Partial genetic deletion of neuregulin 1 modulates the effects of stress on sensorimotor gating, dendritic morphology, and HPA axis activity in adolescent mice

Schizophrenia Bulletin

Volumn 40, Issue 6, 2014, Pages 1272-1284

  Chohan, Tariq W ^a   Boucher, Aurelie A ^a   Spencer, Jarrah R ^a   Kassem, Mustafa S ^a   Hamdi, Areeg A ^a   Karl, Tim ^b   Fok, Sandra Y ^a   Bennett, Maxwell R ^a   Arnold, Jonathon C ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

^b NEUROSCIENCE RESEARCH AUSTRALIA   (Australia)

Author keywords

adolescence; dendritic morphology; neuregulin 1; PPI; schizophrenia; stress

Indexed keywords

CORTICOSTERONE; NEU DIFFERENTIATION FACTOR;

ACUTE STRESS; ADOLESCENT; ADOLESCENT BEHAVIOR; ANIMAL EXPERIMENT; ANTERIOR CINGULATE; ARTICLE; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; DENDRITIC SPINE; DENDRITIC SPINE DENSITY; ENDOPHENOTYPE; FEMALE; GENE DELETION; GENETIC DIFFERENCE; GENETIC SUSCEPTIBILITY; GENETIC VARIABILITY; HIPPOCAMPUS; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; IMMOBILIZATION STRESS; MALE; MOUSE; NERVOUS SYSTEM PARAMETERS; NONHUMAN; PATHOGENESIS; PATHOPHYSIOLOGY; PREFRONTAL CORTEX; PREPULSE INHIBITION; PROTEIN EXPRESSION; PYRAMIDAL NERVE CELL; SENSORY GATING; SINGLE NUCLEOTIDE POLYMORPHISM; STARTLE REFLEX; STRESS; ANIMAL; C57BL MOUSE; CYTOLOGY; DISEASE MODEL; GENETICS; HYPOPHYSIS ADRENAL SYSTEM; HYPOTHALAMUS HYPOPHYSIS SYSTEM; MENTAL STRESS; PHYSIOLOGY;

ANIMALS; DENDRITIC SPINES; DISEASE MODELS, ANIMAL; FEMALE; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; MALE; MICE; MICE, INBRED C57BL; NEUREGULIN-1; PITUITARY-ADRENAL SYSTEM; PREFRONTAL CORTEX; PREPULSE INHIBITION; SENSORY GATING; STRESS, PSYCHOLOGICAL;

EID: 84907570931     PISSN: 05867614     EISSN: 17451701     Source Type: Journal    
DOI: 10.1093/schbul/sbt193     Document Type: Article

References (113)

1. Lewis DA, Levitt P. Schizophrenia as a disorder of neurodevelopment. Annu Rev Neurosci. 2002;25:409-432.
2. van Os J, Kenis G, Rutten BP. The environment and schizophrenia. Nature. 2010;468:203-212.
3. Van Winkel R, Esquivel G, Kenis G, et al. REVIEW: genomewide findings in schizophrenia and the role of gene-environment interplay. CNS Neurosci Ther. 2010;16:e185-e192.
4. Tessner KD, Mittal V, Walker EF. Longitudinal study of stressful life events and daily stressors among adolescents at high risk for psychotic disorders. Schizophr Bull. 2011;37:432-441.
5. Corcoran CM, Smith C, McLaughlin D, Auther A, Malaspina D, Cornblatt B. HPA axis function and symptoms in adolescents at clinical high risk for schizophrenia. Schizophr Res. 2012;135:170-174.
6. van Venrooij JA, Fluitman SB, Lijmer JG, et al. Impaired neuroendocrine and immune response to acute stress in medication-naive patients with a first episode of psychosis. Schizophr Bull. 2012;38:272-279.
7. Thapar A, Harold G, Rice F, Langley K, O'donovan M. The contribution of gene-environment interaction to psychopathology. Dev Psychopathol. 2007;19:989-1004.
8. Haque FN, Lipina TV, Roder JC, Wong AH. Social defeat interacts with Disc1 mutations in the mouse to affect behavior. Behav Brain Res. 2012;233:337-344.
9. Ishihama T, Ago Y, Shintani N, et al. Environmental factors during early developmental period influence psychobehavioral abnormalities in adult PACAP-deficient mice. Behav Brain Res. 2010;209:274-280.
10. Alaerts M, Ceulemans S, Forero D, et al. Support for NRG1 as a susceptibility factor for schizophrenia in a northern Swedish isolated population. Arch Gen Psychiatry. 2009;66:828-837.
11. Chong VZ, Thompson M, Beltaifa S, Webster MJ, Law AJ, Weickert CS. Elevated neuregulin-1 and ErbB4 protein in the prefrontal cortex of schizophrenic patients. Schizophr Res. 2008;100:270-280.
12. Stefansson H, Sigurdsson E, Steinthorsdottir V, et al. Neuregulin 1 and susceptibility to schizophrenia. Am J Hum Genet. 2002;71:877-892.
13. Hatzimanolis A, McGrath JA, Wang R, et al. Multiple variants aggregate in the neuregulin signaling pathway in a subset of schizophrenia patients. Transl Psychiatry. 2013;3:e264.
14. Bousman CA, Yung AR, Pantelis C, et al. Effects of NRG1 and DAOA genetic variation on transition to psychosis in individuals at ultra-high risk for psychosis. Transl Psychiatry. 2013;3:e251.
15. Barros CS, Calabrese B, Chamero P, et al. Impaired maturation of dendritic spines without disorganization of cortical cell layers in mice lacking NRG1/ErbB signaling in the central nervous system. Proc Natl Acad Sci U S A. 2009;106:4507-4512.
16. Bennett MR. Schizophrenia: susceptibility genes, dendriticspine pathology and gray matter loss. Prog Neurobiol. 2011;95:275-300.
17. Chen YJ, Johnson MA, Lieberman MD, et al. Type III neuregulin- 1 is required for normal sensorimotor gating, memory- related behaviors, and corticostriatal circuit components. J Neurosci. 2008;28:6872-6883.
18. Roussos P, Giakoumaki SG, Adamaki E, Bitsios P. The influence of schizophrenia-related neuregulin-1 polymorphisms on sensorimotor gating in healthy males. Biol Psychiatry. 2011;69:479-486.
19. Hong LE, Wonodi I, Stine OC, Mitchell BD, Thaker GK. Evidence of missense mutations on the neuregulin 1 gene affecting function of prepulse inhibition. Biol Psychiatry. 2008;63:17-23.
20. Arnold JC, Boucher AA, Karl T. The yin and yang of cannabisinduced psychosis: the actions of ?(9)-tetrahydrocannabinol and cannabidiol in rodent models of schizophrenia. Curr Pharm Des. 2012;18:5113-5130.
21. Boucher AA, Hunt GE, Karl T, Micheau J, McGregor IS, Arnold JC. Heterozygous neuregulin 1 mice display greater baseline and Delta(9)-tetrahydrocannabinol-induced c-Fos expression. Neuroscience. 2007;149:861-870.
22. Long LE, Chesworth R, Huang XF, McGregor IS, Arnold JC, Karl T. Transmembrane domain Nrg1 mutant mice show altered susceptibility to the neurobehavioural actions of repeated THC exposure in adolescence. Int J Neuropsychopharmacol. 2013;16:163-175.
23. Long LE, Chesworth R, Huang XF, et al. Distinct neurobehavioural effects of cannabidiol in transmembrane domain neuregulin 1 mutant mice. PLoS One. 2012;7:e34129.
24. Spencer JR, Darbyshire KM, Boucher AA, Arnold JC. Adolescent neuregulin 1 heterozygous mice display enhanced behavioural sensitivity to methamphetamine. Prog Neuropsychopharmacol Biol Psychiatry. 2012;39:376-381.
25. Boucher AA, Hunt GE, Micheau J, et al. The schizophrenia susceptibility gene neuregulin 1 modulates tolerance to the effects of cannabinoids. Int J Neuropsychopharmacol. 2011;14:631-643.
26. Spencer JR, Darbyshire KM, Boucher AA, et al. Novel molecular changes induced by Nrg1 hypomorphism and Nrg1-cannabinoid interaction in adolescence: a hippocampal proteomic study in mice. Front Cell Neurosci. 2013;7:15.
27. Karl T, Arnold JC. What does a mouse tell us about neuregulin 1-cannabis interactions? Front Cell Neurosci. 2013;7:18.
28. Spencer JR, Chohan TW, Karl T, Arnold JC. Female neuregulin 1 heterozygous mice require repeated exposure to Delta9- tetrahydrocannabinol to alter sensorimotor gating function. Pharmacopsychiatry. 2013;46:286-291.
29. Han S, Yang BZ, Kranzler HR, et al. Linkage analysis followed by association show NRG1 associated with cannabis dependence in African Americans. Biol Psychiatry. 2012;72:637-644.
30. Stadelmann AM, Roser P, Arning L, Gallinat J, Epplen JT, Juckel G. Acute effects of Delta9-tetrahydrocannabinol on the auditory evoked mismatch negativity are modulated by the NRG1 gene. Pharmacopsychiatry. 2010;43:194-195.
31. Boucher AA, Hunt GE, Micheau J, et al. The schizophrenia susceptibility gene neuregulin 1 modulates tolerance to the effects of cannabinoids. Int J Neuropsychopharmacol. 2011;14:631-643.
32. Desbonnet L, O'Tuathaigh C, Clarke G, et al. Phenotypic effects of repeated psychosocial stress during adolescence in mice mutant for the schizophrenia risk gene neuregulin-1: a putative model of gene × environment interaction. Brain Behav Immun. 2012;26:660-671.
33. van den Buuse M, Wischhof L, Lee RX, Martin S, Karl T. Neuregulin 1 hypomorphic mutant mice: enhanced baseline locomotor activity but normal psychotropic drug-induced hyperlocomotion and prepulse inhibition regulation. Int J Neuropsychopharmacol. 2009;12:1383-1393.
34. Boucher AA, Arnold JC, Duffy L, Schofield PR, Micheau J, Karl T. Heterozygous neuregulin 1 mice are more sensitive to the behavioural effects of Delta9-tetrahydrocannabinol. Psychopharmacology (Berl). 2007;192:325-336.
35. Karl T, Burne TH, Van den Buuse M, Chesworth R. Do transmembrane domain neuregulin 1 mutant mice exhibit a reliable sensorimotor gating deficit? Behav Brain Res. 2011;223:336-341.
36. Burrows EL, McOmish CE, Hannan AJ. Gene-environment interactions and construct validity in preclinical models of psychiatric disorders. Prog Neuropsychopharmacol Biol Psychiatry. 2011;35:1376-1382.
37. Alfarez DN, De Simoni A, Velzing EH, et al. Corticosterone reduces dendritic complexity in developing hippocampal CA1 neurons. Hippocampus. 2009;19:828-836.
38. Radley JJ, Rocher AB, Rodriguez A, et al. Repeated stress alters dendritic spine morphology in the rat medial prefrontal cortex. J Comp Neurol. 2008;507:1141-1150.
39. Swerdlow NR, Weber M, Qu Y, Light GA, Braff DL. Realistic expectations of prepulse inhibition in translational models for schizophrenia research. Psychopharmacology (Berl). 2008;199:331-388.
40. Michelsen KA, van den Hove DL, Schmitz C, Segers O, Prickaerts J, Steinbusch HW. Prenatal stress and subsequent exposure to chronic mild stress influence dendritic spine density and morphology in the rat medial prefrontal cortex. BMC Neurosci. 2007;8:107.
41. Hazlett EA, Buchsbaum MS, Haznedar MM, et al. Prefrontal cortex glucose metabolism and startle eyeblink modification abnormalities in unmedicated schizophrenia patients. Psychophysiology. 1998;35:186-198.
42. Tregellas JR, Davalos DB, Rojas DC, et al. Increased hemodynamic response in the hippocampus, thalamus and prefrontal cortex during abnormal sensory gating in schizophrenia. Schizophr Res. 2007;92:262-272.
43. Valsamis B, Chang M, Typlt M, Schmid S. Activation of mGluR2/3 receptors in the ventro-rostral prefrontal cortex reverses sensorimotor gating deficits induced by systemic NMDA receptor antagonists. Int J Neuropsychopharmacol. 2013:1-10.
44. Shoemaker JM, Saint Marie RL, Bongiovanni MJ, Neary AC, Tochen LS, Swerdlow NR. Prefrontal D1 and ventral hippocampal N-methyl-D-aspartate regulation of startle gating in rats. Neuroscience. 2005;135:385-394.
45. Wegener N, Kuhnert S, Thüns A, Roese R, Koch M. Effects of acute systemic and intra-cerebral stimulation of cannabinoid receptors on sensorimotor gating, locomotion and spatial memory in rats. Psychopharmacology (Berl). 2008;198:375-385.
46. Rompala GR, Zsiros V, Zhang S, Kolata SM, Nakazawa K. Contribution of NMDA receptor hypofunction in prefrontal and cortical excitatory neurons to schizophrenia-like phenotypes. PLoS One. 2013;8:e61278.
47. Kassem MS, Lagopoulos J, Stait-Gardner T, et al. Stressinduced grey matter loss determined by MRI is primarily due to loss of dendrites and their synapses. Mol Neurobiol. 2013;47:645-661.
48. Vázquez DM. Stress and the developing limbic-hypothalamic- pituitary-adrenal axis. Psychoneuroendocrinology. 1998;23:663-700.
49. Stone EA, Quartermain D. Greater behavioral effects of stress in immature as compared to mature male mice. Physiol Behav. 1997;63:143-145.
50. Liu RJ, Aghajanian GK. Stress blunts serotonin- and hypocretin- evoked EPSCs in prefrontal cortex: role of corticosterone- mediated apical dendritic atrophy. Proc Natl Acad Sci U S A. 2008;105:359-364.
51. Cerqueira JJ, Taipa R, Uylings HB, Almeida OF, Sousa N. Specific configuration of dendritic degeneration in pyramidal neurons of the medial prefrontal cortex induced by differing corticosteroid regimens. Cereb Cortex. 2007;17:1998-2006.
52. Czéh B, Perez-Cruz C, Fuchs E, Flügge G. Chronic stressinduced cellular changes in the medial prefrontal cortex and their potential clinical implications: does hemisphere location matter? Behav Brain Res. 2008;190:1-13.
53. Herman JP, Figueiredo H, Mueller NK, et al. Central mechanisms of stress integration: hierarchical circuitry controlling hypothalamo-pituitary-adrenocortical responsiveness. Front Neuroendocrinol. 2003;24:151-180.
54. Radley JJ, Anderson RM, Hamilton BA, Alcock JA, Romig- Martin SA. Chronic stress-induced alterations of dendritic spine subtypes predict functional decrements in an hypothalamo- pituitary-adrenal-inhibitory prefrontal circuit. J Neurosci. 2013;33:14379-14391.
55. O'Tuathaigh CM, O'Connor AM, O'Sullivan GJ, et al. Disruption to social dyadic interactions but not emotional/anxiety-related behaviour in mice with heterozygous ?knockout' of the schizophrenia risk gene neuregulin-1. Prog Neuropsychopharmacol Biol Psychiatry. 2008;32:462-466.
56. O'Tuathaigh CM, Babovic D, O'Sullivan GJ, et al. Phenotypic characterization of spatial cognition and social behavior in mice with ?knockout' of the schizophrenia risk gene neuregulin 1. Neuroscience. 2007;147:18-27.
57. Karl T, Duffy L, Scimone A, Harvey RP, Schofield PR. Altered motor activity, exploration and anxiety in heterozygous neuregulin 1 mutant mice: implications for understanding schizophrenia. Genes Brain Behav. 2007;6:677-687.
58. Duffy L, Cappas E, Lai D, Boucher AA, Karl T. Cognition in transmembrane domain neuregulin 1 mutant mice. Neuroscience. 2010;170:800-807.
59. Dean B, Karl T, Pavey G, Boer S, Duffy L, Scarr E. Increased levels of serotonin 2A receptors and serotonin transporter in the CNS of neuregulin 1 hypomorphic/mutant mice. Schizophr Res. 2008;99:341-349.
60. Bjarnadottir M, Misner DL, Haverfield-Gross S, et al. Neuregulin1 (NRG1) signaling through Fyn modulates NMDA receptor phosphorylation: differential synaptic function in NRG1+/- knock-outs compared with wild-type mice. J Neurosci. 2007;27:4519-4529.
61. Sutherland JE, Conti LH. Restraint stress-induced reduction in prepulse inhibition in Brown Norway rats: role of the CRF2 receptor. Neuropharmacology. 2011;60:561-571.
62. Chesworth R, Yulyaningsih E, Cappas E, Arnold J, Sainsbury A, Karl T. The response of neuregulin 1 mutant mice to acute restraint stress. Neurosci Lett. 2012;515:82-86.
63. Eiland L, McEwen BS. Early life stress followed by subsequent adult chronic stress potentiates anxiety and blunts hippocampal structural remodeling. Hippocampus. 2012;22:82-91.
64. Sutherland JE, Burian LC, Covault J, Conti LH. The effect of restraint stress on prepulse inhibition and on corticotropinreleasing factor (CRF) and CRF receptor gene expression in Wistar-Kyoto and Brown Norway rats. Pharmacol Biochem Behav. 2010;97:227-238.
65. Brown SM, Henning S, Wellman CL. Mild, short-term stress alters dendritic morphology in rat medial prefrontal cortex. Cereb Cortex. 2005;15:1714-1722.
66. Bloss EB, Janssen WG, McEwen BS, Morrison JH. Interactive effects of stress and aging on structural plasticity in the prefrontal cortex. J Neurosci. 2010;30:6726-6731.
67. Radley JJ, Rocher AB, Miller M, et al. Repeated stress induces dendritic spine loss in the rat medial prefrontal cortex. Cereb Cortex. 2006;16:313-320.
68. Martínez-Téllez RI, Hernández-Torres E, Gamboa C, Flores G. Prenatal stress alters spine density and dendritic length of nucleus accumbens and hippocampus neurons in rat offspring. Synapse. 2009;63:794-804.
69. Magariños AM, Li CJ, Gal Toth J, et al. Effect of brain-derived neurotrophic factor haploinsufficiency on stress-induced remodeling of hippocampal neurons. Hippocampus. 2011;21:253-264.
70. Darbra S, Mòdol L, Pallarès M. Allopregnanolone infused into the dorsal (CA1) hippocampus increases prepulse inhibition of startle response in Wistar rats. Psychoneuroendocrinology. 2012;37:581-585.
71. Kusljic S, van den Buuse M. Functional dissociation between serotonergic pathways in dorsal and ventral hippocampus in psychotomimetic drug-induced locomotor hyperactivity and prepulse inhibition in rats. Eur J Neurosci. 2004;20:3424-3432.
72. Eiland L, Ramroop J, Hill MN, Manley J, McEwen BS. Chronic juvenile stress produces corticolimbic dendritic architectural remodeling and modulates emotional behavior in male and female rats. Psychoneuroendocrinology. 2012;37:39-47.
73. Liston C, Miller MM, Goldwater DS, et al. Stress-induced alterations in prefrontal cortical dendritic morphology predict selective impairments in perceptual attentional set-shifting. J Neurosci. 2006;26:7870-7874.
74. Radley JJ, Sisti HM, Hao J, et al. Chronic behavioral stress induces apical dendritic reorganization in pyramidal neurons of the medial prefrontal cortex. Neuroscience. 2004;125:1-6.
75. Benes FM. Amygdalocortical circuitry in schizophrenia: from circuits to molecules. Neuropsychopharmacology. 2010;35:239-257.
76. Glantz LA, Lewis DA. Decreased dendritic spine density on prefrontal cortical pyramidal neurons in schizophrenia. Arch Gen Psychiatry. 2000;57:65-73.
77. Glausier JR, Lewis DA. Dendritic spine pathology in schizophrenia. Neuroscience. 2013;251:90-107.
78. Pawlak R, Rao BS, Melchor JP, Chattarji S, McEwen B, Strickland S. Tissue plasminogen activator and plasminogen mediate stress-induced decline of neuronal and cognitive functions in the mouse hippocampus. Proc Natl Acad Sci U S A. 2005;102:18201-18206.
79. Pillai AG, de Jong D, Kanatsou S, et al. Dendritic morphology of hippocampal and amygdalar neurons in adolescent mice is resilient to genetic differences in stress reactivity. PLoS One. 2012;7:e38971.
80. Buschman TJ, Miller EK. Top-down versus bottom-up control of attention in the prefrontal and posterior parietal cortices. Science. 2007;315:1860-1862.
81. Knight RT, Grabowecky MF, Scabini D. Role of human prefrontal cortex in attention control. Adv Neurol. 1995;66:21- 34; discussion 34-26.
82. Jafari M, Seese RR, Babayan AH, Gall CM, Lauterborn JC. Glucocorticoid receptors are localized to dendritic spines and influence local actin signaling. Mol Neurobiol. 2012;46:304-315.
83. Liston C, Gan WB. Glucocorticoids are critical regulators of dendritic spine development and plasticity in vivo. Proc Natl Acad Sci U S A. 2011;108:16074-16079.
84. Furay AR, Bruestle AE, Herman JP. The role of the forebrain glucocorticoid receptor in acute and chronic stress. Endocrinology. 2008;149:5482-5490.
85. Quednow BB, Schmechtig A, Ettinger U, et al. Sensorimotor gating depends on polymorphisms of the serotonin-2A receptor and catechol-O-methyltransferase, but not on neuregulin- 1 Arg38Gln genotype: a replication study. Biol Psychiatry. 2009;66:614-620.
86. Uehara T, Sumiyoshi T, Seo T, et al. Long-term effects of neonatal MK-801 treatment on prepulse inhibition in young adult rats. Psychopharmacology (Berl). 2009;206:623-630.
87. Pian JP, Criado JR, Ehlers CL. Differential effects of acute alcohol on prepulse inhibition and event-related potentials in adolescent and adult Wistar rats. Alcohol Clin Exp Res. 2008;32:2062-2073.
88. Taylor SB, Taylor AR, Koenig JI. The interaction of disrupted Type II Neuregulin 1 and chronic adolescent stress on adult anxiety- and fear-related behaviors. Neuroscience. 2013;249:31-42.
89. Taylor SB, Taylor AR, Markham JA, Geurts AM, Kanaskie BZ, Koenig JI. Disruption of the neuregulin 1 gene in the rat alters HPA axis activity and behavioral responses to environmental stimuli. Physiol Behav. 2011;104:205-214.
90. Kéri S, Kiss I, Seres I, Kelemen O. A polymorphism of the neuregulin 1 gene (SNP8NRG243177/rs6994992) affects reactivity to expressed emotion in schizophrenia. Am J Med Genet B Neuropsychiatr Genet. 2009;150B:418-420.
91. Johnson MR, Adler LE. Transient impairment in P50 auditory sensory gating induced by a cold-pressor test. Biol Psychiatry. 1993;33:380-387.
92. Dai H, Okuda H, Iwabuchi K, et al. Social isolation stress significantly enhanced the disruption of prepulse inhibition in mice repeatedly treated with methamphetamine. Ann N Y Acad Sci. 2004;1025:257-266.
93. Gabbott PL, Warner TA, Jays PR, Salway P, Busby SJ. Prefrontal cortex in the rat: projections to subcortical autonomic, motor, and limbic centers. J Comp Neurol. 2005;492:145-177.
94. Hammer TB, Oranje B, Skimminge A, et al. Structural brain correlates of sensorimotor gating in antipsychotic-naive men with first-episode schizophrenia. J Psychiatry Neurosci. 2013;38:34-42.
95. Campbell LE, Hughes M, Budd TW, et al. Primary and secondary neural networks of auditory prepulse inhibition: a functional magnetic resonance imaging study of sensorimotor gating of the human acoustic startle response. Eur J Neurosci. 2007;26:2327-2333.
96. Kumari V, Antonova E, Geyer MA, Ffytche D, Williams SC, Sharma T. A fMRI investigation of startle gating deficits in schizophrenia patients treated with typical or atypical antipsychotics. Int J Neuropsychopharmacol. 2007;10:463-477.
97. Fatjó-Vilas M, Pomarol-Clotet E, Salvador R, et al. Effect of the interleukin-1? gene on dorsolateral prefrontal cortex function in schizophrenia: a genetic neuroimaging study. Biol Psychiatry. 2012;72:758-765.
98. Goshen I, Avital A, Kreisel T, Licht T, Segal M, Yirmiya R. Environmental enrichment restores memory functioning in mice with impaired IL-1 signaling via reinstatement of longterm potentiation and spine size enlargement. J Neurosci. 2009;29:3395-3403.
99. Muhammad A, Carroll C, Kolb B. Stress during development alters dendritic morphology in the nucleus accumbens and prefrontal cortex. Neuroscience. 2012;216:103-109.
100. Bock J, Murmu MS, Biala Y, Weinstock M, Braun K. Prenatal stress and neonatal handling induce sex-specific changes in dendritic complexity and dendritic spine density in hippocampal subregions of prepubertal rats. Neuroscience. 2011;193:34-43.
101. Antzoulatos E, Jakowec MW, Petzinger GM, Wood RI. MPTP neurotoxicity and testosterone induce dendritic remodeling of striatal medium spiny neurons in the C57Bl/6 mouse. Parkinsons Dis. 2011;2011:138471.
102. Radley JJ. Toward a limbic cortical inhibitory network: implications for hypothalamic-pituitary-adrenal responses following chronic stress. Front Behav Neurosci. 2012;6:7.
103. Radley JJ, Sawchenko PE. A common substrate for prefrontal and hippocampal inhibition of the neuroendocrine stress response. J Neurosci. 2011;31:9683-9695.
104. Krivosheya D, Tapia L, Levinson JN, et al. ErbB4-neuregulin signaling modulates synapse development and dendritic arborization through distinct mechanisms. J Biol Chem. 2008;283:32944-32956.
105. Gerecke KM, Wyss JM, Carroll SL. Neuregulin-1beta induces neurite extension and arborization in cultured hippocampal neurons. Mol Cell Neurosci. 2004;27:379-393.
106. Weickert CS, Tiwari Y, Schofield PR, Mowry BJ, Fullerton JM. Schizophrenia-associated HapICE haplotype is associated with increased NRG1 type III expression and high nucleotide diversity. Transl Psychiatry. 2012;2:e104.
107. Hashimoto R, Straub RE, Weickert CS, Hyde TM, Kleinman JE, Weinberger DR. Expression analysis of neuregulin-1 in the dorsolateral prefrontal cortex in schizophrenia. Mol Psychiatry. 2004;9:299-307.
108. Law AJ, Lipska BK, Weickert CS, et al. Neuregulin 1 transcripts are differentially expressed in schizophrenia and regulated by 5' SNPs associated with the disease. Proc Natl Acad Sci U S A. 2006;103:6747-6752.
109. Bertram I, Bernstein HG, Lendeckel U, et al. Immunohistochemical evidence for impaired neuregulin-1 signaling in the prefrontal cortex in schizophrenia and in unipolar depression. Ann N Y Acad Sci. 2007;1096:147-156.
110. Parlapani E, Schmitt A, Wirths O, et al. Gene expression of neuregulin-1 isoforms in different brain regions of elderly schizophrenia patients. World J Biol Psychiatry. 2010;11:243-250.
111. Marballi K, Cruz D, Thompson P, Walss-Bass C. Differential neuregulin 1 cleavage in the prefrontal cortex and hippocampus in schizophrenia and bipolar disorder: preliminary findings. PLoS One. 2012;7:e36431.
112. Yin DM, Chen YJ, Lu YS, et al. Reversal of behavioral deficits and synaptic dysfunction in mice overexpressing neuregulin 1. Neuron. 2013;78:644-657.
113. Pan B, Huang XF, Deng C. Antipsychotic treatment and neuregulin 1-ErbB4 signalling in schizophrenia. Prog Neuropsychopharmacol Biol Psychiatry. 2011;35:924-930