Warianty tytułu
Języki publikacji
Abstrakty
Previously, autism spectrum disorder (ASD) has been identified mainly by social communication deficits and behavioral symptoms. However, a link between behaviors and learning process in the brain of animal model of autism remained largely unexplored. Particularly, spontaneous neural signaling in learning-related brain areas has not been studied. This study investigated local field potential (LFP) of the hippocampus (HP), the olfactory bulb (OB) and the medial prefrontal cortex (mPFC) in mice prenatally exposed to valproic acid (VPA) on gestational day 13. Adult male Swiss albino mouse offspring implanted with intracranial electrodes were used. VPA-exposed mice exhibited ASD-associated behaviors. Hippocampal LFP analysis revealed that VPA group significantly increased low gamma activity (25–45 Hz) during awake immobility. Regression analyses confirmed positive correlations between locomotor speed and hippocampal theta oscillations in control but not VPA group. VPA group exhibited increases in delta (1–4 Hz) and beta (25–35 Hz) activities in OB during awake immobility and active exploring, respectively. Moreover, significantly increased and decreased coherences between HP and OB of VPA animals were seen within gamma (active exploration) and theta (awake immobility) ranges, respectively. In addition, significant increase in coherence between HP and mPFC was seen within delta range during active exploration. In addition to three ASD symptoms, VPA animals also exhibited differential patterns of olfacto-hippocampal LFP, altered locomotor speed-related hippocampal theta activities and distinct interplays between HP and learning-related brain areas. The altered olfacto-hippocampal and medial prefrontal cortex-hippocampal networks may underlie impairments in autism mouse model.
Wydawca
Czasopismo
Rocznik
Tom
Numer
Opis fizyczny
p.351-363,fig.,ref.
Twórcy
autor
- Department of Physiology, Faculty of Science, Prince of Songkla University, Songkhla, Thailand
autor
- Department of Physiology, Faculty of Science, Prince of Songkla University, Songkhla, Thailand
Bibliografia
- American Psychiatric Association (2013) Diagnostic and statistical manual of mental disorders: DSM-5. American Psychiatric Association, Washington D.C., USA. Baudouin SJ, Gaudias J, Gerharz S, Hatstatt L, Zhou K, Punnakkal P, Tanaka KF, Spooren W, Hen R, De Zeeuw CI, Vogt K, Scheiffele P (2012) Shared synaptic pathophysiology in syndromic and nonsyndromic rodent models of autism. Science 338: 128–132.
- Bristot Silvestrin R, Bambini-Junior V, Galland F, Daniele Bobermim L, Santos A, Torres Abib R, Zanotto C, Batassini C, Brolese G, Gonçalves CA, Riesgo R, Gottfried C (2013) Animal model of autism induced by prenatal exposure to valproate: Altered glutamate metabolism in the hippocampus. Brain Res 1495: 52–60.
- Buzsaki G (2010) Neural syntax: cell assemblies, synapsembles, and readers. Neuron 68: 362–385. Chaste P, Leboyer M (2012) Autism risk factors: genes, environment, and gene-environment interactions. Dialogues Clin Neurosci 14: 281–292.
- Cheaha D, Bumrungsri S, Chatpun S, Kumarnsit E (2015) Characterization of in utero valproic acid mouse model of autism by local field potential in the hippocampus and the olfactory bulb. Neurosci Res 98: 28–34.
- Cheaha D, Sawangjaroen K, Kumarnsit E (2014) Characterization of fluoxetine effects on ethanol withdrawal-induced cortical hyperexcitability by EEG spectral power in rats. Neuropharmacology 77: 49–56.
- Codagnone MG, Podesta MF, Uccelli NA, Reines A (2015) Differential Local Connectivity and Neuroinflammation Profiles in the Medial Prefrontal Cortex and Hippocampus in the Valproic Acid Rat Model of Autism. Dev Neurosci 37: 215–231.
- Dickerson DD, Restieaux AM, Bilkey DK (2012) Clozapine administration ameliorates disrupted long-range synchrony in a neurodevelopmental animal model of schizophrenia. Schizophr Res 135: 112–115.
- Dickerson DD, Wolff AR, Bilkey DK (2010) Abnormal long-range neural synchrony in a maternal immune activation animal model of schizophrenia. J Neurosci 30: 12424–12431.
- European Science Foundation (2001) Use of Animals in Research. http://www.esf.org/fileadmin/Public_do. Favre MR, Barkat TR, LaMendola D, Khazen G, Markram H, Markram K (2013) General developmental health in the VPA-rat model of autism. Front Behav Neurosci 7: 88.
- Gandal MJ, Edgar JC, Ehrlichman RS, Mehta M, Roberts TP, Siegel SJ (2010) Validating gamma oscillations and delayed auditory responses as translational biomarkers of autism. Biol Psychiatry 68: 1100–1106.
- Gogolla N, LeBlanc JJ, Quast KB, Südhof TC, Fagiolini M, Hensch TK (2009) Common circuit defect of excitatoryinhibitory balance in mouse models of autism. J Neurodev Disord 1: 172–181.
- Hara Y, Takuma K, Takano E, Katashiba K, Taruta A, Higashino K, Hashimoto H, Ago Y, Matsuda T (2015) Reduced prefrontal dopaminergic activity in valproic acid-treated mouse autism model. Behav Brain Res 1: 39–47.
- National Research Council Institute for Laboratory Animal Research (2004) The Development of Science-based Guidelines for Laboratory Animal Care: Proceedings of the November 2003 International Workshop. National Academies Press, Washington DC, USA. Jamain S, Quach H, Betancur C, Rastam M, Colineaux C, Gillberg IC, Soderstrom H, Giros B, Leboyer M, Gillberg C, Bourgeron T (2003) Mutations of the X-linked genes encoding neuroligins NLGN3 and NLGN4 are associated with autism. Nat Genet 34: 27–29.
- Kim KC, Kim P, Go HS, Choi CS, Park JH, Kim HJ, Jeon SJ, dela Pena IC, Han SH, Cheong JH, Ryu JH, Shin CY (2013) Male-specific alteration in excitatory post-synaptic development and social interaction in pre-natal valproic acid exposure model of autism spectrum disorder. J Neurochem 124: 832–843.
- Kim KC, Kim P, Go HS, Choi CS, Yang SI, Cheong JH, Shin CY, Ko KH (2011) The critical period of valproate exposure to induce autistic symptoms in Sprague-Dawley rats. Toxicol Lett 201: 137–142.
- Kolozsi E, Mackenzie RN, Roullet FI, Decatanzaro D, Foster JA (2009) Prenatal exposure to valproic acid leads to reduced expression of synaptic adhesion molecule neuroligin 3 in mice. Neuroscience 163: 1201–1210.
- Lin DY, Zhang SZ, Block E, Katz LC (2005) Encoding social signals in the mouse main olfactory bulb. Nature 434: 470–477.
- Markram K, Rinaldi T, Mendola DL, Sandi C, Markram H (2007) Abnormal Fear Conditioning and Amygdala Processing in an Animal Model of Autism. Neuropsychopharmacology 33: 901–912.
- Martin C, Beshel J, Kay LM (2007) An Olfacto-hippocampal network is dynamically involved in odor-discrimination learning. J Neurophysiol 98: 2196–2205.
- Meador KJ, Baker GA, Browning N, Clayton-Smith J, Combs-Cantrell DT, Cohen M, Kalayjian LA, Kanner A, Liporace JD, Pennell PB, Privitera M, Loring DW (2009) Cognitive function at 3 years of age after fetal exposure to antiepileptic drugs. N Engl J Med 360: 1597–1605.
- Miyazaki K, Narita N, Narita M (2005) Maternal administration of thalidomide or valproic acid causes abnormal serotonergic neurons in the offspring: implication for pathogenesis of autism. Int J Dev Neurosci 23: 287–297.
- Moldrich RX, Leanage G, She D, Dolan-Evans E, Nelson M, Reza N, Reutens DC (2013) Inhibition of histone deacetylase in utero causes sociability deficits in postnatal mice. Behav Brain Res 257: 253–264.
- Murray EK, Varnum MM, Fernandez JL, de Vries GJ, Forger NG (2011) Effects of neonatal treatment with valproic acid on vasopressin immunoreactivity and olfactory behaviour in mice. J Neuroendocrinol 23: 906–914.
- Narita M, Oyabu A, Imura Y, Kamada N, Yokoyama T, Tano K, Uchida A, Narita N (2010) Nonexploratory movement and behavioral alterations in a thalidomide or valproic acid-induced autism model rat. Neurosci Res 66: 2–6.
- Ornoy A (2009) Valproic acid in pregnancy: How much are we endangering the embryo and fetus?. Reprod Toxicol 28: 1–10.
- Orekhova EV, Stroganova TA, Prokofyev AO, Nygren G, Gillberg C, and Elam M (2008) Sensory gating in young children with autism: Relation to age, IQ, and EEG gamma oscillations. Neurosci Lett 434: 218–223.
- Paxinos G, Franklin KBJ (1998) The mouse brain in stereotaxic coordinates. Academic Press, San Diego–California– London, USA–UK. Phiel CJ, Zhang F, Huang EY, Guenther MG, Lazar MA, Klein PS (2001) Histone deacetylase is a direct target of valproic acid, a potent anticonvulsant, mood stabilizer, and teratogen. J Biol Chem 276: 36734–36741.
- Rice D, Barone S (2000) Critical periods of vulnerability for the developing nervous system: evidence from humans and animal models. Environ Health Perspect 3: 511– 533.
- Rinaldi T, Kulangara K, Antoniello K, Markram H (2007) Elevated NMDA receptor levels and enhanced postsynaptic long-term potentiation induced by prenatal exposure to valproic acid. Proc Natl Acad Sci U S A: 13501– 13506.
- Rinaldi T, Perrodin C, Markram H (2008) Hyper-Connectivity and Hyper-Plasticity in the Medial Prefrontal Cortex in the Valproic Acid Animal Model of Autism. Front Neural Circuits 2: 4. Rubenstein JLR, Merzenich MM (2003) Model of autism: increased ratio of excitation/inhibition in key neural systems. Genes Brain Behav 2: 255–267.
- Schneider T, Przewłocki R (2004) Behavioral alterations in rats prenatally exposed to valproic acid: animal model of autism. Neuropsychopharmacology 30: 80–89.
- Shen C, Huo LR, Zhao XL, Wang PR, Zhong N (2015) Novel interactive partners of neuroligin 3: new aspects for pathogenesis of autism. J Mol Neurosci 56: 89–101.
- Shin J, Talnov A, Matsumoto G, Brankack J (2001) Hippocampal theta rhythm and running speed: A reconsideration using within-single trial analysis. Neurocomputing 38: 1567–1574.
- Sigurdsson T, Stark KL, Karayiorgou M, Gogos JA, Gordon JA (2010) Impaired hippocampal-prefrontal synchrony in a genetic mouse model of schizophrenia. Nature 464(7289): 763–767.
- Silva GT, Le Bé JV, Riachi I, Rinaldi T, Markram K, Markram H (2009) Enhanced long term microcircuit plasticity in the valproic acid animal model of autism. Front Synaptic Neurosci 1: 1. Sosa-Díaz N, Bringas ME, Atzori M, Flores G (2014) Prefrontal cortex, hippocampus, and basolateral amygdala plasticity in a rat model of autism spectrum. Synapse 68: 468–473.
- Strömland K, Nordin V, Miller M, Akerström B, Gillberg C (1994) Autism in thalidomide embryopathy: a population study. Dev Med Child Neurol 36: 351–356.
- Tadel F, Baillet S, Mosher JC, Pantazis D, Leahy RM (2011) Brainstorm: A user-friendly application for MEG/EEG analysis. Comput Intell Neurosci 2011: 879716.
- Uhlhaas PJ, Roux F, Singer W, Haenschel C, Sireteanu R, Rodriguez E (2009) The development of neural synchrony reflects late maturation and restructuring of functional networks in humans. Proc Natl Acad Sci U S A 106: 9866–9871.
- Uylings HB, Groenewegen HJ, Kolb B (2003) Do rats have a prefrontal cortex?. Behav Brain Res 146: 3–17.
- Volk HE, Kerin T, Lurmann F, Hertz-Picciotto I, McConnell R, Campbell DB (2014) Autism spectrum disorder: interaction of air pollution with the MET receptor tyrosine kinase gene. Epidemiology 25: 44–47.
- Vorhees CV, Rauch SL, Hitzemann RJ (1991) Prenatal valproic acid exposure decreases neuronal membrane order in rat offspring hippocampus and cortex. Neurotoxicol Teratol 13(4): 471–474.
- Whishaw IQ, Vanderwolf CH (1973) Hippocampal EEG and behavior: Change in amplitude and frequency of RSA (Theta rhythm) associated with spontaneous and learned movement patterns in rats and cats. Behav Biol 8: 461– 484.
- Williams G, King J, Cunningham M, Stephan M, Kerr B, Hersh JH (2001) Fetal valproate syndrome and autism: additional evidence of an association. Dev Med Child Neurol 43: 202–206.
- Willsey AJ, Sanders SJ, Li M, Dong S, Tebbenkamp AT, Muhle RA, Reilly SK, Lin L, Fertuzinhos S, Miller JA, Murtha MT, Bichsel C, Niu W, Cotney J, ErcanSencicek AG, Gockley J, Gupta A, Han W, He X, Hoffman E, Klei L, Lei J, Liu W, Liu L, Lu C, Xu X, Zhu Y, Mane SM, Lein ES, Wei L, Noonan JP, Roeder K, Devlin B, Sestan N, State M (2013) Coexpression networks implicate human midfetal deep cortical projection neurons in the pathogenesis of autism. Cell 155: 997–1007.
- Yanovsky Y, Ciatipis M, Draguhn A, Tort AB, Brankačk J (2014) Slow oscillations in the mouse hippocampus entrained by nasal respiration. J Neurosci 34(17): 5949– 5964.
Typ dokumentu
Bibliografia
Identyfikatory
Identyfikator YADDA
bwmeta1.element.agro-bbe9324c-5c31-463e-8030-367d6f71fb66