Top

Published in:

01-11-2015 | Original Paper

Effects of Hydrogen Sulfide on Modulation of Theta–Gamma Coupling in Hippocampus in Vascular Dementia Rats

Authors: Xiaxia Xu, Chunhua Liu, Zhanyong Li, Tao Zhang

Published in: Brain Topography | Issue 6/2015

Abstract

Our previous study showed that hydrogen sulfide (H₂S) could alleviate the cognitive deficits in vascular dementia (VD) rats associated with the improvement of synaptic plasticity. Neural oscillations are reported to interact with each other through either identical-frequency or cross-frequency coupling. This study examined whether impaired neural couplings could be alleviated by H₂S in the hippocampal CA3–CA1 of VD rats and explored its possible mechanism. A VD rat model was established by two-vessel occlusion. Sodium hydrosulfide (NaHS), a kind of H₂S donor, was administered intraperitoneally (5.6 mg/kg/day) for 3 weeks. Local field potentials were simultaneously collected in the hippocampal CA3 and CA1. The effects of NaHS on the modulation of theta–gamma coupling were evaluated by using the measurements of both phase–phase coupling and phase–amplitude coupling, while several other approaches including behavior, electrophysiology, western blot, immunofluorescence staining were also employed. The results showed that NaHS significantly prevented spatial learning and memory impairments (p < 0.01). NaHS considerably alleviated the impairment of neural coupling in VD rats in an identical-frequency rhythm and between cross-frequency bands. Moreover, the expression of cystathionine-β-synthase (CBS) was markedly attenuated in VD rats. NaHS elevated the expression of CBS to maintain the intrinsic balance of H₂S. Interestingly, it was observed that NaHS increased the protein expression of N-methyl-d-aspartic acid receptor 2A (NMDAR2A) in VD rats. In conclusion, the data suggest that NaHS played the neuroprotective role partly via modulating the expression of NMDAR2A in order to alleviate the impairments of neural couplings in VD rats.

Abe K, Kimura H (1996) The possible role of hydrogen sulfide as an endogenous neuromodulator. J Neurosci 16:1066–1071PubMed

Akaike H (1974) A new look at the statistical model identification. IEEE Trans Autom Control 19:716–723CrossRef

Baccala LA, Sameshima K, Takahashi DY (2007) Generalized partial directed coherence. Proceedings of the 2007 15th international conference on digital signal processing, 163–166

Barth AMI, Mody I (2011) Changes in hippocampal neuronal activity during and after unilateral selective hippocampal ischemia in vivo. J Neurosci 31:851–860CrossRefPubMed

Behrendt RP (2010) Contribution of hippocampal region CA3 to consciousness and schizophrenic hallucinations. Neurosci Biobehav Rev 34:1121–1136CrossRefPubMed

Belluscio MA, Mizuseki K, Schmidt R, Kempter R, Buzsaki G (2012) Cross-frequency phase–phase coupling between theta and gamma oscillations in the hippocampus. J Neurosci 32:423–435PubMedCentralCrossRefPubMed

Billings LM, Oddo S, Green KN, McGaugh JL, LaFerla FM (2005) Intraneuronal Aβ causes the onset of early Alzheimer’s disease-related cognitive deficits in transgenic mice. Neuron 45:675–688CrossRefPubMed

Buzsaki G (2010) Neural syntax: cell assemblies, synapsembles, and readers. Neuron 68:362–385PubMedCentralCrossRefPubMed

Buzsaki G, Draguhn A (2004) Neuronal oscillations in cortical networks. Science 304:1926–1929CrossRefPubMed

Caixeta FV, Cornélio AM, Scheffer-Teixeira R, Ribeiro S, Tort ABL (2013) Ketamine alters oscillatory coupling in the hippocampus. Sci Rep 3:2348. doi:10.1038/srep02348

Canolty RT, Edwards E, Dalal SS, Soltani M, Nagarajan SS, Kirsch HE, Berger MS, Barbaro NM, Knight RT (2006) High gamma power is phase-locked to theta oscillations in human neocortex. Science 313:1626–1628PubMedCentralCrossRefPubMed

Debanne D, Guerineau NC, Gahwiler BH, Thompson SM (1995) Physiology and pharmacology of unitary synaptic connections between pairs of cells in areas CA3 and CA1 of rat hippocampal slice cultures. J Neurophysiol 73:1282–1294PubMed

Dello Russo C, Tringali G, Ragazzoni E, Maggiano N, Menini E, Vairano M, Preziosi P, Navarra P (2000) Evidence that hydrogen sulphide can modulate hypothalamo-pituitary-adrenal axis function: in vitro and in vivo studies in the rat. J Neuroendocrinol 12:225–233CrossRefPubMed

Delorme A, Makeig S (2004) EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. J Neurosci Methods 134:9–21CrossRefPubMed

Fein G, Di Sclafani V, Tanabe J, Cardenas V, Weiner MW, Jagust WJ, Reed BR, Norman D, Schuff N, Kusdra L, Greenfield T, Chui H (2000) Hippocampal and cortical atrophy predict dementia in subcortical ischemic vascular disease. Neurology 55:1626–1635PubMedCentralCrossRefPubMed

Fell J, Axmacher N (2011) The role of phase synchronization in memory processes. Nat Rev Neurosci 12:105–118CrossRefPubMed

Fell J, Klaver P, Lehnertz K, Grunwald T, Schaller C, Elger CE, Fernandez G (2001) Human memory formation is accompanied by rhinal–hippocampal coupling and decoupling. Nat Neurosci 4:1259–1264CrossRefPubMed

Ford JM, Roach BJ, Hoffman RS, Mathalon DH (2008) The dependence of P300 amplitude on gamma synchrony breaks down in schizophrenia. Brain Res 1235:133–142PubMedCentralCrossRefPubMed

Gallinat J, Kunz D, Senkowski D, Kienast T, Seifert F, Schubert F, Heinz A (2006) Hippocampal glutamate concentration predicts cerebral theta oscillations during cognitive processing. Psychopharmacology 187:103–111CrossRefPubMed

Gerstner W, Kempter R, van Hemmen JL, Wagner H (1996) A neuronal learning rule for sub-millisecond temporal coding. Nature 383:76–81CrossRefPubMed

Gosselin N, Johnston K, Leclerc S, Montplaisir J, Lassonde M (2001) Deficits in the early and late stages of auditory information processing in brain concussed patients. Int J Psychophysiol 41:218

Goutagny R, Krantic S (2013) Hippocampal oscillatory activity in Alzheimer’s disease: toward the identification of early biomarkers? Aging Dis 4:134–140PubMedCentralPubMed

Gupta YK, Dahiya AK, Reeta KH (2010) Gaso-transmitter hydrogen sulphide: potential new target in pharmacotherapy. Indian J Exp Biol 48:1069–1077PubMed

Hakami T, Jones NC, Tolmacheva EA, Gaudias J, Chaumont J, Salzberg M, O’Brien TJ, Pinault D (2009) NMDA receptor hypofunction leads to generalized and persistent aberrant gamma oscillations independent of hyperlocomotion and the state of consciousness. Plos One 4:e6755PubMedCentralCrossRefPubMed

Hardingham GE, Fukunaga Y, Bading H (2002) Extrasynaptic NMDARs oppose synaptic NMDARs by triggering CREB shut-off and cell death pathways. Nat Neurosci 5:405–414PubMed

Iadecola C (2013) The pathobiology of vascular dementia. Neuron 80:844–866CrossRefPubMed

Jensen O, Lisman JE (1996) Theta/gamma networks with slow NMDA channels learn sequences and encode episodic memory: role of NMDA channels in recall. Learn Mem 3:264–278CrossRefPubMed

Kahana MJ, Seelig D, Madsen JR (2001) Theta returns. Curr Opin Neurobiol 11:739–744CrossRefPubMed

Kimura H (2000) Hydrogen sulfide induces cyclic AMP and modulates the NMDA receptor. Biochem Biophys Res Commun 267:129–133CrossRefPubMed

Kimura H (2002) Hydrogen sulfide as a neuromodulator. Mol Neurobiol 26:13–19CrossRefPubMed

Kittelberger K, Hur EE, Sazegar S, Keshavan V, Kocsis B (2012) Comparison of the effects of acute and chronic administration of ketamine on hippocampal oscillations: relevance for the NMDA receptor hypofunction model of schizophrenia. Brain Struct Funct 217:395–409PubMedCentralCrossRefPubMed

Kocsis B (2012) Differential role of NR2A and NR2B subunits in N-methyl-d-aspartate receptor antagonist-induced aberrant cortical gamma oscillations. Biol Psychiatry 71:987–995PubMedCentralCrossRefPubMed

Kramer MA, Tort AB, Kopell NJ (2008) Sharp edge artifacts and spurious coupling in EEG frequency comodulation measures. J Neurosci Methods 170:352–357CrossRefPubMed

Lachaux JP, Rodriguez E, Martinerie J, Varela FJ (1999) Measuring phase synchrony in brain signals. Hum Brain Mapp 8:194–208CrossRefPubMed

Li Z, Wang Y, Xie Y, Yang Z, Zhang T (2011) Protective effects of exogenous hydrogen sulfide on neurons of hippocampus in a rat model of brain ischemia. Neurochem Res 36:1840–1849CrossRefPubMed

Lisman JE, Idiart MA (1995) Storage of 7 ± 2 short-term memories in oscillatory subcycles. Science 267:1512–1515CrossRefPubMed

Liu CH, Liu Y, Yang Z (2014) Myocardial infarction induces cognitive impairment by increasing the production of hydrogen peroxide in adult rat hippocampus. Neurosci Lett 560:112–116CrossRefPubMed

Maerz S, Liu CH, Guo W, Zhu YZ (2011) Anti-ischaemic effects of bilobalide on neonatal rat cardiomyocytes and the involvement of the platelet-activating factor receptor. Biosci Rep 31:439–447PubMedCentralCrossRefPubMed

Markram H, Lubke J, Frotscher M, Sakmann B (1997) Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs. Science 275:213–215CrossRefPubMed

Mitra P, Bokil H (2008) Observed brain dynamics. Oxford University Press, New York

Olivares D, Deshpande VK, Shi Y, Lahiri DK, Greig NH, Rogers JT, Huang XD (2012) N-methyl d-aspartate (NMDA) receptor antagonists and memantine treatment for Alzheimer’s disease, vascular dementia and Parkinson’s disease. Curr Alzheimer Res 9:746–758CrossRefPubMed

Palu M, Stefanovska A (2003) Direction of coupling from phases of interacting oscillators: an information-theoretic approach. Phys Rev E 67:55201CrossRef

Palu M, Komárek V, Hrní Z, těrbová K (2001) Synchronization as adjustment of information rates: detection from bivariate time series. Phys Rev E 63:46211CrossRef

Paxinos G, Watson C (2007) The rat brain in stereotaxic coordinates. Academic Press/Elsevier, Amsterdam, Boston

Penny WD, Duzel E, Miller KJ, Ojemann JG (2008) Testing for nested oscillation. J Neurosci Methods 174:50–61PubMedCentralCrossRefPubMed

Tanovic A, Alfaro V (2006) Glutamate-related excitoxicity neuroprotection with memantine, an uncompetitive antagonist of NMDA-glutamate receptor, in Alzheimer’s disease and vascular dementia. Rev Neurologia 42:607–616

Tass P, Rosenblum MG, Weule J, Kurths J, Pikovsky A, Volkmann J, Schnitzler A, Freund HJ (1998) Detection of n:m phase locking from noisy data: application to magnetoencephalography. Phys Rev Lett 81:3291–3294CrossRef

Taxidis J, Coomber B, Mason R, Owen M (2010) Assessing cortico-hippocampal functional connectivity under anesthesia and kainic acid using generalized partial directed coherence. Biol Cybern 102:327–340CrossRefPubMed

Thomson DJ (1982) Spectrum estimation and harmonic analysis. Proc IEEE 70:1055–1096CrossRef

Tropini G, Chiang J, Wang Z, McKeown MJ (2009) Partial directed coherence-based information flow in Parkinson’s disease patients performing a visually-guided motor task. Conf Proc IEEE Eng Med Biol Soc 2009:1873–1878PubMed

Tuffrey-Wijne I, Watchman K (2014) Sharing the diagnosis of dementia: breaking bad news to people with intellectual disabilities. J Appl Res Intellect 27:357CrossRef

van der Meer MAA, Redish AD (2011) Theta phase precession in rat ventral striatum links place and reward information. J Neurosci 31:2843–2854PubMedCentralCrossRefPubMed

Varela F, Lachaux JP, Rodriguez E, Martinerie J (2001) The brainweb: phase synchronization and large-scale integration. Nat Rev Neurosci 2:229–239CrossRefPubMed

von Stein A, Sarnthein J (2000) Different frequencies for different scales of cortical integration: from local gamma to long range alpha/theta synchronization. Int J Psychophysiol 38:301–313CrossRef

Wang R (2002) Two’s company, three’s a crowd: can H2S be the third endogenous gaseous transmitter? FASEB J 16:1792–1798CrossRefPubMed

Xu X, Li Z, Yang Z, Zhang T (2012) Decrease of synaptic plasticity associated with alteration of information flow in a rat model of vascular dementia. Neuroscience 206:136–143CrossRefPubMed

Xu XX, An L, Mi XC, Zhang T (2013a) Impairment of cognitive function and synaptic plasticity associated with alteration of information flow in theta and gamma oscillations in melamine-treated rats. Plos One 8:e77796PubMedCentralCrossRefPubMed

Xu XX, Zheng CG, Zhang T (2013b) Reduction in LFP cross-frequency coupling between theta and gamma rhythms associated with impaired STP and LTP in a rat model of brain ischemia. Front Comput Neurosci 7:27PubMedCentralCrossRefPubMed

Yener GG, Guntekin B, Oniz A, Basar E (2007) Increased frontal phase-locking of event-related theta oscillations in Alzheimer patients treated with cholinesterase inhibitors. Int J Psychophysiol 64:46–52CrossRefPubMed

Zhang XZ, Bian JS (2014) Hydrogen Sulfide: a neuromodulator and neuroprotectant in the central nervous system. ACS Chem Neurosci 5:876–883CrossRefPubMed

Zhang M, Zheng C, Quan M, An L, Yang Z, Zhang T (2011) Directional indicator on neural oscillations as a measure of synaptic plasticity in chronic unpredictable stress rats. Neurosignals 19:189–197CrossRefPubMed

Zheng C, Zhang T (2013) Alteration of phase-phase coupling between theta and gamma rhythms in a depression-model of rats. Cogn Neurodyn 7(2):167–172PubMedCentralCrossRefPubMed

Zheng C, Quan M, Yang Z, Zhang T (2011) Directionality index of neural information flow as a measure of synaptic plasticity in chronic unpredictable stress rats. Neurosci Lett 490:52–56CrossRefPubMed

Title: Effects of Hydrogen Sulfide on Modulation of Theta–Gamma Coupling in Hippocampus in Vascular Dementia Rats
Authors: Xiaxia Xu
Chunhua Liu
Zhanyong Li
Tao Zhang
Publication date: 01-11-2015
Publisher: Springer US
Published in: Brain Topography / Issue 6/2015
Print ISSN: 0896-0267
Electronic ISSN: 1573-6792
DOI: https://doi.org/10.1007/s10548-015-0430-x

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Effects of Hydrogen Sulfide on Modulation of Theta–Gamma Coupling in Hippocampus in Vascular Dementia Rats

Abstract

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 6/2015

Localization of Epileptogenic Zone on Pre-surgical Intracranial EEG Recordings: Toward a Validation of Quantitative Signal Analysis Approaches

Real-Time MEG Source Localization Using Regional Clustering

MEG–EEG Information Fusion and Electromagnetic Source Imaging: From Theory to Clinical Application in Epilepsy

Somatosensory Event-Related Potentials and Association with Tactile Behavioral Responsiveness Patterns in Children with ASD

Hemodynamic and EEG Time-Courses During Unilateral Hand Movement in Patients with Cortical Myoclonus. An EEG-fMRI and EEG-TD-fNIRS Study

Modulation of Posterior Alpha Activity by Spatial Attention Allows for Controlling A Continuous Brain–Computer Interface