Induction of long-term oscillations in the γ frequency band by nAChR activation in rat hippocampal CA3 area

Neuroscience

Volumn 301, Issue , 2015, Pages 49-60

  Zhang, X ^a   Ge, X Y ^a   Wang, J G ^a   Wang, Y L ^a   Wang, Y ^a   Yu, Y ^a   Li, P P ^a   Lu, C B ^a  

^a XINXIANG MEDICAL UNIVERSITY   (China)

Author keywords

Hippocampus; Long term oscillation; Neural network oscillation; Nicotinic acetylcholine receptor

Indexed keywords

KAINIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NICOTINE; NICOTINIC RECEPTOR; NICOTINIC AGENT; NICOTINIC RECEPTOR ALPHA4BETA2;

ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CONTROLLED STUDY; CORTICAL SYNCHRONIZATION; HIPPOCAMPAL CA3 REGION; LONG TERM OSCILLATION AT GAMMA FREQUENCY BAND; MALE; MOUSE; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NERVOUS SYSTEM PARAMETERS; NEUROTRANSMISSION; NONHUMAN; OSCILLATION; PRIORITY JOURNAL; ANIMAL; DRUG EFFECTS; GAMMA RHYTHM; PHYSIOLOGY; RAT; WISTAR RAT;

ANIMALS; CA3 REGION, HIPPOCAMPAL; GAMMA RHYTHM; KAINIC ACID; MALE; NEURONAL PLASTICITY; NICOTINE; NICOTINIC AGONISTS; RATS; RATS, WISTAR; RECEPTORS, N-METHYL-D-ASPARTATE; RECEPTORS, NICOTINIC;

EID: 84931269294     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2015.05.060     Document Type: Article

References (42)

1. Alkadhi K.A. Chronic stress and Alzheimer's disease-like pathogenesis in a rat model: prevention by nicotine. Curr Neuropharmacol 2011, 9:587-597.
2. Alkondon M., Pereira E.F., Barbosa C.T., Albuquerque E.X. Neuronal nicotinic acetylcholine receptor activation modulates gamma-aminobutyric acid release from CA1 neurons of rat hippocampal slices. J Pharmacol Exp Ther 1997, 283:1396-1411.
3. Andre J.M., Leach P.T., Gould T.J. Nicotine ameliorates NMDA receptor antagonist-induced deficits in contextual fear conditioning through high-affinity nicotinic acetylcholine receptors in the hippocampus. Neuropharmacology 2011, 60:617-625.
4. Anver H., Ward P.D., Magony A., Vreugdenhil M. NMDA receptor hypofunction phase couples independent gamma-oscillations in the rat visual cortex. Neuropsychopharmacology 2011, 36:519-528.
5. Buzsaki G., Wang X.J. Mechanisms of gamma oscillations. Annu Rev Neurosci 2012, 35:203-225.
6. Cheng Q., Yakel J.L. Presynaptic alpha7 nicotinic acetylcholine receptors enhance hippocampal mossy fiber glutamatergic transmission via PKA activation. J Neurosci 2014, 34:124-133.
7. Colgin L.L., Kubota D., Lynch G. Cholinergic plasticity in the hippocampus. Proc Natl Acad Sci USA 2003, 100:2872-2877.
8. Driver J.E., Racca C., Cunningham M.O., Towers S.K., Davies C.H., Whittington M.A., LeBeau F.E. Impairment of hippocampal gamma-frequency oscillations in vitro in mice overexpressing human amyloid precursor protein (APP). Eur J Neurosci 2007, 26:1280-1288.
9. Fisahn A., Neddens J., Yan L., Buonanno A. Neuregulin-1 modulates hippocampal gamma oscillations: implications for schizophrenia. Cereb Cortex 2009, 19:612-618.
10. Fujii S., Ji Z., Sumikawa K. Inactivation of alpha7 ACh receptors and activation of non-alpha7 ACh receptors both contribute to long term potentiation induction in the hippocampal CA1 region. Neurosci Lett 2000, 286:134-138.
11. Fujii S., Jia Y., Yang A., Sumikawa K. Nicotine reverses GABAergic inhibition of long-term potentiation induction in the hippocampal CA1 region. Brain Res 2000, 863:259-265.
12. Hajos M., Hurst R.S., Hoffmann W.E., Krause M., Wall T.M., Higdon N.R., Groppi V.E. The selective alpha7 nicotinic acetylcholine receptor agonist PNU-282987 [N-[(3R)-1-Azabicyclo[2.2.2]oct-3-yl]-4-chlorobenzamide hydrochloride] enhances GABAergic synaptic activity in brain slices and restores auditory gating deficits in anesthetized rats. J Pharmacol Exp Therap 2005, 312:1213-1222.
13. Jefferys J.G., Traub R.D., Whittington M.A. Neuronal networks for induced '40 Hz' rhythms. Trends Neurosci 1996, 19:202-208.
14. Ji D., Dani J.A. Inhibition and disinhibition of pyramidal neurons by activation of nicotinic receptors on hippocampal interneurons. J Neurophysiol 2000, 83:2682-2690.
15. Ji D., Lape R., Dani J.A. Timing and location of nicotinic activity enhances or depresses hippocampal synaptic plasticity. Neuron 2001, 31:131-141.
16. Jia Y., Yamazaki Y., Nakauchi S., Ito K., Sumikawa K. Nicotine facilitates long-term potentiation induction in oriens-lacunosum moleculare cells via Ca2+ entry through non-alpha7 nicotinic acetylcholine receptors. Eur J Neurosci 2010, 31:463-476.
17. Jones S., Yakel J.L. Functional nicotinic ACh receptors on interneurones in the rat hippocampus. J Physiol 1997, 504(Pt 3):603-610.
18. Kawai H., Zago W., Berg D.K. Nicotinic alpha 7 receptor clusters on hippocampal GABAergic neurons: regulation by synaptic activity and neurotrophins. J Neurosci 2002, 22:7903-7912.
19. Li C., Guo Z., Wang Y., Li X., Henderson Z., Lu C.B. A model of synaptic plasticity: activation of mGluR I induced long-term theta oscillations in medial septal diagonal band of rat brain slice. Neurol Sci 2014, 35:551-557.
20. Lu C.B., Henderson Z. Nicotine induction of theta frequency oscillations in rodent hippocampus in vitro. Neuroscience 2010, 166:84-93.
21. Lu W., Man H., Ju W., Trimble W.S., MacDonald J.F., Wang Y.T. Activation of synaptic NMDA receptors induces membrane insertion of new AMPA receptors and LTP in cultured hippocampal neurons. Neuron 2001, 29:243-254.
22. Lu C.B., Vreugdenhil M., Toescu E.C. The effect of aging-associated impaired mitochondrial status on kainate-evoked hippocampal gamma oscillations. Neurobiol Aging 2012.
23. Lu C.B., Wang Z.H., Zhou Y.H., Vreugdenhil M. Temperature- and concentration-dependence of kainate-induced gamma oscillation in rat hippocampal slices under submerged condition. Acta Pharmacol Sin 2012, 33:214-220.
24. Malenka R.C., Bear M.F. LTP and LTD: an embarrassment of riches. Neuron 2004, 44:5-21.
25. Mansvelder H.D., Keath J.R., McGehee D.S. Synaptic mechanisms underlie nicotine-induced excitability of brain reward areas. Neuron 2002, 33:905-919.
26. Matias C.M., Dionisio J.C., Arif M., Quinta-Ferreira M.E. Effect of D-2 amino-5-phosphonopentanoate and nifedipine on postsynaptic calcium changes associated with long-term potentiation in hippocampal CA1 area. Brain Res 2003, 976:90-99.
27. Meyer E.L., Gahring L.C., Rogers S.W. Nicotine preconditioning antagonizes activity-dependent caspase proteolysis of a glutamate receptor. J Biol Chem 2002, 277:10869-10875.
28. Nakao K., Nakazawa K. Brain state-dependent abnormal LFP activity in the auditory cortex of a schizophrenia mouse model. Front Neurosci 2014, 8:168.
29. Nakauchi S., Sumikawa K. Endogenously released ACh and exogenous nicotine differentially facilitate long-term potentiation induction in the hippocampal CA1 region of mice. Eur J Neurosci 2012, 35:1381-1395.
30. Pietersen A.N., Lancaster D.M., Patel N., Hamilton J.B., Vreugdenhil M. Modulation of gamma oscillations by endogenous adenosine through A1 and A2A receptors in the mouse hippocampus. Neuropharmacology 2009, 56:481-492.
31. Sharma G., Grybko M., Vijayaraghavan S. Action potential-independent and nicotinic receptor-mediated concerted release of multiple quanta at hippocampal CA3-mossy fiber synapses. J Neurosci 2008, 28:2563-2575.
32. Song C., Murray T.A., Kimura R., Wakui M., Ellsworth K., Javedan S.P., Marxer-Miller S., Lukas R.J., Wu J. Role of alpha7-nicotinic acetylcholine receptors in tetanic stimulation-induced gamma oscillations in rat hippocampal slices. Neuropharmacology 2005, 48:869-880.
33. Tassin T.C., Benavides D.R., Plattner F., Nishi A., Bibb J.A. Regulation of ERK Kinase by MEK1 Kinase Inhibition in the Brain. J Biol Chem 2015.
34. Traub R.D., Bibbig A., LeBeau F.E., Buhl E.H., Whittington M.A. Cellular mechanisms of neuronal population oscillations in the hippocampus in vitro. Annu Rev Neurosci 2004, 27:247-278.
35. Verret L., Mann E.O., Hang G.B., Barth A.M., Cobos I., Ho K., Devidze N., Masliah E., Kreitzer A.C., Mody I., Mucke L., Palop J.J. Inhibitory interneuron deficit links altered network activity and cognitive dysfunction in Alzheimer model. Cell 2012, 149:708-721.
36. Wang H.L., Chen X.T., Luo L., Lou Z.Y., Wang S., Chen J.T., Wang M., Sun L.G., Ruan D.Y. Reparatory effects of nicotine on NMDA receptor-mediated synaptic plasticity in the hippocampal CA1 region of chronically lead-exposed rats. Eur J Neurosci 2006, 23:1111-1119.
37. Welsby P., Rowan M., Anwyl R. Nicotinic receptor-mediated enhancement of long-term potentiation involves activation of metabotropic glutamate receptors and ryanodine-sensitive calcium stores in the dentate gyrus. Eur J Neurosci 2006, 24:3109-3118.
38. Welsby P.J., Rowan M.J., Anwyl R. Intracellular mechanisms underlying the nicotinic enhancement of LTP in the rat dentate gyrus. Eur J Neurosci 2009, 29:65-75.
39. Yamazaki Y., Jia Y., Hamaue N., Sumikawa K. Nicotine-induced switch in the nicotinic cholinergic mechanisms of facilitation of long-term potentiation induction. Eur J Neurosci 2005, 22:845-860.
40. Yamazaki Y., Jia Y., Niu R., Sumikawa K. Nicotine exposure in vivo induces long-lasting enhancement of NMDA receptor-mediated currents in the hippocampus. Eur J Neurosci 2006, 23:1819-1828.
41. Zappettini S., Grilli M., Lagomarsino F., Cavallero A., Fedele E., Marchi M. Presynaptic nicotinic alpha7 and non-alpha7 receptors stimulate endogenous GABA release from rat hippocampal synaptosomes through two mechanisms of action. PLoS One 2011, 6:e16911.
42. Zhang J., Berg D.K. Reversible inhibition of GABAA receptors by alpha7-containing nicotinic receptors on the vertebrate postsynaptic neurons. J Physiol 2007, 579:753-763.