C-type natriuretic peptide decreases hippocampal network oscillations in adult rats in vitro

Neuroscience

Volumn 164, Issue 4, 2009, Pages 1764-1775

  Decker, J M ^a   Wojtowicz A M ^a   Haq, R Ul ^a   Braunewell, K H ^a   Heinemann, U ^a   Behrens, C J ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

C type natriuretic peptides; gamma; natriuretic peptide receptor B; network oscillations; ripples; sharp waves

Indexed keywords

ACETYLCHOLINE; GLUTAMATE DECARBOXYLASE 65; GLUTAMATE DECARBOXYLASE 67; NATRIURETIC PEPTIDE TYPE C; NEUROPEPTIDE; PHYSOSTIGMINE;

ANIMAL TISSUE; ARTICLE; BRAIN REGION; BRAIN SLICE; CEREBROSPINAL FLUID; COGNITION; CONTROLLED STUDY; HIPPOCAMPUS; HYPERPOLARIZATION; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; INFORMATION STORAGE; INTERNEURON; LONG TERM POTENTIATION; MEMORY CONSOLIDATION; NERVOUS SYSTEM CONDUCTANCE; NONHUMAN; OSCILLATION; PRIORITY JOURNAL; PROTEIN BINDING; RAT; RECEPTOR BINDING;

ACETYLCHOLINE; ANIMALS; ELECTRIC STIMULATION; FEMALE; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; INTERNEURONS; NATRIURETIC PEPTIDE, C-TYPE; NERVE NET; PERIODICITY; PHYSOSTIGMINE; PROTEIN BINDING; PYRAMIDAL CELLS; RATS; RATS, WISTAR; RECEPTORS, ATRIAL NATRIURETIC FACTOR; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 70449523224     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2009.09.036     Document Type: Article

References (57)

1. Bains J.S., Longacher J.M., and Staley K.J. Reciprocal interactions between CA3 network activity and strength of recurrent collateral synapses. Nat Neurosci 2 (1999) 720-726
2. Bartos M., Vida I., and Jonas P. Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks. Nat Rev Neurosci 8 (2007) 45-56
3. Behrens C.J., van den Boom L.P., de Hoz L., Friedman A., and Heinemann U. Induction of sharp wave-ripple complexes in vitro and reorganization of hippocampal networks. Nat Neurosci 8 (2005) 1560-1567
4. Behrens C.J., van den Boom L.P., and Heinemann U. Effects of the GABA(A) receptor antagonists bicuculline and gabazine on stimulus-induced sharp wave-ripple complexes in adult rat hippocampus in vitro. Eur J Neurosci 25 (2007) 2170-2181
5. Biro E., Toth G., and Telegdy G. Effect of receptor blockers on brain natriuretic peptide and C-type natriuretic peptide caused anxiolytic state in rats. Neuropeptides 30 (1996) 59-65
6. Both M., Bähner F., von Bohlen und Halbach O., and Draguhn A. Propagation of specific network patterns through the mouse hippocampus. Hippocampus 18 9 (2008) 899-908
7. Bragin A., Jandó G., Nádasdy Z., Hetke J., Wise K., and Buzsáki G. Gamma (40-100 Hz) oscillation in the hippocampus of the behaving rat. J Neurosci 15 (1995) 47-60
8. Buzsaki G. Hippocampal sharp waves: their origin and significance. Brain Res 398 (1986) 242-252
9. Buzsaki G. Two-stage model of memory trace formation: a role for "noisy" brain states. Neuroscience 31 (1989) 551-570
10. Buzsáki G. Memory consolidation during sleep: a neurophysiological perspective. J Sleep Res 7 (1998) 17-23
11. Buzsaki G., Buhl D.L., Harris K.D., Csicsvari J., Czeh B., and Morozov A. Hippocampal network patterns of activity in the mouse. Neuroscience 116 (2003) 201-211
12. Buzsaki G., and Chrobak J.J. Synaptic plasticity and self-organization in the hippocampus. Nat Neurosci 8 (2005) 1418-1420
13. Buzsaki G., Geisler C., Henze D.A., and Wang X.J. Interneuron diversity series: circuit complexity and axon wiring economy of cortical interneurons. Trends Neurosci 27 (2004) 186-193
14. Cahill L., and McGaugh J.L. Mechanisms of emotional arousal and lasting declarative memory. Trends Neurosci 21 (1998) 294-299
15. Cauli B., Audinat E., Lambolez B., Angulo M.C., Ropert N., Tsuzuki K., Hestrin S., and Rossier J. Molecular and physiological diversity of cortical nonpyramidal cells. J Neurosci 17 (1997) 3894-3906
16. Chrobak J.J., and Buzsáki G. Gamma oscillations in the entorhinal cortex of the freely behaving rat. J Neurosci 18 (1998) 388-398
17. Colgin L.L., Jia Y., Sabatier J.M., and Lynch G. Blockade of NMDA receptors enhances spontaneous sharp waves in rat hippocampal slices. Neurosci Lett 385 (2005) 46-51
18. Decker J.M., Wojtowicz A., Heinemann U., and Braunewell K.H. C-type natriuretic peptide modulates pre- and postsynaptic properties in hippocampal area CA1 in vitro. Biochem Biophys Res Commun 377 (2008) 820-825
19. Deschepper C.F., and Picard S. Effects of C-type natriuretic peptide on rat astrocytes: regional differences and characterization of receptors. J Neurochem 62 (1994) 1974-1982
20. Dugladze T., Vida I., Tort A.B., Gross A., Otahal J., Heinemann U., Kopell N.J., and Gloveli T. Impaired hippocampal rhythmogenesis in a mouse model of mesial temporal lobe epilepsy. Proc Natl Acad Sci U S A 104 (2007) 17530-17535
21. Fisahn A., Pike F.G., Buhl E.H., and Paulsen O. Cholinergic induction of network oscillations at 40 Hz in the hippocampus in vitro. Nature 394 (1998) 186-189
22. Freund T.F. Interneuron diversity series: rhythm and mood in perisomatic inhibition. Trends Neurosci 26 (2003) 489-495
23. Gloveli T., Dugladze T., Rotstein H.G., Traub R.D., Monyer H., Heinemann U., Whittington M.A., and Kopell N.J. Orthogonal arrangement of rhythm-generating microcircuits in the hippocampus. Proc Natl Acad Sci U S A 102 (2005) 13295-13300
24. Gloveli T., Dugladze T., Saha S., Monyer H., Heinemann U., Traub R.D., Whittington M.A., and Buhl E.H. Differential involvement of oriens/pyramidale interneurones in hippocampal network oscillations in vitro. J Physiol 562 (2005) 131-147
25. Hablitz J.J. Picrotoxin-induced epileptiform activity in hippocampus: role of endogenous versus synaptic factors. J Neurophysiol 51 (1984) 1011-1027
26. Hajos N., Ellender T.J., Zemankovics R., Mann E.O., Exley R., Cragg S.J., Freund T.F., and Paulsen O. Maintaining network activity in submerged hippocampal slices: importance of oxygen supply. Eur J Neurosci 29 (2009) 319-327
27. Hajos N., Katona I., Naiem S.S., Mackie K., Ledent C., Mody I., and Freund T.F. Cannabinoids inhibit hippocampal GABAergic transmission and network oscillations. Eur J Neurosci 12 (2000) 3239-3249
28. Herman J.P., Dolgas C.M., Rucker D., and Langub Jr. M.C. Localization of natriuretic peptide-activated guanylate cyclase mRNAs in the rat brain. J Comp Neurol 369 (1996) 165-187
29. Hormuzdi S.G., Pais I., LeBeau F.E., Towers S.K., Rozov A., Buhl E.H., Whittington M.A., and Monyer H. Impaired electrical signaling disrupts gamma frequency oscillations in connexin 36-deficient mice. Neuron 31 (2001) 487-495
30. Klausberger T., Magill P.J., Marton L.F., Roberts J.D., Cobden P.M., Buzsaki G., and Somogyi P. Brain-state- and cell-type-specific firing of hippocampal interneurons in vivo. Nature 421 (2003) 844-848
31. Klausberger T., Marton L.F., O'Neill J., Huck J.H., Dalezios Y., Fuentealba P., Suen W.Y., Papp E., Kaneko T., Watanabe M., Csicsvari J., and Somogyi P. Complementary roles of cholecystokinin- and parvalbumin-expressing GABAergic neurons in hippocampal network oscillations. J Neurosci 25 (2005) 9782-9793
32. Klausberger T., and Somogyi P. Neuronal diversity and temporal dynamics: the unity of hippocampal circuit operations. Science 321 (2008) 53-57
33. Langub Jr. M.C., Watson Jr. R.E., and Herman J.P. Distribution of natriuretic peptide precursor mRNAs in the rat brain. J Comp Neurol 356 (1995) 183-199
34. Luhmann H.J., and Prince D.A. Postnatal maturation of the GABAergic system in rat neocortex. J Neurophysiol 65 (1991) 247-263
35. Maier N., Nimmrich V., and Draguhn A. Cellular and network mechanisms underlying spontaneous sharp wave-ripple complexes in mouse hippocampal slices. J Physiol 550 (2003) 873-887
36. Miles R., and Wong R.K.S. Single neurones can initiate synchronized population discharge in the hippocampus. Nature 306 (1983) 371-373
37. Montkowski A., Jahn H., Strohle A., Poettig M., Holsboer F., and Wiedemann K. C-type natriuretic peptide exerts effects opposing those of atrial natriuretic peptide on anxiety-related behaviour in rats. Brain Res 792 (1998) 358-360
38. Poschel B., Heinemann U., and Draguhn A. High frequency oscillations in the dentate gyrus of rat hippocampal slices induced by tetanic stimulation. Brain Res 959 (2003) 320-327
39. Romo-Parra H., Trevino M., Heinemann U., and Gutierrez R. GABA actions in hippocampal area CA3 during postnatal development: differential shift from depolarizing to hyperpolarizing in somatic and dendritic compartments. J Neurophysiol 99 (2008) 1523-1534
40. Schneiderman J.H. Low concentrations of penicillin reveal rhythmic, synchronous synaptic potentials in hippocampal slice. Brain Res 398 (1986) 231-241
41. Schuchmann S., Meierkord H., Stenkamp K., Breustedt J., Windmuller O., Heinemann U., and Buchheim K. Synaptic and nonsynaptic ictogenesis occurs at different temperatures in submerged and interface rat brain slices. J Neurophysiol 87 (2002) 2929-2935
42. Schwartzkroin P.A., and Prince D.A. Cellular and field potential properties of epileptogenic hippocampal slices. Brain Res 147 (1978) 117-130
43. Singer W., and Gray C.M. Visual feature integration and the temporal correlation hypothesis. Annu Rev Neurosci 18 (1995) 555-586
44. Squire L.R. Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. Psychol Rev 99 (1992) 195-221
45. Stelzer A., Slater N.T., and ten Bruggencate G. Activation of NMDA receptors blocks GABAergic inhibition in an in vitro model of epilepsy. Nature 326 (1987) 698-701
46. Telegdy G., Kokavszky K., and Nyerges A. Action of C-type natriuretic peptide (CNP) on passive avoidance learning in rats: involvement of transmitters. Eur J Neurosci 11 (1999) 3302-3306
47. Tian M., and Yang X.L. C-type natriuretic peptide modulates glutamate receptors on cultured rat retinal amacrine cells. Neuroscience 139 (2006) 1211-1220
48. Toki S., Morishita Y., Sano T., and Matsuda Y. HS-142-1, a novel non-peptide ANP antagonist, blocks the cyclic GMP production elicited by natriuretic peptides in PC12 and NG108-15 cells. Neurosci Lett 135 (1992) 117-120
49. Traub R.D., Whittington M.A., Stanford I.M., and Jefferys J.G. A mechanism for generation of long-range synchronous fast oscillations in the cortex. Nature 383 (1996) 621-624
50. van Welie I., van Hooft J.A., and Wadman W.J. Homeostatic scaling of neuronal excitability by synaptic modulation of somatic hyperpolarization-activated Ih channels. Proc Natl Acad Sci U S A 101 (2004) 5123-5128
51. Vanderwolf C.H. Hippocampal electrical activity and voluntary movement in the rat. Electroencephalogr Clin Neurophysiol 26 (1969) 407-418
52. Wang X.J., and Buzsaki G. Gamma oscillation by synaptic inhibition in a hippocampal interneuronal network model. J Neurosci 16 (1996) 6402-6413
53. Weiss T., Veh R.W., and Heinemann U. Dopamine depresses cholinergic oscillatory network activity in rat hippocampus. Eur J Neurosci 18 (2003) 2573-2580
54. Whittington M.A., Stanford I.M., Colling S.B., Jefferys J.G.R., and Traub R.D. Spatiotemporal patterns of t frequency oscillations tetanically induced in the rat hippocampal slice. J Physiol (Lond) 502 (1997) 591-607
55. Whittington M.A., Traub R.D., and Jefferys J.G.R. Synchronized oscillations in interneuron networks driven by metabotropic glutamate receptor activation. Nature 373 (1995) 612-615
56. Wiedemann K., Jahn H., and Kellner M. Effects of natriuretic peptides upon hypothalamo-pituitary-adrenocortical system activity and anxiety behaviour. Exp Clin Endocrinol Diabetes 108 (2000) 5-13
57. Wojtowicz A.M., van den B.L., Chakrabarty A., Maggio N., Haq R.U., Behrens C.J., and Heinemann U. Monoamines block kainate- and carbachol-induced gamma-oscillations but augment stimulus-induced gamma-oscillations in rat hippocampus in vitro. Hippocampus 19 (2009) 273-288