nach oben

Erschienen in:

19.02.2019 | Original Paper

Optogenetic Stimulation of the Anterior Cingulate Cortex Ameliorates Autistic-Like Behaviors in Rats Induced by Neonatal Isolation, Caudate Putamen as a Site for Alteration

verfasst von: Elham Sadat Sayed Javad Javaheri, Mohammad Reza Bigdeli, Mohammad Ismail Zibaii, Leila Dargahi, Hamid Reza Pouretemad

Erschienen in: NeuroMolecular Medicine | Ausgabe 2/2019

Einloggen, um Zugang zu erhalten

Abstract

Epigenetic agents, such as neonatal isolation during neurodevelopmental period of life, can change various regions of the brain. It may further induce psychological disorders such as autistic-like phenomena. This study indicated the role of chronic increased anterior cingulate cortex (ACC) output on alteration of caudate putamen (CPu) as a main behavior regulator region of the brain in adult maternal deprived (MD) rats. For making an animal model, neonates were isolated from their mothers in postnatal days (PND 1–10, 3 h/day). Subsequently, they bilaterally received pLenti-CaMKIIa-hChR2 (H134R)-mCherry-WPRE virus in ACC area via stereotaxic surgery in PND50. After 22 days, these regions were exposed to blue laser (473 nm) for six consecutive days (15 min/day). Then, behavioral deficits were tested and were compared with control group in the following day. Animals were immediately killed and their brains were prepared for tissue processing. Results showed that neonatal isolation induces autistic-like behaviors and leads to overexpression of NMDAR1 and Nox2-gp91^phox proteins and elevation of catalase activity in the CPu regions of the adult offspring compared with control group. Chronic optogenetic stimulation of ACC neurons containing (ChR2+) led to significant reduction in the appearance of stereotypical behavior and alien-phobia in MD rats. The amount of NMDAR1 and Nox2-gp91^phox expression and the catalase activity in CPu were reduced after this treatment. Therefore, autistic-like behavior seems to be related with elevation of NMDAR1 and Nox2-gp91^phox protein levels that enhance the effect of glutamatergic projection on CPu regions. Optogenetic treatment also could ameliorate behavioral deficits by modulating these protein densities.

Albin, R. L., Makowiec, R. L., Hollingsworth, Z. R., Dure, L. S. T., Penney, J. B., & Young, A. B. (1992). Excitatory amino acid binding sites in the basal ganglia of the rat: A quantitative autoradiographic study. Neuroscience, 46(1), 35–48.CrossRef

Alexander, B., & Poletaev, B. A. S. (2016). Autism: Genetics or Epigenetics? ARC Journals of Immunology and Vaccines, 1(2), 7.

Association, A. P. (2013). Diagnostic and statistical manual of mental disorders. Washington DC: American Psychiatric Association.CrossRef

Bahi, A. (2017). Hippocampal BDNF overexpression or microR124a silencing reduces anxiety- and autism-like behaviors in rats. Behavioural Brain Research, 326, 281–290. https://doi.org/10.1016/j.bbr.2017.03.010.CrossRefPubMed

Brennan, A. M., Suh, S. W., Won, S. J., Narasimhan, P., Kauppinen, T. M., Lee, H., … Swanson, R. A. (2009). NADPH oxidase is the primary source of superoxide induced by NMDA receptor activation. Nature Neuroscience, 12(7), 857–863. https://doi.org/10.1038/nn.2334.PubMedCentralCrossRefPubMed

Burguiere, E., Monteiro, P., Feng, G., & Graybiel, A. M. (2013). Optogenetic stimulation of lateral orbitofronto-striatal pathway suppresses compulsive behaviors. Science, 340(6137), 1243–1246. https://doi.org/10.1126/science.1232380.CrossRefPubMed

Calabrese, F., Guidotti, G., Molteni, R., Racagni, G., Mancini, M., & Riva, M. A. (2012). Stress-induced changes of hippocampal NMDA receptors: Modulation by duloxetine treatment. PLoS ONE, 7(5), e37916. https://doi.org/10.1371/journal.pone.0037916.PubMedCentralCrossRefPubMed

Campos-Rangel, A., Saavedra-Molina, L. T.-A., & Manzo-Avalos, A. S. (2017). Effect of maternal separation on oxidative and nitrosative stress in the brain of rat offspring. The FASEB Journal, 31(1), 779-7.

Carvajal, F. J., Mattison, H. A., & Cerpa, W. (2016). Role of NMDA receptor-mediated glutamatergic signaling in chronic and acute neuropathologies. Neural Plasticity, 2016, 2701526. https://doi.org/10.1155/2016/2701526.PubMedCentralCrossRefPubMed

Cho, H., Kim, C. H., Knight, E. Q., Oh, H. W., Park, B., Kim, D. G., & Park, H. J. (2017). Changes in brain metabolic connectivity underlie autistic-like social deficits in a rat model of autism spectrum disorder. Scientific Reports, 7(1), 13213. https://doi.org/10.1038/s41598-017-13642-3.PubMedCentralCrossRefPubMed

Crawley, J. N. (2007). Mouse behavioral assays relevant to the symptoms of autism. Brain Pathology, 17(4), 448–459. https://doi.org/10.1111/j.1750-3639.2007.00096.x.CrossRefPubMed

Crawley, J. N. (2012). Translational animal models of autism and neurodevelopmental disorders. Dialogues in Clinical Neuroscience, 14(3), 293–305.PubMedCentralPubMed

Curley, J. P., Jensen, C. L., Mashoodh, R., & Champagne, F. A. (2011). Social influences on neurobiology and behavior: Epigenetic effects during development. Psychoneuroendocrinology, 36(3), 352–371. https://doi.org/10.1016/j.psyneuen.2010.06.005.CrossRefPubMed

Deisseroth, K. (2012). Optogenetics and psychiatry: Applications, challenges, and opportunities. Biological Psychiatry, 71(12), 1030–1032. https://doi.org/10.1016/j.biopsych.2011.12.021.CrossRefPubMed

Diehl, L. A., Pereira Nde, S., Laureano, D. P., Benitz, A. N., Noschang, C., Ferreira, A. G., … Dalmaz, C. (2014). Contextual fear conditioning in maternal separated rats: The amygdala as a site for alterations. Neurochemical Research, 39(2), 384–393. https://doi.org/10.1007/s11064-013-1230-x.CrossRefPubMed

Fonnum, F., Storm-Mathisen, J., & Divac, I. (1981). Biochemical evidence for glutamate as neurotransmitter in corticostriatal and corticothalamic fibres in rat brain. Neuroscience, 6(5), 863–873.CrossRef

Fuccillo, M. V. (2016). Striatal circuits as a common node for autism pathophysiology. Frontiers in Neuroscience, 10, 27. https://doi.org/10.3389/fnins.2016.00027.PubMedCentralCrossRefPubMed

Girouard, H., Wang, G., Gallo, E. F., Anrather, J., Zhou, P., Pickel, V. M., & Iadecola, C. (2009). NMDA receptor activation increases free radical production through nitric oxide and NOX2. Journal of Neuroscience, 29(8), 2545–2552. https://doi.org/10.1523/JNEUROSCI.0133-09.2009.CrossRefPubMed

González-Fraguel, M. E., Hung, M. L. D., Vera, H., Maragoto, C., Noris, E., Blanco, L., ... & Robinson, M. (2013). Oxidative stress markers in children with autism spectrum disorders. British Journal of Medicine & Medical Research, 3(2), 10.

Guang-yan Wu, G. L., Zhang, H., Chen, C., Liu, S., Feng, H., & Sui, J. F. (2015). Optogenetic stimulation of mPFC pyramidal neurons as a conditioned stimulus supports associative learning in rats. Scientific Reports, 5, 11.

Gudsnuk, K., & Champagne, F. A. (2012). Epigenetic influence of stress and the social environment. ILAR Journal, 53(3–4), 279–288. https://doi.org/10.1093/ilar.53.3-4.279.PubMedCentralCrossRefPubMed

Guglielmi, G., Falk, H. J., & De Renzis, S. (2016). Optogenetic control of protein function: From intracellular processes to tissue morphogenesis. Trends in Cell Biology, 26(11), 864–874. https://doi.org/10.1016/j.tcb.2016.09.006.PubMedCentralCrossRefPubMed

Hauber, W., & Sommer, S. (2009). Prefrontostriatal circuitry regulates effort-related decision making. Cerebral Cortex, 19(10), 2240–2247. https://doi.org/10.1093/cercor/bhn241.CrossRef

Hosenbocus, S., & Chahal, R. (2013). Memantine: A review of possible uses in child and adolescent psychiatry. Journal of the Canadian Academy of Child and Adolescent Psychiatry, 22(2), 166–171.PubMedCentralPubMed

Ji, G., Lv, K., Chen, H., Wang, T., Wang, Y., Zhao, D., … Li, Y. (2013). miR-146a regulates SOD2 expression in H₂O₂ stimulated PC12 cells. PLoS ONE, 8(7), e69351. https://doi.org/10.1371/journal.pone.0069351.PubMedCentralCrossRefPubMed

Jin, W., Chung, J.-H. S., Baek, S.-B., Kim, C.-J., & Kim, T.-W. (2014). Treadmill exercise inhibits hippocampal apoptosis through enhancing N-methyl-D-aspartate receptor expression in the MK-801-induced schizophrenic mice. Journal of Exercise Rehabilitation, 10(4), 7.

Kaidanovich-Beilin, O., Lipina, T., Vukobradovic, I., Roder, J., & Woodgett, J. R. (2011). Assessment of social interaction behaviors. Journal of Visualized Experiments. https://doi.org/10.3791/2473.CrossRefPubMed

Karreman, M., & Moghaddam, B. (1996). The prefrontal cortex regulates the basal release of dopamine in the limbic striatum: An effect mediated by ventral tegmental area. Journal of Neurochemistry, 66(2), 589–598.CrossRef

Kim, H., Lee, Y., Park, J. Y., Kim, J. E., Kim, T. K., Choi, J., … Han, P. L. (2017). Loss of adenylyl cyclase type-5 in the dorsal striatum produces autistic-like behaviors. Molecular Neurobiology, 54(10), 7994–8008. https://doi.org/10.1007/s12035-016-0256-x.CrossRefPubMed

Kim, H., Lim, C. S., & Kaang, B. K. (2016). Neuronal mechanisms and circuits underlying repetitive behaviors in mouse models of autism spectrum disorder. Behavioral and Brain Functions, 12(1), 3. https://doi.org/10.1186/s12993-016-0087-y.CrossRefPubMed

Kishida, K. T., & Klann, E. (2007). Sources and targets of reactive oxygen species in synaptic plasticity and memory. Antioxidants & Redox Signaling, 9(2), 233–244. https://doi.org/10.1089/ars.2007.9.ft-8.CrossRef

Lee, E. J., Choi, S. Y., & Kim, E. (2015). NMDA receptor dysfunction in autism spectrum disorders. Current Opinion Pharmacology, 20, 8–13. https://doi.org/10.1016/j.coph.2014.10.007.CrossRef

Lee, P. R., Brady, D., & Koenig, J. I. (2003). Corticosterone alters N-methyl-D-aspartate receptor subunit mRNA expression before puberty. Molecular Brain Research, 115(1), 55–62.CrossRef

Lee, Y., Kim, H., Kim, J. E., Park, J. Y., Choi, J., Lee, J. E., … Han, P. L. (2018). Excessive D1 dopamine receptor activation in the dorsal striatum promotes autistic-like behaviors. Molecular Neurobiology, 55(7), 5658–5671. https://doi.org/10.1007/s12035-017-0770-5.CrossRefPubMed

Luo, W., Zhang, C., Jiang, Y. H., & Brouwer, C. R. (2018). Systematic reconstruction of autism biology from massive genetic mutation profiles. Science Advances, 4(4), e1701799. https://doi.org/10.1126/sciadv.1701799.PubMedCentralCrossRefPubMed

Lupien, S. J., McEwen, B. S., Gunnar, M. R., & Heim, C. (2009). Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nature Reviews Neuroscience, 10(6), 434–445. https://doi.org/10.1038/nrn2639.CrossRefPubMed

Markovic, B., Radonjic, N. V., Jevtic, G., Stojkovic, T., Velimirovic, M., Aksic, M., … Petronijevic, N. D. (2017). Long-term effects of maternal deprivation on redox regulation in rat brain: Involvement of NADPH oxidase. Oxidative Medicine and Cellular Longevity, 2017, 7390516. https://doi.org/10.1155/2017/7390516.PubMedCentralCrossRefPubMed

Martin, K. P., & Wellman, C. L. (2011). NMDA receptor blockade alters stress-induced dendritic remodeling in medial prefrontal cortex. Cerebral Cortex, 21(10), 2366–2373. https://doi.org/10.1093/cercor/bhr021.CrossRefPubMed

McGeer, P. L., McGeer, E. G., Scherer, U., & Singh, K. (1977). A glutamatergic corticostriatal path? Brain Research, 128(2), 369–373.CrossRef

McGinnis, W. R. (2004). Oxidative stress in autism. Alternative Therapies Health and Medicine, 10(6), 22–36 (quiz 37, 92).

Milanizadeh, S., Zuwarali, K. N. N., Aliaghaei, A., & Bigdeli, M. R. (2018). Therapeutic potential of pretreatment with allograft sertoli cells transplantation in brain ischemia by improving oxidative defenses. Journal of Molecular Neuroscience, 64(4), 533–542. https://doi.org/10.1007/s12031-018-1054-x.CrossRefPubMed

Mohammed, C. P., Rhee, H., Phee, B. K., Kim, K., Kim, H. J., Lee, H., … Kim, K. (2016). miR-204 downregulates EphB2 in aging mouse hippocampal neurons. Aging Cell, 15(2), 380–388. https://doi.org/10.1111/acel.12444.CrossRefPubMed

Naziroglu, M. (2012). Molecular role of catalase on oxidative stress-induced Ca(2+) signaling and TRP cation channel activation in nervous system. Journal of Receptors and Signal Transduction, 32(3), 134–141. https://doi.org/10.3109/10799893.2012.672994.CrossRefPubMed

Rees, S. L., Akbari, E., Steiner, M., & Fleming, A. S. (2008). Effects of early deprivation and maternal separation on pup-directed behavior and HPA axis measures in the juvenile female rat. Developmental Psychobiology, 50(4), 315–321. https://doi.org/10.1002/dev.20292.CrossRefPubMed

Rice, M. W., Smith, K. L., Roberts, R. C., Perez-Costas, E., & Melendez-Ferro, M. (2014). Assessment of cytochrome C oxidase dysfunction in the substantia nigra/ventral tegmental area in schizophrenia. PLoS ONE, 9(6), e100054. https://doi.org/10.1371/journal.pone.0100054.PubMedCentralCrossRefPubMed

Rojas, D. C. (2014). The role of glutamate and its receptors in autism and the use of glutamate receptor antagonists in treatment. Journal of Neural Transmission (Vienna), 121(8), 891–905. https://doi.org/10.1007/s00702-014-1216-0.CrossRef

Sogut, S., Zoroglu, S. S., Ozyurt, H., Yilmaz, H. R., Ozugurlu, F., Sivasli, E., … Akyol, O. (2003). Changes in nitric oxide levels and antioxidant enzyme activities may have a role in the pathophysiological mechanisms involved in autism. Clinica Chimica Acta, 331(1–2), 111–117.CrossRef

Sorce, S., & Krause, K. H. (2009). NOX enzymes in the central nervous system: from signaling to disease. Antioxidants & Redox Signaling, 11(10), 2481–2504. https://doi.org/10.1089/ARS.2009.2578.CrossRef

Sparta, D. R., Stamatakis, A. M., Phillips, J. L., van Zessen, R., & Stuber, G. D. (2012). Construction of implantable optical fibers for long-term optogenetic manipulation of neural circuits. Nature Protocols, 7(1), 12.CrossRef

Standaert, D. G., Friberg, I. K., Landwehrmeyer, G. B., Young, A. B., & Penney, J. B. Jr. (1999). Expression of NMDA glutamate receptor subunit mRNAs in neurochemically identified projection and interneurons in the striatum of the rat. Brain Research Molecular Brain Research, 64(1), 11–23.CrossRef

Tan, T., Wang, W., Xu, H., Huang, Z., Wang, Y. T., & Dong, Z. (2018). Low-frequency rTMS ameliorates autistic-like behaviors in rats induced by neonatal isolation through regulating the synaptic GABA transmission. Frontiers in Cell Neuroscience, 12, 46. https://doi.org/10.3389/fncel.2018.00046.CrossRef

Tsuda, M. C., & Ogawa, S. (2012). Long-lasting consequences of neonatal maternal separation on social behaviors in ovariectomized female mice. PLoS ONE, 7(3), e33028. https://doi.org/10.1371/journal.pone.0033028.PubMedCentralCrossRefPubMed

Vertes, R. P. (2006). Interactions among the medial prefrontal cortex, hippocampus and midline thalamus in emotional and cognitive processing in the rat. Neuroscience, 142(1), 1–20. https://doi.org/10.1016/j.neuroscience.2006.06.027.CrossRefPubMed

Wu, X., Bai, Y., Tan, T., Li, H., Xia, S., Chang, X., … Dong, Z. (2014). Lithium ameliorates autistic-like behaviors induced by neonatal isolation in rats. Frontiers in Behavioral Neuroscience, 8, 234. https://doi.org/10.3389/fnbeh.2014.00234.PubMedCentralCrossRefPubMed

Xie, Y., Chu, A., Feng, Y., Chen, L., Shao, Y., Luo, Q., … Chen, Y. (2018). MicroRNA-146a: A comprehensive indicator of inflammation and oxidative stress status induced in the brain of chronic T2DM rats. Frontiers in Pharmacology, 9, 478. https://doi.org/10.3389/fphar.2018.00478.PubMedCentralCrossRefPubMed

Yizhar, O. (2012). Optogenetic insights into social behavior function. Biological Psychiatry, 71(12), 1075–1080. https://doi.org/10.1016/j.biopsych.2011.12.029.CrossRefPubMed

Zahra, A., Jiang, J., Chen, Y., Long, C., & Yang, L. (2018). Memantine rescues prenatal citalopram exposure-induced striatal and social abnormalities in mice. Experimental Neurology, 307, 145–154. https://doi.org/10.1016/j.expneurol.2018.06.003.CrossRefPubMed

Titel: Optogenetic Stimulation of the Anterior Cingulate Cortex Ameliorates Autistic-Like Behaviors in Rats Induced by Neonatal Isolation, Caudate Putamen as a Site for Alteration
verfasst von: Elham Sadat Sayed Javad Javaheri
Mohammad Reza Bigdeli
Mohammad Ismail Zibaii
Leila Dargahi
Hamid Reza Pouretemad
Publikationsdatum: 19.02.2019
Verlag: Springer US
Erschienen in: NeuroMolecular Medicine / Ausgabe 2/2019
Print ISSN: 1535-1084
Elektronische ISSN: 1559-1174
DOI: https://doi.org/10.1007/s12017-019-08526-w

Leitlinien kompakt für die Neurologie

Mit medbee Pocketcards sicher entscheiden.

^{Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag}

Kostenlos registrieren

Neu im Fachgebiet Neurologie

25.04.2024 | Hypotonie | Nachrichten

Update Neurologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.

Newsletter bestellen

Springer Medizin

Optogenetic Stimulation of the Anterior Cingulate Cortex Ameliorates Autistic-Like Behaviors in Rats Induced by Neonatal Isolation, Caudate Putamen as a Site for Alteration

Abstract

Leitlinien kompakt für die Neurologie

Neu im Fachgebiet Neurologie

Niedriger diastolischer Blutdruck erhöht Risiko für schwere kardiovaskuläre Komplikationen

Frühe Alzheimertherapie lohnt sich

Viel Bewegung in der Parkinsonforschung

Demenzkranke durch Antipsychotika vielfach gefährdet

Update Neurologie

Springer Medizin

Abstract

Bitte loggen Sie sich ein, um Zugang zu diesem Inhalt zu erhalten

Weitere Artikel der Ausgabe 2/2019

The Emerging Roles of Ferroptosis in Huntington’s Disease

Network Analysis of Depression-Related Transcriptomic Profiles

C9orf72 Intermediate Alleles in Patients with Amyotrophic Lateral Sclerosis, Systemic Lupus Erythematosus, and Rheumatoid Arthritis

Overexpression of Human Mutant PANK2 Proteins Affects Development and Motor Behavior of Zebrafish Embryos

Hydrogen Sulfide Inhibits Formaldehyde-Induced Senescence in HT-22 Cells via Upregulation of Leptin Signaling

The Neuronal Ceroid Lipofuscinoses-Linked Loss of Function CLN5 and CLN8 Variants Disrupt Normal Lysosomal Function

Leitlinien kompakt für die Neurologie

Neu im Fachgebiet Neurologie

Niedriger diastolischer Blutdruck erhöht Risiko für schwere kardiovaskuläre Komplikationen

Frühe Alzheimertherapie lohnt sich

Viel Bewegung in der Parkinsonforschung

Demenzkranke durch Antipsychotika vielfach gefährdet

Update Neurologie