Social isolation-induced increase in NMDA receptors in the hippocampus exacerbates emotional dysregulation in mice

ABSTRACT Epidemiological studies have shown that early life adverse events have long‐term effects on the susceptibility to subsequent stress exposure in adolescence, but the precise mechanism is unclear. In the present study, mice on postnatal day 21–28 were randomly assigned to either a group or is...

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Published inHippocampus Vol. 25; no. 4; pp. 474 - 485
Main Authors Chang, Chih-Hua, Hsiao, Ya-Hsin, Chen, Yu-Wen, Yu, Yang-Jung, Gean, Po-Wu
Format Journal Article
LanguageEnglish
Published United States Blackwell Publishing Ltd 01.04.2015
Wiley Subscription Services, Inc
Subjects
acute stress
Affective Symptoms - etiology
Affective Symptoms - pathology
aggression
Aggression - physiology
Animals
Animals, Newborn
depression
Dizocilpine Maleate - pharmacology
Excitatory Amino Acid Antagonists - pharmacology
Excitatory Postsynaptic Potentials - drug effects
Exploratory Behavior - physiology
Gene Expression Regulation - physiology
Hippocampus - cytology
Hippocampus - metabolism
Male
Membrane Potentials - drug effects
Membrane Potentials - physiology
Mice
Mice, Inbred C57BL
Neurons - drug effects
Neurons - physiology
NMDA receptor
Piperidines - pharmacology
Prepulse Inhibition - drug effects
Prepulse Inhibition - physiology
Random Allocation
Receptors, N-Methyl-D-Aspartate - metabolism
Reflex, Startle - physiology
social isolation
Social Isolation - psychology
Swimming - psychology
Synaptosomes - drug effects
Synaptosomes - metabolism
social isolation
aggression
depression
NMDA receptor
acute stress
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Abstract ABSTRACT Epidemiological studies have shown that early life adverse events have long‐term effects on the susceptibility to subsequent stress exposure in adolescence, but the precise mechanism is unclear. In the present study, mice on postnatal day 21–28 were randomly assigned to either a group or isolated cages for 8 weeks. The socially isolated (SI) mice exhibited a higher level of spontaneous locomotor activity, a longer duration of immobility in the forced swimming test (FST), significantly less prepulse inhibition (PPI) and an increase in aggressive (but not attack) behavior. However, acute stress markedly exacerbated the attack counts of the SI mice but did not affect the group housing (GH) mice. SI mice exhibited higher synaptosomal NR2A and NR2B levels in the hippocampus as compared to the GH mice. Whole‐cell patch clamp recordings of CA1 neurons in hippocampal slices showed that the SI mice exhibited a higher input‐output relationship of NMDAR‐EPSCs as compared to the GH mice. Application of the NR2B‐specific antagonist ifenprodil produced a greater attenuating effect on NMDAR‐EPSCs in slices from the SI mice. NMDAR EPSCs recorded from the SI mice had a slower deactivation kinetic. MK‐801, CPP and ifenprodil, the NMDA antagonists, reversed acute stress‐induced exaggeration of aggressive and depressive behaviors. Furthermore, acute stress‐induced exacerbation of attack behavior in the SI mice was abolished after the knockdown of NR2B expression. These results suggest that social isolation‐induced increased expression of NMDA receptors in the hippocampus involves stress exacerbation of aggressive behaviors. Amelioration of aggressive behaviors by NMDA antagonists may open a new avenue for the treatment of psychopathologies that involve outbursts of emotional aggression in neglected children. © 2014 Wiley Periodicals, Inc.
AbstractList Epidemiological studies have shown that early life adverse events have long‐term effects on the susceptibility to subsequent stress exposure in adolescence, but the precise mechanism is unclear. In the present study, mice on postnatal day 21–28 were randomly assigned to either a group or isolated cages for 8 weeks. The socially isolated (SI) mice exhibited a higher level of spontaneous locomotor activity, a longer duration of immobility in the forced swimming test (FST), significantly less prepulse inhibition (PPI) and an increase in aggressive (but not attack) behavior. However, acute stress markedly exacerbated the attack counts of the SI mice but did not affect the group housing (GH) mice. SI mice exhibited higher synaptosomal NR 2A and NR 2B levels in the hippocampus as compared to the GH mice. Whole‐cell patch clamp recordings of CA1 neurons in hippocampal slices showed that the SI mice exhibited a higher input‐output relationship of NMDAR‐EPSCs as compared to the GH mice. Application of the NR 2B ‐specific antagonist ifenprodil produced a greater attenuating effect on NMDAR‐EPSCs in slices from the SI mice. NMDAR EPSCs recorded from the SI mice had a slower deactivation kinetic. MK‐801, CPP and ifenprodil, the NMDA antagonists, reversed acute stress‐induced exaggeration of aggressive and depressive behaviors. Furthermore, acute stress‐induced exacerbation of attack behavior in the SI mice was abolished after the knockdown of NR 2B expression. These results suggest that social isolation‐induced increased expression of NMDA receptors in the hippocampus involves stress exacerbation of aggressive behaviors. Amelioration of aggressive behaviors by NMDA antagonists may open a new avenue for the treatment of psychopathologies that involve outbursts of emotional aggression in neglected children. © 2014 Wiley Periodicals, Inc.
Epidemiological studies have shown that early life adverse events have long-term effects on the susceptibility to subsequent stress exposure in adolescence, but the precise mechanism is unclear. In the present study, mice on postnatal day 21-28 were randomly assigned to either a group or isolated cages for 8 weeks. The socially isolated (SI) mice exhibited a higher level of spontaneous locomotor activity, a longer duration of immobility in the forced swimming test (FST), significantly less prepulse inhibition (PPI) and an increase in aggressive (but not attack) behavior. However, acute stress markedly exacerbated the attack counts of the SI mice but did not affect the group housing (GH) mice. SI mice exhibited higher synaptosomal NR2A and NR2B levels in the hippocampus as compared to the GH mice. Whole-cell patch clamp recordings of CA1 neurons in hippocampal slices showed that the SI mice exhibited a higher input-output relationship of NMDAR-EPSCs as compared to the GH mice. Application of the NR2B-specific antagonist ifenprodil produced a greater attenuating effect on NMDAR-EPSCs in slices from the SI mice. NMDAR EPSCs recorded from the SI mice had a slower deactivation kinetic. MK-801, CPP and ifenprodil, the NMDA antagonists, reversed acute stress-induced exaggeration of aggressive and depressive behaviors. Furthermore, acute stress-induced exacerbation of attack behavior in the SI mice was abolished after the knockdown of NR2B expression. These results suggest that social isolation-induced increased expression of NMDA receptors in the hippocampus involves stress exacerbation of aggressive behaviors. Amelioration of aggressive behaviors by NMDA antagonists may open a new avenue for the treatment of psychopathologies that involve outbursts of emotional aggression in neglected children. © 2014 Wiley Periodicals, Inc.
ABSTRACT Epidemiological studies have shown that early life adverse events have long‐term effects on the susceptibility to subsequent stress exposure in adolescence, but the precise mechanism is unclear. In the present study, mice on postnatal day 21–28 were randomly assigned to either a group or isolated cages for 8 weeks. The socially isolated (SI) mice exhibited a higher level of spontaneous locomotor activity, a longer duration of immobility in the forced swimming test (FST), significantly less prepulse inhibition (PPI) and an increase in aggressive (but not attack) behavior. However, acute stress markedly exacerbated the attack counts of the SI mice but did not affect the group housing (GH) mice. SI mice exhibited higher synaptosomal NR2A and NR2B levels in the hippocampus as compared to the GH mice. Whole‐cell patch clamp recordings of CA1 neurons in hippocampal slices showed that the SI mice exhibited a higher input‐output relationship of NMDAR‐EPSCs as compared to the GH mice. Application of the NR2B‐specific antagonist ifenprodil produced a greater attenuating effect on NMDAR‐EPSCs in slices from the SI mice. NMDAR EPSCs recorded from the SI mice had a slower deactivation kinetic. MK‐801, CPP and ifenprodil, the NMDA antagonists, reversed acute stress‐induced exaggeration of aggressive and depressive behaviors. Furthermore, acute stress‐induced exacerbation of attack behavior in the SI mice was abolished after the knockdown of NR2B expression. These results suggest that social isolation‐induced increased expression of NMDA receptors in the hippocampus involves stress exacerbation of aggressive behaviors. Amelioration of aggressive behaviors by NMDA antagonists may open a new avenue for the treatment of psychopathologies that involve outbursts of emotional aggression in neglected children. © 2014 Wiley Periodicals, Inc.
Epidemiological studies have shown that early life adverse events have long-term effects on the susceptibility to subsequent stress exposure in adolescence, but the precise mechanism is unclear. In the present study, mice on postnatal day 21-28 were randomly assigned to either a group or isolated cages for 8 weeks. The socially isolated (SI) mice exhibited a higher level of spontaneous locomotor activity, a longer duration of immobility in the forced swimming test (FST), significantly less prepulse inhibition (PPI) and an increase in aggressive (but not attack) behavior. However, acute stress markedly exacerbated the attack counts of the SI mice but did not affect the group housing (GH) mice. SI mice exhibited higher synaptosomal NR2A and NR2B levels in the hippocampus as compared to the GH mice. Whole-cell patch clamp recordings of CA1 neurons in hippocampal slices showed that the SI mice exhibited a higher input-output relationship of NMDAR-EPSCs as compared to the GH mice. Application of the NR2B -specific antagonist ifenprodil produced a greater attenuating effect on NMDAR-EPSCs in slices from the SI mice. NMDAR EPSCs recorded from the SI mice had a slower deactivation kinetic. MK-801, CPP and ifenprodil, the NMDA antagonists, reversed acute stress-induced exaggeration of aggressive and depressive behaviors. Furthermore, acute stress-induced exacerbation of attack behavior in the SI mice was abolished after the knockdown of NR2B expression. These results suggest that social isolation-induced increased expression of NMDA receptors in the hippocampus involves stress exacerbation of aggressive behaviors. Amelioration of aggressive behaviors by NMDA antagonists may open a new avenue for the treatment of psychopathologies that involve outbursts of emotional aggression in neglected children.Epidemiological studies have shown that early life adverse events have long-term effects on the susceptibility to subsequent stress exposure in adolescence, but the precise mechanism is unclear. In the present study, mice on postnatal day 21-28 were randomly assigned to either a group or isolated cages for 8 weeks. The socially isolated (SI) mice exhibited a higher level of spontaneous locomotor activity, a longer duration of immobility in the forced swimming test (FST), significantly less prepulse inhibition (PPI) and an increase in aggressive (but not attack) behavior. However, acute stress markedly exacerbated the attack counts of the SI mice but did not affect the group housing (GH) mice. SI mice exhibited higher synaptosomal NR2A and NR2B levels in the hippocampus as compared to the GH mice. Whole-cell patch clamp recordings of CA1 neurons in hippocampal slices showed that the SI mice exhibited a higher input-output relationship of NMDAR-EPSCs as compared to the GH mice. Application of the NR2B -specific antagonist ifenprodil produced a greater attenuating effect on NMDAR-EPSCs in slices from the SI mice. NMDAR EPSCs recorded from the SI mice had a slower deactivation kinetic. MK-801, CPP and ifenprodil, the NMDA antagonists, reversed acute stress-induced exaggeration of aggressive and depressive behaviors. Furthermore, acute stress-induced exacerbation of attack behavior in the SI mice was abolished after the knockdown of NR2B expression. These results suggest that social isolation-induced increased expression of NMDA receptors in the hippocampus involves stress exacerbation of aggressive behaviors. Amelioration of aggressive behaviors by NMDA antagonists may open a new avenue for the treatment of psychopathologies that involve outbursts of emotional aggression in neglected children.
Epidemiological studies have shown that early life adverse events have long-term effects on the susceptibility to subsequent stress exposure in adolescence, but the precise mechanism is unclear. In the present study, mice on postnatal day 21-28 were randomly assigned to either a group or isolated cages for 8 weeks. The socially isolated (SI) mice exhibited a higher level of spontaneous locomotor activity, a longer duration of immobility in the forced swimming test (FST), significantly less prepulse inhibition (PPI) and an increase in aggressive (but not attack) behavior. However, acute stress markedly exacerbated the attack counts of the SI mice but did not affect the group housing (GH) mice. SI mice exhibited higher synaptosomal NR2A and NR2B levels in the hippocampus as compared to the GH mice. Whole-cell patch clamp recordings of CA1 neurons in hippocampal slices showed that the SI mice exhibited a higher input-output relationship of NMDAR-EPSCs as compared to the GH mice. Application of the NR2B -specific antagonist ifenprodil produced a greater attenuating effect on NMDAR-EPSCs in slices from the SI mice. NMDAR EPSCs recorded from the SI mice had a slower deactivation kinetic. MK-801, CPP and ifenprodil, the NMDA antagonists, reversed acute stress-induced exaggeration of aggressive and depressive behaviors. Furthermore, acute stress-induced exacerbation of attack behavior in the SI mice was abolished after the knockdown of NR2B expression. These results suggest that social isolation-induced increased expression of NMDA receptors in the hippocampus involves stress exacerbation of aggressive behaviors. Amelioration of aggressive behaviors by NMDA antagonists may open a new avenue for the treatment of psychopathologies that involve outbursts of emotional aggression in neglected children.
Epidemiological studies have shown that early life adverse events have long-term effects on the susceptibility to subsequent stress exposure in adolescence, but the precise mechanism is unclear. In the present study, mice on postnatal day 21-28 were randomly assigned to either a group or isolated cages for 8 weeks. The socially isolated (SI) mice exhibited a higher level of spontaneous locomotor activity, a longer duration of immobility in the forced swimming test (FST), significantly less prepulse inhibition (PPI) and an increase in aggressive (but not attack) behavior. However, acute stress markedly exacerbated the attack counts of the SI mice but did not affect the group housing (GH) mice. SI mice exhibited higher synaptosomal NR sub(2A) and NR sub(2B) levels in the hippocampus as compared to the GH mice. Whole-cell patch clamp recordings of CA1 neurons in hippocampal slices showed that the SI mice exhibited a higher input-output relationship of NMDAR-EPSCs as compared to the GH mice. Application of the NR sub(2B)-specific antagonist ifenprodil produced a greater attenuating effect on NMDAR-EPSCs in slices from the SI mice. NMDAR EPSCs recorded from the SI mice had a slower deactivation kinetic. MK-801, CPP and ifenprodil, the NMDA antagonists, reversed acute stress-induced exaggeration of aggressive and depressive behaviors. Furthermore, acute stress-induced exacerbation of attack behavior in the SI mice was abolished after the knockdown of NR sub(2B) expression. These results suggest that social isolation-induced increased expression of NMDA receptors in the hippocampus involves stress exacerbation of aggressive behaviors. Amelioration of aggressive behaviors by NMDA antagonists may open a new avenue for the treatment of psychopathologies that involve outbursts of emotional aggression in neglected children. copyright 2014 Wiley Periodicals, Inc.
Author Chen, Yu-Wen
Chang, Chih-Hua
Hsiao, Ya-Hsin
Gean, Po-Wu
Yu, Yang-Jung
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  surname: Chang
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  surname: Hsiao
  fullname: Hsiao, Ya-Hsin
  organization: Department of Pharmacology, College of Medicine, National Cheng Kung University, Tainan, Taiwan
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  surname: Chen
  fullname: Chen, Yu-Wen
  organization: Department of Pharmacology, College of Medicine, National Cheng Kung University, Tainan, Taiwan
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  givenname: Yang-Jung
  surname: Yu
  fullname: Yu, Yang-Jung
  organization: Institute of Basic Medical Science, National Cheng Kung University, Tainan, Taiwan
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  givenname: Po-Wu
  surname: Gean
  fullname: Gean, Po-Wu
  email: powu@mail.ncku.edu.tw
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/25348768$$D View this record in MEDLINE/PubMed
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Issue 4
Keywords social isolation
aggression
depression
NMDA receptor
acute stress
Language English
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PublicationTitle Hippocampus
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References Heinz AJ, Beck A, Meyer-Lindenberg A, Sterzer P, Heinz A. 2011. Cognitive and neurobiological mechanisms of alcohol-related aggression. Nat Rev Neurosci 12:400-413.
Lin D, Boyle MP, Dollar P, Lee H, Lein ES, Perona P, Anderson DJ. 2011. Functional identification of an aggression locus in the mouse hypothalamus. Nature 470:221-226.
Cossenza M, Cadilhe DV, Coutinho RN, Paes-de-Carvalho R. 2006. Inhibition of protein synthesis by activation of NMDA receptors in cultured retinal cells: A new mechanism for the regulation of nitric oxide production. J Neurochem 97(5):1481-93.
Ho JM, Murray JH, Demas GE, Goodson JL. 2010. Vasopressin cell groups exhibit strongly divergent responses to copulation and male-male interactions in mice. Horm Behav 58:368-377.
Von Frijtag JC, Schot M, van den Bos R, Spruijt BM. 2002. Individual housing during the play period results in changed responses to and consequences of a psychosocial stress situation in rats. Dev Psychobiol 41:58-69.
Bibancos T, Jardim DL, Aneas I, Chiavegatto S. 2007. Social isolation and expression of serotonergic neurotransmission-related genes in several brain areas of male mice. Genes Brain Behav 6:529-539.
Naert A, Callaerts-Vegh Z, D'Hooge R. 2011. Nocturnal hyperactivity, increased social novelty preference and delayed extinction of fear responses in post-weaning socially isolated mice. Brain Res Bull 85:354-362.
Surget A, Tanti A, Leonardo ED, Laugeray A, Rainer Q, Touma C, Palme R, Griebel G, Ibarguen-Vargas Y, Hen R, Belzung C. 2011. Antidepressants recruit new neurons to improve stress response regulation. Mol Psychiatry 16:1177-1188.
Geyer MA, Dulawa SC. 2003. Assessment of murine startle reactivity, prepulse inhibition, and habituation. Curr Protoc Neurosci Chapter 8:Unit 8.17.
Goosens KA. 2011. Hippocampal regulation of aversive memories. Curr Opin Neurobiol 21:460-466.
Bartolomucci A, Palanza P, Sacerdote P, Panerai AE, Sgoifo A, Dantzer R, Parmigiani S. 2005. Social factors and individual vulnerability to chronic stress exposure. Neurosci Biobehav Rev 29:67-81.
Davidson RJ, McEwen BS. 2012. Social influences on neuroplasticity: Stress and interventions to promote well-being. Nat Neurosci 15:689-695.
Workman JL, Fonken LK, Gusfa J, Kassouf KM, Nelson RJ. 2011. Post-weaning environmental enrichment alters affective responses and interacts with behavioral testing to alter nNOS immunoreactivity. Pharmacol Biochem Behav 100:25-32.
Belozertseva IV, Bespalov AY. 1999. Effects of NMDA receptor channel blockade on aggression in isolated male mice. Aggressive Behav 25:381-396.
Papolos DF, Teicher MH, Faedda GL, Murphy P, Mattis S. 2013. Clinical experience using intranasal ketamine in the treatment of pediatric bipolar disorder/fear of harm phenotype. J Affect Disord 147:431-436.
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.
Carrillo M, Ricci LA, Coppersmith GA, Melloni RH Jr. 2009. The effect of increased serotonergic neurotransmission on aggression: A critical meta-analytical review of preclinical studies. Psychopharmacology (Berl) 205:349-368.
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.
Magarinos AM, Li CJ, Gal Toth J, Bath KG, Jing D, Lee FS, McEwen BS. 2011. Effect of brain-derived neurotrophic factor haploinsufficiency on stress-induced remodeling of hippocampal neurons. Hippocampus 21:253-264.
Li Y, Luikart BW, Birnbaum S, Chen J, Kwon CH, Kernie SG, Bassel-Duby R, Parada LF. 2008. TrkB regulates hippocampal neurogenesis and governs sensitivity to antidepressive treatment. Neuron 59:399-412.
Popoli M, Yan Z, McEwen BS, Sanacora G. 2012. The stressed synapse: The impact of stress and glucocorticoids on glutamate transmission. Nat Rev Neurosci 13:22-37.
Lewis DO. 1992. From abuse to violence: Psychophysiological consequences of maltreatment. J Am Acad Child Adolesc Psychiatry 31:383-391.
Cull-Candy SG, Leszkiewicz DN. 2004. Role of distinct NMDA receptor subtypes at central synapses. Sci STKE 2004:re16.
Sahay A, Hen R. 2007. Adult hippocampal neurogenesis in depression. Nat Neurosci 10:1110-1105.
Duman RS, Li N, Liu RJ, Duric V, Aghajanian G. 2012. Signaling pathways underlying the rapid antidepressant actions of ketamine. Neuropharmacology 62:35-41.
Adachi M, Barrot M, Autry AE, Theobald D, Monteggia LM. 2008. Selective loss of brain-derived neurotrophic factor in the dentate gyrus attenuates antidepressant efficacy. Biol Psychiatry 63:642-649.
Hildyard KL, Wolfe DA. 2002. Child neglect: Developmental issues and outcomes. Child Abuse Negl 26:679-695.
Newman EL, Chu A, Bahamon B, Takahashi A, Debold JF, Miczek KA. 2012. NMDA receptor antagonism: Escalation of aggressive behavior in alcohol-drinking mice. Psychopharmacology (Berl) 224:167-77.
Rodenas-Ruano A, Chavez AE, Cossio MJ, Castillo PE, Zukin RS. 2012. REST-dependent epigenetic remodeling promotes the developmental switch in synaptic NMDA receptors. Nat Neurosci 15:1382-1390.
Springer KW, Sheridan J, Kuo D, Carnes M. 2007. Long-term physical and mental health consequences of childhood physical abuse: Results from a large population-based sample of men and women. Child Abuse Negl 31:517-530.
Herman JP, Ostrander MM, Mueller NK, Figueiredo H. 2005. Limbic system mechanisms of stress regulation: Hypothalamo-pituitary-adrenocortical axis. Prog Neuropsychopharmacol Biol Psychiatry 29:1201-1213.
Fonagy P. 2004. Early-life trauma and the psychogenesis and prevention of violence. Ann N Y Acad Sci 1036:181-200.
Luecken LJ, Lemery KS. 2004. Early caregiving and physiological stress responses. Clin Psychol Rev 24:171-191.
Samuels BA, Hsueh YP, Shu T, Liang H, Tseng HC, Hong CJ, Su SC, Volker J, Neve RL, Yue DT, Tsai LH. 2007. Cdk5 promotes synaptogenesis by regulating the subcellular distribution of the MAGUK family member CASK. Neuron 56:823-837.
van den Berg CL, Hol T, Van Ree JM, Spruijt BM, Everts H, Koolhaas JM. 1999. Play is indispensable for an adequate development of coping with social challenges in the rat. Dev Psychobiol 34:129-138.
Silva-Gomez AB, Rojas D, Juarez I, Flores G. 2003. Decreased dendritic spine density on prefrontal cortical and hippocampal pyramidal neurons in postweaning social isolation rats. Brain Res 983:128-136.
Petit-Demouliere B, Chenu F, Bourin M. 2005. Forced swimming test in mice: A review of antidepressant activity. Psychopharmacology (Berl) 177:245-255.
Autry AE, Adachi M, Nosyreva E, Na ES, Los MF, Cheng PF, Kavalali ET, Monteggia LM. 2011. NMDA receptor blockade at rest triggers rapid behavioural antidepressant responses. Nature 475:91-95.
Zhao X, Sun L, Jia H, Meng Q, Wu S, Li N, He S. 2009. Isolation rearing induces social and emotional function abnormalities and alters glutamate and neurodevelopment-related gene expression in rats. Prog Neuropsychopharmacol Biol Psychiatry 33:1173-1177.
Fone KC, Porkess MV. 2008. Behavioural and neurochemical effects of post-weaning social isolation in rodents-relevance to developmental neuropsychiatric disorders. Neurosci Biobehav Rev 32:1087-1102.
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.
McCormick CM, Thomas CM, Sheridan CS, Nixon F, Flynn JA, Mathews IZ. 2012. Social instability stress in adolescent male rats alters hippocampal neurogenesis and produces deficits in spatial location memory in adulthood. Hippocampus 22:1300-1312.
Duman RS, Voleti B. 2012. Signaling pathways underlying the pathophysiology and treatment of depression: Novel mechanisms for rapid-acting agents. Trends Neurosci 35:47-56.
Loeber R, Stouthamer-Loeber M. 1998. Development of juvenile aggression and violence. Some common misconceptions and controversies. Am Psychol 53:242-259.
Toth M, Mikics E, Tulogdi A, Aliczki M, Haller J. 2011. Post-weaning social isolation induces abnormal forms of aggression in conjunction with increased glucocorticoid and autonomic stress responses. Horm Behav 60:28-36.
Christian KM, Miracle AD, Wellman CL, Nakazawa K. 2011. Chronic stress-induced hippocampal dendritic retraction requires CA3 NMDA receptors. Neuroscience 174:26-36.
Dranovsky A, Picchini AM, Moadel T, Sisti AC, Yamada A, Kimura S, Leonardo ED, Hen R. 2011. Experience dictates stem cell fate in the adult hippocampus. Neuron 70:908-923.
Ito W, Chehab M, Thakur S, Li J, Morozov A. 2011. BDNF-restricted knockout mice as an animal model for aggression. Genes Brain Behav 10:365-374.
Renault J, Aubert A. 2006. Immunity and emotions: Lipopolysaccharide increases defensive behaviours and potentiates despair in mice. Brain Behav Immun 20:517-526.
Ferris CF, Stolberg T, Kulkarni P, Murugavel M, Blanchard R, Blanchard DC, Febo M, Brevard M, Simon NG. 2008. Imaging the neural circuitry and chemical control of aggressive motivation. BMC Neurosci 9:111.
Nelson RJ, Trainor BC. 2007. Neural mechanisms of aggression. Nat Rev Neurosci 8:536-546.
Browne CA, Lucki I. 2013. Antidepressant effects of ketamine: Mechanisms underlying fast-acting novel antidepressants. Front Pharmacol 4:161.
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.
Dodge KA, Bates JE, Pettit GS. 1990. Mechanisms in the cycle of violence. Science 250:1678-1683.
Marino MD, Bourdelat-Parks BN, Cameron Liles L, Weinshenker D. 2005. Genetic reduction of noradrenergic function alters social memory and reduces aggression in mice. Behav Brain Res 161:197-203.
Hallett PJ, Collins TL, Standaert DG, Dunah AW. 2008. Biochemical fractionation of brain tissue for studies of receptor distribution and trafficking. Curr Protoc Neurosci Chapter 1:Unit 1.16.
2013; 4
2010; 58
2005; 177
2011; 60
2004; 24
2008; 9
2011; 10
2008; 32
2011; 12
2012; 15
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2007; 31
2011; 470
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2011; 475
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References_xml – reference: Belozertseva IV, Bespalov AY. 1999. Effects of NMDA receptor channel blockade on aggression in isolated male mice. Aggressive Behav 25:381-396.
– reference: Adachi M, Barrot M, Autry AE, Theobald D, Monteggia LM. 2008. Selective loss of brain-derived neurotrophic factor in the dentate gyrus attenuates antidepressant efficacy. Biol Psychiatry 63:642-649.
– reference: Ferris CF, Stolberg T, Kulkarni P, Murugavel M, Blanchard R, Blanchard DC, Febo M, Brevard M, Simon NG. 2008. Imaging the neural circuitry and chemical control of aggressive motivation. BMC Neurosci 9:111.
– reference: Bibancos T, Jardim DL, Aneas I, Chiavegatto S. 2007. Social isolation and expression of serotonergic neurotransmission-related genes in several brain areas of male mice. Genes Brain Behav 6:529-539.
– reference: 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.
– reference: Newman EL, Chu A, Bahamon B, Takahashi A, Debold JF, Miczek KA. 2012. NMDA receptor antagonism: Escalation of aggressive behavior in alcohol-drinking mice. Psychopharmacology (Berl) 224:167-77.
– reference: Naert A, Callaerts-Vegh Z, D'Hooge R. 2011. Nocturnal hyperactivity, increased social novelty preference and delayed extinction of fear responses in post-weaning socially isolated mice. Brain Res Bull 85:354-362.
– reference: Hildyard KL, Wolfe DA. 2002. Child neglect: Developmental issues and outcomes. Child Abuse Negl 26:679-695.
– reference: Fone KC, Porkess MV. 2008. Behavioural and neurochemical effects of post-weaning social isolation in rodents-relevance to developmental neuropsychiatric disorders. Neurosci Biobehav Rev 32:1087-1102.
– reference: Zhao X, Sun L, Jia H, Meng Q, Wu S, Li N, He S. 2009. Isolation rearing induces social and emotional function abnormalities and alters glutamate and neurodevelopment-related gene expression in rats. Prog Neuropsychopharmacol Biol Psychiatry 33:1173-1177.
– reference: Cull-Candy SG, Leszkiewicz DN. 2004. Role of distinct NMDA receptor subtypes at central synapses. Sci STKE 2004:re16.
– reference: Samuels BA, Hsueh YP, Shu T, Liang H, Tseng HC, Hong CJ, Su SC, Volker J, Neve RL, Yue DT, Tsai LH. 2007. Cdk5 promotes synaptogenesis by regulating the subcellular distribution of the MAGUK family member CASK. Neuron 56:823-837.
– reference: Von Frijtag JC, Schot M, van den Bos R, Spruijt BM. 2002. Individual housing during the play period results in changed responses to and consequences of a psychosocial stress situation in rats. Dev Psychobiol 41:58-69.
– reference: 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.
– reference: Sahay A, Hen R. 2007. Adult hippocampal neurogenesis in depression. Nat Neurosci 10:1110-1105.
– reference: Autry AE, Adachi M, Nosyreva E, Na ES, Los MF, Cheng PF, Kavalali ET, Monteggia LM. 2011. NMDA receptor blockade at rest triggers rapid behavioural antidepressant responses. Nature 475:91-95.
– reference: Springer KW, Sheridan J, Kuo D, Carnes M. 2007. Long-term physical and mental health consequences of childhood physical abuse: Results from a large population-based sample of men and women. Child Abuse Negl 31:517-530.
– reference: Heinz AJ, Beck A, Meyer-Lindenberg A, Sterzer P, Heinz A. 2011. Cognitive and neurobiological mechanisms of alcohol-related aggression. Nat Rev Neurosci 12:400-413.
– reference: 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.
– reference: Dodge KA, Bates JE, Pettit GS. 1990. Mechanisms in the cycle of violence. Science 250:1678-1683.
– reference: Marino MD, Bourdelat-Parks BN, Cameron Liles L, Weinshenker D. 2005. Genetic reduction of noradrenergic function alters social memory and reduces aggression in mice. Behav Brain Res 161:197-203.
– reference: Workman JL, Fonken LK, Gusfa J, Kassouf KM, Nelson RJ. 2011. Post-weaning environmental enrichment alters affective responses and interacts with behavioral testing to alter nNOS immunoreactivity. Pharmacol Biochem Behav 100:25-32.
– reference: Ho JM, Murray JH, Demas GE, Goodson JL. 2010. Vasopressin cell groups exhibit strongly divergent responses to copulation and male-male interactions in mice. Horm Behav 58:368-377.
– reference: McCormick CM, Thomas CM, Sheridan CS, Nixon F, Flynn JA, Mathews IZ. 2012. Social instability stress in adolescent male rats alters hippocampal neurogenesis and produces deficits in spatial location memory in adulthood. Hippocampus 22:1300-1312.
– reference: Luecken LJ, Lemery KS. 2004. Early caregiving and physiological stress responses. Clin Psychol Rev 24:171-191.
– reference: Cossenza M, Cadilhe DV, Coutinho RN, Paes-de-Carvalho R. 2006. Inhibition of protein synthesis by activation of NMDA receptors in cultured retinal cells: A new mechanism for the regulation of nitric oxide production. J Neurochem 97(5):1481-93.
– reference: Toth M, Mikics E, Tulogdi A, Aliczki M, Haller J. 2011. Post-weaning social isolation induces abnormal forms of aggression in conjunction with increased glucocorticoid and autonomic stress responses. Horm Behav 60:28-36.
– reference: Davidson RJ, McEwen BS. 2012. Social influences on neuroplasticity: Stress and interventions to promote well-being. Nat Neurosci 15:689-695.
– reference: Dranovsky A, Picchini AM, Moadel T, Sisti AC, Yamada A, Kimura S, Leonardo ED, Hen R. 2011. Experience dictates stem cell fate in the adult hippocampus. Neuron 70:908-923.
– reference: Lewis DO. 1992. From abuse to violence: Psychophysiological consequences of maltreatment. J Am Acad Child Adolesc Psychiatry 31:383-391.
– reference: Duman RS, Voleti B. 2012. Signaling pathways underlying the pathophysiology and treatment of depression: Novel mechanisms for rapid-acting agents. Trends Neurosci 35:47-56.
– reference: Rodenas-Ruano A, Chavez AE, Cossio MJ, Castillo PE, Zukin RS. 2012. REST-dependent epigenetic remodeling promotes the developmental switch in synaptic NMDA receptors. Nat Neurosci 15:1382-1390.
– reference: Browne CA, Lucki I. 2013. Antidepressant effects of ketamine: Mechanisms underlying fast-acting novel antidepressants. Front Pharmacol 4:161.
– reference: Christian KM, Miracle AD, Wellman CL, Nakazawa K. 2011. Chronic stress-induced hippocampal dendritic retraction requires CA3 NMDA receptors. Neuroscience 174:26-36.
– reference: Li Y, Luikart BW, Birnbaum S, Chen J, Kwon CH, Kernie SG, Bassel-Duby R, Parada LF. 2008. TrkB regulates hippocampal neurogenesis and governs sensitivity to antidepressive treatment. Neuron 59:399-412.
– reference: Lin D, Boyle MP, Dollar P, Lee H, Lein ES, Perona P, Anderson DJ. 2011. Functional identification of an aggression locus in the mouse hypothalamus. Nature 470:221-226.
– reference: Popoli M, Yan Z, McEwen BS, Sanacora G. 2012. The stressed synapse: The impact of stress and glucocorticoids on glutamate transmission. Nat Rev Neurosci 13:22-37.
– reference: Herman JP, Ostrander MM, Mueller NK, Figueiredo H. 2005. Limbic system mechanisms of stress regulation: Hypothalamo-pituitary-adrenocortical axis. Prog Neuropsychopharmacol Biol Psychiatry 29:1201-1213.
– reference: Petit-Demouliere B, Chenu F, Bourin M. 2005. Forced swimming test in mice: A review of antidepressant activity. Psychopharmacology (Berl) 177:245-255.
– reference: Duman RS, Li N, Liu RJ, Duric V, Aghajanian G. 2012. Signaling pathways underlying the rapid antidepressant actions of ketamine. Neuropharmacology 62:35-41.
– reference: Surget A, Tanti A, Leonardo ED, Laugeray A, Rainer Q, Touma C, Palme R, Griebel G, Ibarguen-Vargas Y, Hen R, Belzung C. 2011. Antidepressants recruit new neurons to improve stress response regulation. Mol Psychiatry 16:1177-1188.
– reference: Nelson RJ, Trainor BC. 2007. Neural mechanisms of aggression. Nat Rev Neurosci 8:536-546.
– reference: Silva-Gomez AB, Rojas D, Juarez I, Flores G. 2003. Decreased dendritic spine density on prefrontal cortical and hippocampal pyramidal neurons in postweaning social isolation rats. Brain Res 983:128-136.
– reference: Hallett PJ, Collins TL, Standaert DG, Dunah AW. 2008. Biochemical fractionation of brain tissue for studies of receptor distribution and trafficking. Curr Protoc Neurosci Chapter 1:Unit 1.16.
– reference: Papolos DF, Teicher MH, Faedda GL, Murphy P, Mattis S. 2013. Clinical experience using intranasal ketamine in the treatment of pediatric bipolar disorder/fear of harm phenotype. J Affect Disord 147:431-436.
– reference: Geyer MA, Dulawa SC. 2003. Assessment of murine startle reactivity, prepulse inhibition, and habituation. Curr Protoc Neurosci Chapter 8:Unit 8.17.
– reference: Goosens KA. 2011. Hippocampal regulation of aversive memories. Curr Opin Neurobiol 21:460-466.
– reference: van den Berg CL, Hol T, Van Ree JM, Spruijt BM, Everts H, Koolhaas JM. 1999. Play is indispensable for an adequate development of coping with social challenges in the rat. Dev Psychobiol 34:129-138.
– reference: 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.
– reference: Carrillo M, Ricci LA, Coppersmith GA, Melloni RH Jr. 2009. The effect of increased serotonergic neurotransmission on aggression: A critical meta-analytical review of preclinical studies. Psychopharmacology (Berl) 205:349-368.
– reference: Renault J, Aubert A. 2006. Immunity and emotions: Lipopolysaccharide increases defensive behaviours and potentiates despair in mice. Brain Behav Immun 20:517-526.
– reference: Fonagy P. 2004. Early-life trauma and the psychogenesis and prevention of violence. Ann N Y Acad Sci 1036:181-200.
– reference: Loeber R, Stouthamer-Loeber M. 1998. Development of juvenile aggression and violence. Some common misconceptions and controversies. Am Psychol 53:242-259.
– reference: Magarinos AM, Li CJ, Gal Toth J, Bath KG, Jing D, Lee FS, McEwen BS. 2011. Effect of brain-derived neurotrophic factor haploinsufficiency on stress-induced remodeling of hippocampal neurons. Hippocampus 21:253-264.
– reference: Ito W, Chehab M, Thakur S, Li J, Morozov A. 2011. BDNF-restricted knockout mice as an animal model for aggression. Genes Brain Behav 10:365-374.
– reference: Bartolomucci A, Palanza P, Sacerdote P, Panerai AE, Sgoifo A, Dantzer R, Parmigiani S. 2005. Social factors and individual vulnerability to chronic stress exposure. Neurosci Biobehav Rev 29:67-81.
– volume: 15
  start-page: 689
  year: 2012
  end-page: 695
  article-title: Social influences on neuroplasticity: Stress and interventions to promote well‐being
  publication-title: Nat Neurosci
– volume: 10
  start-page: 365
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Snippet ABSTRACT Epidemiological studies have shown that early life adverse events have long‐term effects on the susceptibility to subsequent stress exposure in...
Epidemiological studies have shown that early life adverse events have long‐term effects on the susceptibility to subsequent stress exposure in adolescence,...
Epidemiological studies have shown that early life adverse events have long-term effects on the susceptibility to subsequent stress exposure in adolescence,...
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StartPage 474
SubjectTerms acute stress
Affective Symptoms - etiology
Affective Symptoms - pathology
aggression
Aggression - physiology
Animals
Animals, Newborn
depression
Dizocilpine Maleate - pharmacology
Excitatory Amino Acid Antagonists - pharmacology
Excitatory Postsynaptic Potentials - drug effects
Exploratory Behavior - physiology
Gene Expression Regulation - physiology
Hippocampus - cytology
Hippocampus - metabolism
Male
Membrane Potentials - drug effects
Membrane Potentials - physiology
Mice
Mice, Inbred C57BL
Neurons - drug effects
Neurons - physiology
NMDA receptor
Piperidines - pharmacology
Prepulse Inhibition - drug effects
Prepulse Inhibition - physiology
Random Allocation
Receptors, N-Methyl-D-Aspartate - metabolism
Reflex, Startle - physiology
social isolation
Social Isolation - psychology
Swimming - psychology
Synaptosomes - drug effects
Synaptosomes - metabolism
Title Social isolation-induced increase in NMDA receptors in the hippocampus exacerbates emotional dysregulation in mice
URI https://api.istex.fr/ark:/67375/WNG-FLBQ21D1-R/fulltext.pdf
https://onlinelibrary.wiley.com/doi/abs/10.1002%2Fhipo.22384
https://www.ncbi.nlm.nih.gov/pubmed/25348768
https://www.proquest.com/docview/1664409284
https://www.proquest.com/docview/1665120248
https://www.proquest.com/docview/1668257695
Volume 25
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