Juvenile Stress Induces Behavioral Change and Affects Perineuronal Net Formation in Juvenile Mice

Overview

Journal BMC Neurosci

Publisher Biomed Central

Specialty Neurology

Date 2018 Jul 18

PMID 30012101

Citations 28

Authors

Hiroshi Ueno

Shunsuke Suemitsu

Shinji Murakami

Naoya Kitamura

Kenta Wani

Yosuke Matsumoto

Motoi Okamoto

Shozo Aoki

Takeshi Ishihara

Affiliations

Soon will be listed here.

Abstract

Background: Many neuropsychiatric disorders develop in early life. Although the mechanisms involved have not been elucidated, it is possible that functional abnormalities of parvalbumin-positive interneurons (PV neurons) are present. Several previous studies have shown that juvenile stress is implicated in the development of neuropsychiatric disorders. We aimed to clarify the effects of juvenile stress on behavior and on the central nervous system. We investigated behavioral abnormalities of chronically-stressed mice during juvenilehood and the effect of juvenile stress on PV neurons and WFA-positive perineuronal nets (PNNs), which are associated with vulnerability and plasticity in the mouse brain.

Results: Due to juvenile stress, mice showed neurodevelopmental disorder-like behavior. Juvenile stressed mice did not show depressive-like behaviors, but on the contrary, they showed increased activity and decreased anxiety-like behavior. In the central nervous system of juvenile stressed mice, the fluorescence intensity of WFA-positive PNNs decreased, which may signify increased vulnerability.

Conclusion: This study suggested that juvenile stressed mice showed behavioral abnormalities, resembling those seen in neuropsychiatric disorders, and increased brain vulnerability.

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References

Isgor C, Kabbaj M, Akil H, Watson S . Delayed effects of chronic variable stress during peripubertal-juvenile period on hippocampal morphology and on cognitive and stress axis functions in rats. Hippocampus. 2004; 14(5):636-48. DOI: 10.1002/hipo.10207. View

Khundakar A, Morris C, Thomas A . The immunohistochemical examination of GABAergic interneuron markers in the dorsolateral prefrontal cortex of patients with late-life depression. Int Psychogeriatr. 2010; 23(4):644-53. DOI: 10.1017/S1041610210001444. View

Kessler R, Berglund P, Demler O, Jin R, Merikangas K, Walters E . Lifetime prevalence and age-of-onset distributions of DSM-IV disorders in the National Comorbidity Survey Replication. Arch Gen Psychiatry. 2005; 62(6):593-602. DOI: 10.1001/archpsyc.62.6.593. View

Liang D, Li G, Liao X, Yu D, Wu J, Zhang M . Developmental loss of parvalbumin-positive cells in the prefrontal cortex and psychiatric anxiety after intermittent hypoxia exposures in neonatal rats might be mediated by NADPH oxidase-2. Behav Brain Res. 2015; 296:134-140. DOI: 10.1016/j.bbr.2015.08.033. View

Urakawa S, Takamoto K, Hori E, Sakai N, Ono T, Nishijo H . Rearing in enriched environment increases parvalbumin-positive small neurons in the amygdala and decreases anxiety-like behavior of male rats. BMC Neurosci. 2013; 14:13. PMC: 3599335. DOI: 10.1186/1471-2202-14-13. View

Fawcett J . The extracellular matrix in plasticity and regeneration after CNS injury and neurodegenerative disease. Prog Brain Res. 2015; 218:213-26. DOI: 10.1016/bs.pbr.2015.02.001. View

Jones P . Adult mental health disorders and their age at onset. Br J Psychiatry Suppl. 2013; 54:s5-10. DOI: 10.1192/bjp.bp.112.119164. View

Tottenham N, Sheridan M . A review of adversity, the amygdala and the hippocampus: a consideration of developmental timing. Front Hum Neurosci. 2010; 3:68. PMC: 2813726. DOI: 10.3389/neuro.09.068.2009. View

Jacob J . Cortical interneuron dysfunction in epilepsy associated with autism spectrum disorders. Epilepsia. 2015; 57(2):182-93. DOI: 10.1111/epi.13272. View

10.

Agoglia A, Holstein S, Small A, Spanos M, Burrus B, Hodge C . Comparison of the adolescent and adult mouse prefrontal cortex proteome. PLoS One. 2017; 12(6):e0178391. PMC: 5453624. DOI: 10.1371/journal.pone.0178391. View

11.

Augusto de Araujo Costa Folha O, Bahia C, de Aguiar G, Herculano A, Coelho N, de Sousa M . Effect of chronic stress during adolescence in prefrontal cortex structure and function. Behav Brain Res. 2017; 326:44-51. DOI: 10.1016/j.bbr.2017.02.033. View

12.

DeVallance E, Riggs D, Jackson B, Parkulo T, Zaslau S, Chantler P . Effect of chronic stress on running wheel activity in mice. PLoS One. 2017; 12(9):e0184829. PMC: 5604985. DOI: 10.1371/journal.pone.0184829. View

13.

Marin O . Interneuron dysfunction in psychiatric disorders. Nat Rev Neurosci. 2012; 13(2):107-20. DOI: 10.1038/nrn3155. View

14.

Balmer T . Perineuronal Nets Enhance the Excitability of Fast-Spiking Neurons. eNeuro. 2016; 3(4). PMC: 4987413. DOI: 10.1523/ENEURO.0112-16.2016. View

15.

Matsumoto Y, Katayama K, Okamoto T, Yamada K, Takashima N, Nagao S . Impaired auditory-vestibular functions and behavioral abnormalities of Slitrk6-deficient mice. PLoS One. 2011; 6(1):e16497. PMC: 3027700. DOI: 10.1371/journal.pone.0016497. View

16.

Turner R, Lloyd D . Stress burden and the lifetime incidence of psychiatric disorder in young adults: racial and ethnic contrasts. Arch Gen Psychiatry. 2004; 61(5):481-8. DOI: 10.1001/archpsyc.61.5.481. View

17.

Yoon S, Kim B, Ye S, Kim M . Chronic non-social stress affects depressive behaviors but not anxiety in mice. Korean J Physiol Pharmacol. 2014; 18(3):263-8. PMC: 4071180. DOI: 10.4196/kjpp.2014.18.3.263. View

18.

Ueno H, Suemitsu S, Murakami S, Kitamura N, Wani K, Okamoto M . Region-specific impairments in parvalbumin interneurons in social isolation-reared mice. Neuroscience. 2017; 359:196-208. DOI: 10.1016/j.neuroscience.2017.07.016. View

19.

Greenberg G, Laman-Maharg A, Campi K, Voigt H, Orr V, Schaal L . Sex differences in stress-induced social withdrawal: role of brain derived neurotrophic factor in the bed nucleus of the stria terminalis. Front Behav Neurosci. 2014; 7:223. PMC: 3885825. DOI: 10.3389/fnbeh.2013.00223. View

20.

Yao B, Cheng Y, Wang Z, Li Y, Chen L, Huang L . DNA N6-methyladenine is dynamically regulated in the mouse brain following environmental stress. Nat Commun. 2017; 8(1):1122. PMC: 5654764. DOI: 10.1038/s41467-017-01195-y. View