ZF, Kepecs A, (2009) Neural representation of behavioral outcomes in the orbitofrontal cortex. Curr Opin Neurobiol 19: 84-91.
82. Rolls ET, Grabenhorst F, (2008) The orbitofrontal cortex and beyond: from affect to decision-making. Prog Neurobiol 86: 216-244.
83. Takahashi YK, Roesch MR, Stalnaker TA, Haney RZ, Calu DJ, et al. (2009) The orbitofrontal cortex and ventral tegmental area are necessary for learning from unexpected outcomes. Neuron 62: 269-280.
84. Schoenbaum G, Setlow B, Saddoris MP, Gallagher M, (2003) Encoding predicted outcome and acquired value in orbitofrontal cortex during cue sampling depends upon input from basolateral amygdala. Neuron 39: 855-867.
85. Clark L, Bechara A, Damasio H, Aitken MR, Sahakian BJ, et al. (2008) Differential effects of insular and ventromedial prefrontal cortex lesions on risky decision-making. Brain 131: 1311-1322.
86. Preuschoff K, Quartz SR, Bossaerts P, (2008) Human insula activation reflects risk prediction errors as well as risk. J Neurosci 28: 2745-2752.
87. Yu R, Mobbs D, Seymour B, Calder AJ, (2010) Insula and striatum mediate the default bias. J Neurosci 30: 14702-14707.
88. Weller JA, Levin IP, Shiv B, Bechara A, (2009) The effects of insula damage on decision-making for risky gains and losses. Soc Neurosci 4: 347-358.
89. Paulus MP, Rogalsky C, Simmons A, Feinstein JS, Stein MB, (2003) Increased activation in the right insula during risk-taking decision making is related to harm avoidance and neuroticism. Neuroimage 19: 1439-1448.
90. Kesner RP, Gilbert PE, (2007) The role of the agranular insular cortex in anticipation of reward contrast. Neurobiol Learn Mem 88: 82-86.
91. Cardinal RN, Parkinson JA, Hall J, Everitt BJ, (2003) The contribution of the amygdala, nucleus accumbens, and prefrontal cortex to emotion and motivated behaviour. International Congress Series 1250: 347-370.
92. Naqvi NH, Bechara A, (2009) The hidden island of addiction: the insula. Trends Neurosci 32: 56-67.
93. Xue G, Lu Z, Levin IP, Bechara A, (2010) The impact of prior risk experiences on subsequent risky decision-making: the role of the insula. Neuroimage 50: 709-716.
94. Contreras M, Ceric F, Torrealba F, (2007) Inactivation of the interoceptive insula disrupts drug craving and malaise induced by lithium. Science 318: 655-658.
95. Holmes A, Wellman CL, (2009) Stress-induced prefrontal reorganization and executive dysfunction in rodents. Neurosci Biobehav Rev 33: 773-783.
96. Lapiz-Bluhm MD, Bondi CO, Doyen J, Rodriguez GA, Bedard-Arana T, et al. (2008) Behavioural assays to model cognitive and affective dimensions of depression and anxiety in rats. J Neuroendocrinol 20: 1115-1137.
97. Liston C, Miller MM, Goldwater DS, Radley JJ, Rocher AB, et al. (2006) Stress-induced alterations in prefrontal cortical dendritic morphology predict selective impairments in perceptual attentional set-shifting. J Neurosci 26: 7870-7874.
98. Nagai M, Kishi K, Kato S, (2007) Insular cortex and neuropsychiatric disorders: a review of recent literature. Eur Psychiatry 22: 387-394.