Unstable Maternal Environment Affects Stress Response in Adult Mice in a Genotype-Dependent Manner

Cerebral Cortex

Volumn 26, Issue 11, 2016, Pages 4370-4380

  Di Segni, Matteo ^a,b   Andolina, Diego ^a,d   Luchetti, Alessandra ^e   Babicola, Lucy ^b   D'Apolito, Lina Ilaras ^c   Pascucci, Tiziana ^a,b   Conversi, David ^a,b   Accoto, Alessandra ^b   D'Amato, Francesca R ^e,f   Ventura, Rossella ^a,b  

^a IRCCS FONDAZIONE SANTA LUCIA   (Italy)

^b Department of Psychology and Daniel Bovet Center ^*  (Italy)

^c SAPIENZA UNIVERSITY OF ROME   (Italy)

^d UNIVERSITY OF L'AQUILA   (Italy)

^e CNR   (Italy)

^f UNIVERSITÉ LAVAL   (Canada)

Author keywords

anhedonia; dopamine; early environment; inbred strains; mice, prefrontal accumbal system; stress

Indexed keywords

CATECHOLAMINE; PROTEIN C FOS; DOPAMINE; NORADRENALIN;

ACUTE STRESS; ANIMAL EXPERIMENT; ARTICLE; BRAIN REGION; CONTROLLED STUDY; COPING BEHAVIOR; ENVIRONMENTAL STRESS; EXPERIMENTAL BEHAVIORAL TEST; FEMALE; FORCED SWIM TEST; GENOTYPE; IMMUNOHISTOCHEMISTRY; MATERNAL STRESS; MEDIAL PREFRONTAL CORTEX; MICRODIALYSIS; MOUSE; NONHUMAN; NUCLEUS ACCUMBENS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SACCHARINE PREFERENCE TEST; SEX DIFFERENCE; ANIMAL; C57BL MOUSE; DBA MOUSE; DISEASE MODEL; EXERCISE; FOOD PREFERENCE; GENETICS; MALE; MATERNAL BEHAVIOR; MENTAL STRESS; METABOLISM; NEWBORN; PATHOPHYSIOLOGY; PHYSIOLOGY; PREFRONTAL CORTEX; PSYCHOLOGY; RAT; SWIMMING;

ADAPTATION, PSYCHOLOGICAL; ANIMALS; ANIMALS, NEWBORN; DISEASE MODELS, ANIMAL; DOPAMINE; FEMALE; FOOD PREFERENCES; GENOTYPE; MALE; MATERNAL BEHAVIOR; MICE; MICE, INBRED C57BL; MICE, INBRED DBA; MICRODIALYSIS; NOREPINEPHRINE; PREFRONTAL CORTEX; PROTO-ONCOGENE PROTEINS C-FOS; RATS; RESTRAINT, PHYSICAL; STRESS, PSYCHOLOGICAL; SWIMMING;

EID: 84994627631     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhv204     Document Type: Article

References (75)

1. Aisa B, Elizalde N, Tordera R, Lasheras B, Del Río J, Ramírez MJ. 2009. Effects of neonatal stress on markers of synaptic plasticity in the hippocampus: implications for spatial memory. Hippocampus. 19:1222-1231.
2. Alcaro A, Cabib S, Ventura R, Puglisi-Allegra S. 2002. Genotype-and experience-dependent susceptibility to depressive-like responses in the forced-swimming test. Psychopharmacology (Berl). 164:138-143.
3. Andolina D, Maran D, Viscomi MT, Puglisi-Allegra S. 2014. Straindependent variations in stress coping behavior are mediated by a 5-HT/GABA interaction within the prefrontal corticolimbic system. Int J Neuropsychopharmacol. doi:10. 1093/ijnp/ pyu074.
4. Andolina D, Puglisi-Allegra S, Ventura R. 2015. Strain-dependent differences in corticolimbic processing of aversive or rewarding stimuli. Front Syst Neurosci. 8:207.
5. Arborelius L, Eklund MB. 2007. Both long and brief maternal separation produces persistent changes in tissue levels of brain monoamines in middle-aged female rats. Neurosci. 145:738-750.
6. Bale TL. 2006. Stress sensitivity and the development of affective disorders. Horm Behav. 50:529-533.
7. Barros VG, Berger MA, Martijena ID, Sarchi MI, Pérez AA, Molina VA, Tarazi FI, Antonelli MC. 2004. Early adoption modifies the effects of prenatal stress on dopamine and glutamate receptors in adult rat brain. J Neurosci Res. 76:488-496.
8. Becker JB, Monteggia LM, Perrot-Sinal TS, Romeo RD, Taylor JR, Yehuda R, Bale TL. 2007. Stress and disease: is being female a predisposing factor J Neurosci. 27:11851-11855.
9. Benes FM, Taylor JB, Cunningham MC. 2000. Convergence and plasticity of monoaminergic systems in the medial prefrontal cortex during the postnatal period: implications for the development of psychopathology. Cerb Cortex. 10:1014-1027.
10. Boccia ML, Razzoli M, Vadlamudi SP, Trumbull W, Caleffie C, Pedersen CA. 2007. Repeated long separations from pups produce depression-like behavior in rat mothers. Psychoneuroendocrinology. 32:65-71.
11. BrakeWG, Zhang TY, Diorio J, Meaney MJ, Gratton A. 2004. Influence of early postnatal rearing conditions on mesocorticolimbicdopamine and behavioural responses to psychostimulants and stressors in adult rats. Eur J Neurosci. 19:1863-1874.
12. Braun K, Lange E, Metzger M, Poeggel G. 2000. Maternal separation followed by early social deprivation affects the development of monoaminergic fiber systems in the medial prefrontal cortex of Octodon degus. Neurosci. 95:309-318.
13. Cabib S, Oliverio A, Ventura R, Lucchese F, Puglisi-Allegra S. 1997. Brain dopamine receptor plasticity: Testing a diathesis-stress hypothesis in an animal model. Psychopharmacology (Berl). 132:153-160.
14. Cabib S, Orsini C, Le Moal M, Piazza PV. 2000. Abolition and reversal of strain differences in behavioral responses to drugs of abuse after a brief experience. Science. 289:463-465.
15. Cabib S, Puglisi-Allegra S. 1991. Genotype-dependent effects of chronic stress on apomorphine-induced alterations of striatal and mesolimbic dopamine metabolism. Brain Res. 542:91-96.
16. Cabib S, Puglisi-Allegra S. 2012. The mesoaccumbens dopamine in coping with stress. Neurosci Biobehav Rev. 36:79-89.
17. Cabib S, Puglisi-Allegra S, Ventura R. 2002. The contribution of comparative studies in inbred strains of mice to the understanding of the hyperactive phenotype. Behav Brain Res. 130:103-109.
18. Caspi A, Moffitt TE. 2006. Gene-environment interactions in psychiatry: joining forces with neuroscience. Nat Rev Neurosci. 7:583-590.
19. Chandler DJ, Gao WJ, Waterhouse BD. 2014. Heterogeneous organization of the locus coeruleus projections to prefrontal and motor cortices. Proc Natl Acad Sci USA. 111:6816-6821.
20. Chandler DJ, Waterhouse BD, Gao WJ. 2014. New perspectives on catecholaminergic regulation of executive circuits: evidence for independent modulation of prefrontal functions by midbrain dopaminergic and noradrenergic neurons. Front Neural Circuits. 8:53.
21. Coccurello R, D'Amato FR, Moles A. 2009. Chronic social stress, hedonism and vulnerability to obesity: lessons from rodents. Neurosi Biobehav Rev. 33:537-550.
22. Conversi D, Orsini C, Cabib S. 2004. Distinct patterns of Fos expression induced by systemic amphetamine in the striatal complex of C57BL/6JICo and DBA/2JICo inbred strains of mice. Brain Res. 1025:59-66.
23. Crawley JN, Belknap JK, Collins A, Crabbe JC, Frankel W, Henderson N, Hitzemann RJ, Maxson SC, Miner LL, Silva AJ, et al. 1997. Behavioral phenotypes of inbred mouse strains: implications and recommendations for molecular studies. Psychopharmacology (Berl). 132:107-124.
24. D'Amato FR, Zanettini C, Lampis V, Coccurello R, Pascucci T, Ventura R, Puglisi-Allegra S, Spatola CA, Pesenti-Gritti P, Oddi D, et al. 2011. Unstable maternal environment, separation anxiety, and heightened CO2 sensitivity induced by gene-by-environment interplay. PLoS One. 6:e18637.
25. Dayan P, Yu AJ. 2006. Phasic norepinephrine: A neural interrupt signal for unexpected events. Network. 17:335-350.
26. Der-Avakian A, Markou A. 2010. Neonatal maternal separation exacerbates the reward-enhancing effect of acute amphetamine administration and the anhedonic effect of repeated social defeat in adult rats. Neuroscience. 170:1189-1198.
27. Di Chiara G, Tanda G, Frau R, Carboni E. 1993. On the preferential release of dopamine in the nucleus accumbens by amphetamine: further evidence obtained by vertically implanted concentric dialysis probes. Psychopharmacology (Berlin). 112:398-402.
28. Doya K. 2008. Modulators of decision making. Nat Neurosci. 11:410-416.
29. Feenstra MG, Botterblom MH, Mastenbroek S. 2000. Dopamine and noradrenaline efflux in the prefrontal cortex in the light and dark period: effects of novelty and handling and comparison to the nucleus accumbens. Neuroscience. 100:741-748.
30. Finlay JM, Zigmond MJ, Abercrombie ED. 1995. Increased dopamine and norepinephrine release in medial prefrontal cortex induced by acute and chronic stress: effects of diazepam. Neuroscience. 64:619-628.
31. Franklin KBJ, Paxinos G. 1997. The mouse brain: in stereotaxic coordinates. San Diego: Academic.
32. Franklin TB, Saab BJ, Mansuy IM. 2012. Neural mechanisms of stress resilience and vulnerability. Neuron. 75:747-761.
33. 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.
34. Heim C, Nemeroff CB. 2002. Neurobiology of early life stress: clinical studies. Sem Clin Neuropsychiatry. 7:147-159.
35. Huppertz-Kessler CJ, Poeschl J, Hertel R, Unsicker K, Schenkel J. 2012. Effects of a newpostnatal stress model on monoaminergic neurotransmitters in rat brains. Brain Dev. 34:274-279.
36. Jahng JW, Ryu V, Yoo SB, Noh SJ, Kim JY, Lee JH. 2010. Mesolimbic dopaminergic activity responding to acute stress is blunted in adolescent rats that experienced neonatal maternal separation. Neuroscience. 171:144-152.
37. Jezierski G, Zehle S, Bock J, Braun K, Gruss M. 2007. Early stress and chronic methylphenidate cross-sensitize dopaminergic responses in the adolescent medial prefrontal cortex and nucleus accumbens. J Neurochem. 103:2234-2244.
38. Kember RL, Dempster EL, Lee TH, Schalkwyk LC, Mill J, Fernandes C. 2012. Maternal separation is associated with strain-specific responses to stress and epigenetic alterations to Nr3c1, Avp, and Nr4a1 in mouse. Brain Behav. 2:455-467.
39. Kikusui T, Mori Y. 2009. Behavioural and neurochemical consequences of early weaning in rodents. J Neuroendocrinol. 21:427-431.
40. Korosi A, Naninck EF, Oomen CA, Schouten M, Krugers H, Fitzsimons C, Lucassen PJ. 2011. Early-life stress mediated modulation of adult neurogenesis and behavior. Behav Brain Res. 227:400-409.
41. Latagliata EC, Valzania A, Pascucci T, Campus P, Cabib S, Puglisi-Allegra S. 2014. Stress-induced activation of ventral tegmental mu-opioid receptors reduces accumbens dopamine tone by enhancing dopamine transmission in the medial pre-frontal cortex. Psychopharmacology (Berl). 231:4099-4108.
42. Lupien SJ, McEwen BS, Gunnar MR, Heim C. 2009. Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nat Rev Neurosci. 10:434-445.
43. Maccari S, Krugers HJ, Morley-Fletcher S, Szyf M, Brunton PJ. 2014. The consequences of early-life adversity: neurobiological, behavioural and epigenetic adaptations. J Neuroendocrinol. 26:707-723.
44. McClelland S, Korosi A, Cope J, Ivy A, Baram TZ. 2011. Emerging roles of epigenetic mechanisms in the enduring effects of early-life stress and experience on learning and memory. Neurobiol Learn Mem. 96:79-88.
45. McQuade R, Creton D, Stanford SC. 1999. Effect of novel environmental stimuli onrat behaviour and centralnoradrenaline function measured by in vivo microdialysis. Psychopharmacology. 145:393-400.
46. Meaney MJ. 2001. Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Annu Rev Neurosci. 24:1161-1192.
47. Meaney MJ, Brake W, Gratton A. 2002. Environmental regulation of the development of mesolimbic dopamine systems: A neurobiological mechanism for vulnerability to drug abuse Psychoneuroendocrinology. 27:127-138.
48. Mintz M, Ruedi-Bettschen D, Feldon J, Pryce CR. 2005. Early social and physical deprivation leads to reduced social motivation in adulthood in Wistar rats. Behav Brain Res. 156:311-320.
49. Nestler EJ, Barrot M, Di Leone RJ, Eisch AJ, Gold SJ, Monteggia LM. 2002. Neurobiology of depression. Neuron. 34:13-25.
50. Oswald LM, Wand GS, Kuwabara H, Wong DF, Zhu S, Brasic JR. 2014. History of childhood adversity is positively associated with ventral striatal dopamine responses to amphetamine. Psychopharmacology (Berl). 231:2417-2433.
51. Pascual R, Zamora-León SP. 2007. Effects of neonatal maternal deprivation and postweaning environmental complexity on dendritic morphology of prefrontal pyramidal neurons in the rat. Acta Neurobiol Exp. 67:471-479.
52. Pascucci T, AndolinaD, Mela IL, Conversi D, Latagliata C, Ventura R, Puglisi-Allegra S, Cabib S. 2009. 5-Hydroxytryptophan rescues serotonin response to stress in prefrontal cortex of hyperphenylalaninaemic mice. Int J Neuropsychopharmacol. 12: 1067-1079.
53. Pascucci T, Ventura R, Latagliata EC, Cabib S, Puglisi-Allegra S. 2007. The medial prefrontal cortex determines the accumbens dopamine response to stress through the opposing influences of norepinephrine and dopamine. Cereb Cortex. 17:2796-2804.
54. Peña CJ, Neugut YD, Calarco CA, Champagne FA. 2014. Effects of maternal care on the development of midbrain dopamine pathways and reward-directed behavior in female offspring. Eur J Neurosci. 39:946-956.
55. Petrill SA, Bartlett CW, Blair C. 2013. Gene-environment interplay in child psychology and psychiatry-challenges and ways forward. J Child Psychol Psychiatry. 54:1029.
56. Pryce CR, Ruedi-Bettschen D, Dettling AC, Weston A, Russig H, Ferger B, Feldon J. 2005. Long-term effects of early-life environmental manipulations in rodents and primates: potential animal models in depression research. Neurosci Biobehav Rev. 29:649-674.
57. Puglisi-Allegra S, Ventura R. 2012. Prefrontal/accumbal catecholamine system processes emotionally driven attribution of motivational salience. Rev Neurosci. 23:509-526.
58. Rana S, Pugh PC, Jackson N, Clinton SM, Kerman IA. 2015. Inborn stress reactivity shapes adult behavioral consequences of early-life maternal separation stress. Neurosci Lett. 584:146-150.
59. Rincón-Cortés M, Sullivan RM. 2014. Early life trauma and attachment: immediate and enduring effects on neurobehavioral and stress axis development. Front Endocrinol (Lausanne). 5:33.
60. Rivarola MA, Suárez MM. 2009. Early maternal separation and chronic variable stress in adulthood changes the neural activity and the expression of glucocorticoid receptor in limbic structures. Int J Dev Neurosci. 27:567-574.
61. Rodrigues AJ, Leão P, Carvalho M, Almeida OFX, Sousa N. 2011. Potential programming of dopaminergic circuits by early life stress. Psychopharmacology. 214:107-120.
62. Rutter M, Moffitt TE, Caspi A. 2006. Gene-environment interplay and psychopathology: multiple varieties but real effects. J Child Psychol Psychiatry 47:226-261.
63. Sánchez 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.
64. Sara SJ, Bouret S. 2012. Orienting and reorienting: The locus coeruleus mediates cognition through arousal. Neuron Rev. 76:130-141.
65. Spinelli S, Chefer S, Suomi SJ, Higley JD, Barr CS, Stein E. 2009. Early life stress induces long-term morphologic changes in primate brain. Arch Gen Psychiatry. 66:658-665.
66. Suri D, Teixeira CM, Cagliostro MK, Mahadevia D, Ansorge MS. 2015. Monoamine-sensitive developmental periods impacting adult emotional and cognitive behaviors. Neuropsychopharmacology. 40:88-112.
67. Teicher MH, Andersen SL, Polcari A, Anderson CM, Navalta CP, Kim DM. 2003. The neurobiological consequences of early stress and childhood maltreatment. Neurosci Biobehav Rev. 27:33-44.
68. van der Veen R, Koehl M, Abrous DN, de Kloet ER, Piazza PV, Deroche-Gamonet V. 2008. Maternal environment influences cocaine intake in adulthood in a genotype-dependent manner. PLoS One. 3:e2245.
69. Ventura R, Cabib S, Puglisi-Allegra S. 2001. Opposite genotype-dependent mesocorticolimbic dopamine response to stress. Neuroscience. 104:627-631.
70. Ventura R, Cabib S, Puglisi-Allegra S. 2002. Genetic susceptibility of mesocortical dopamine to stress determines liability to inhibition of mesoaccumbens dopamine and to behavioral 'despair' in a mouse model of depression. Neuroscience. 115:999-1007.
71. Ventura R, Coccurello R, Andolina D, Latagliata EC, Zanettini C, Lampis V, Battaglia M, D'Amato FR, Moles A. 2013. Postnatal aversive experience impairs sensitivity to natural rewards and increases susceptibility to negative events in adult life. Cereb Cortex. 23:1606-1617.
72. Ventura R, Latagliata EC, Morrone C, La Mela I, Puglisi-Allegra S. 2008. Prefrontal norepinephrine determines attribution of "high" motivational salience. PLoS One. 22:e3044.
73. Ventura R, Morrone C, Puglisi-Allegra S. 2007. Prefrontal/accumbal catecholamine system determines motivational salience attribution to both reward-and aversion-related stimuli. Proc Natl Acad Sci USA. 104:5181-5186.
74. Wise RA. 2008. Dopamine and reward: The anhedonia hypothesis 30 years on. Neurotox Res. 14:169-183.
75. Yang XD, Liao XM, Uribe-Mariño A, Liu R, Xie XM, Jia J, Su YA, Li JT, SchmidtMV, Wang XD, et al. 2014. Stress during a critical postnatal period induces region-specific structural abnormalities and dysfunction of the prefrontal cortex via CRF1. Neuropsychopharmacology. doi:10. 1038/npp. 2014. 304.