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Abstract:

We previously reported that persistent application of the non-specific cholinergic agonist carbachol (CAR) increased the frequency of calcium channel-mediated oscillatory activity in pedunculopontine nucleus (PPN) neurons, which we identified as dependent on voltage-gated, high-threshold P/Q-type channels. Here, we tested the hypothesis that M2 muscarinic receptors and G-proteins associated with M2 receptors mediate the increase in oscillatory frequency in PPN neurons. We found, using depolarizing ramps, that patch clamped 9-12 day old rat PPN neurons (n = 189) reached their peak oscillatory activity around -20 mV membrane potential. Acute (short duration) application of CAR blocked the oscillatory activity through M2 muscarinic receptors, an effect blocked by atropine. However, persistent (long duration) application of CAR significantly increased the frequency of oscillatory activity in PPN neurons through M2 receptors [40 ± 1 Hz (with CAR) vs. 23 ± 1 Hz (without CAR); p < 0.001]. We then tested the effects of the G-protein antagonist guanosine 5'-[β-thio] diphosphate trilithium salt (GDP-β-S), and the G-protein agonist 5'-[γ-thio] triphosphate trilithium salt (GTP-γ-S). We found, using a three-step protocol in voltage-clamp mode, that the increase in the frequency of oscillations induced by M2 cholinergic receptors was linked to a voltage-dependent G-protein mechanism. In summary, these results suggest that persistent cholinergic input creates a permissive activation state in the PPN that allows high frequency P/Q-type calcium channel-mediated gamma oscillations to occur. © 2013 Kezunovic, Hyde, Goitia, Bisagno, Urbano and Garcia-Rill.

Registro:

Documento: Artículo
Título:Muscarinic modulation of high frequency oscillations in pedunculopontine neurons
Autor:Kezunovic, N.; Hyde, J.; Goitia, B.; Bisagno, V.; Urbano, F.J.; Garcia-Rill, E.
Filiación:Department of Neurobiology and Developmental Sciences, Center for Translational Neuroscience, University of Arkansas for Medical Sciences, Little Rock, AR 72205, United States
IFIBYNE-CONICET-UBA, University of Buenos Aires, Buenos Aires, Argentina
Palabras clave:5'-[β-thio] diphosphate trilithium salt; 5'-[γ-thio] triphosphate trilithium salt; Calcium channels; Carbachol; G-proteins; Gamma oscillations; Muscarinic receptors; acetylcholine; atropine; calcium channel; carbachol; cholinergic receptor; guanine nucleotide binding protein; muscarinic M2 receptor; potassium channel; voltage gated sodium channel; animal cell; animal experiment; article; brain stem; calcium current; cell density; controlled study; dendrite; electroencephalogram; female; high frequency oscillation; male; membrane potential; nerve cell; nerve cell membrane potential; nerve cell membrane steady potential; neuromodulation; nonhuman; patch clamp technique; pedunculopontine tegmental nucleus; protein function; rat; substantia nigra pars compacta; voltage clamp technique
Año:2013
Volumen:4 NOV
DOI: http://dx.doi.org/10.3389/fneur.2013.00176
Título revista:Frontiers in Neurology
Título revista abreviado:Front. Neurol.
ISSN:16642295
CAS:acetylcholine, 51-84-3, 60-31-1, 66-23-9; atropine, 51-55-8, 55-48-1; carbachol, 462-58-8, 51-83-2
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_16642295_v4NOV_n_p_Kezunovic

Referencias:

  • Garcia-Rill, E., Reticular activating system (2009) The Neuroscience of Sleep, pp. 133-139. , Stickgold R, Walker M, editors. Oxford: Elsevier
  • Simon, C., Kezunovic, N., Ye, M., Hyde, J., Hayar, A., Williams, D.K., Gamma band unit and population responses in the pedunculopontine nucleus (2010) J Neurophysiol, 104, pp. 463-474. , doi: 10.1152/jn.00242.2010
  • Kezunovic, N., Urbano, F.J., Simon, C., Hyde, J., Smith, K., Garcia-Rill, E., Mechanism behind gamma band activity in pedunculopontine nucleus (PPN) (2011) Eur J Neurosci, 34, pp. 404-415. , doi:10.1111/j.1460-9568.2011.07766.x
  • Semba, K., Fibiger, H.C., Afferent connections of the laterodorsal and the pedunculopontine tegmental nuclei in the rat: a retro- and antero-grade transport and immunohistochemical study (1992) J Comp Neurol, 323, pp. 387-410. , doi:10.1002/cne.903230307
  • Fernández-Fernández, J.M., Abogadie, F.C., Milligan, G., Delmas, P., Brown, D.A., Multiple pertussis toxin-sensitive G-proteins can couple receptors to GIRK channels in rat sympathetic neurons when expressed heterologously, but only native G(i)-proteins do so in situ (2001) Eur J Neurosci, 14, pp. 283-292. , doi:10.1046/j.0953-816x.2001.01642.x
  • Zhu, J.J., Uhlrich, D.J., Cellular mechanisms underlying two muscarinic receptor-mediated depolarizing responses in relay cells of the rat lateral geniculate nucleus (1998) Neuroscience, 87, pp. 767-781. , doi:10.1016/S0306-4522(98)00209-7
  • Luebke, J.I., McCarley, R.W., Greene, R.W., Inhibitory action of muscarinic agonists on neurons in the rat laterodorsal tegmental nucleus in vitro (1993) J Neurosci, 70, pp. 2128-2135
  • Leonard, C.S., Llinas, R., Serotonergic and cholinergic inhibition of mesopontine cholinergic neurons controlling REM sleep: an in vitro electrophysiological study (1994) Neuroscience, 59, pp. 309-330. , doi:10.1016/0306-4522(94)90599-1
  • Vilaro, M.T., Wiederhold, K.H., Palacios, J.M., Mengod, G., Muscarinic M2 receptor mRNA expression and receptor binding in cholinergic and non-cholinergic cells in the rat brain: a correlative study using in situ hybridization histochemistry and receptor autobiography (1992) Neuroscience, 47, pp. 367-393. , doi:10.1016/0306-4522(92)90253-X
  • Vilaro, M.T., Palacios, J.M., Mengod, G., Multiplicity of muscarinic autoreceptor subtypes? Comparison of the distribution of cholinergic cells and cells containing mRNA for five subtypes of muscarinic receptors in the rat brain (1994) Brain Res Mol Brain Res, 21, pp. 30-46. , doi:10.1016/0169-328X(94)90375-1
  • Ye, M., Hayar, A., Strotman, B., Garcia-Rill, E., Cholinergic modulation of fast inhibitory and excitatory transmission to pedunculopontine thalamic projecting neurons (2010) J Neurophysiol, 103, pp. 2417-2432. , doi:10.1152/jn.01143.2009
  • Bean, B.P., Neurotransmitter inhibition of neuronal calcium currents by changes in channel voltage dependence (1989) Nature, 340, pp. 153-156. , doi:10.1038/340153a0
  • Kuo, C.C., Bean, B.P., G-protein modulation of ion permeation through N-type calcium channels (1993) Nature, 365, pp. 258-262. , doi:10.1038/365258a0
  • Ikeda, S.R., Voltage-dependent modulation of N-type calcium channels by G-protein beta gamma subunits (1996) Nature, 380, pp. 255-258. , doi:10.1038/380255a0
  • Herlitze, S., Garcia, D.E., Mackie, K., Hille, B., Scheuer, T., Catterall, W.A., Modulation of Ca2+ channels by G-protein beta gamma subunits (1996) Nature, 380, pp. 258-262. , doi:10.1038/380258a0
  • Kammermeier, P.J., Ruiz-Velasco, V., Ikeda, S.R., A voltage-independent calcium current inhibitory pathway activated by muscarinic agonists in rat sympathetic neurons requires both Ga q/11 and Gß? (2000) J Neurosci, 20, pp. 5623-5629
  • Hille, B., Modulation of ion-channel function by G-protein-coupled receptors (1994) Trends Neurosci, 17, pp. 531-536. , doi:10.1016/0166-2236(94)90157-0
  • Jouvet-Mounier, D., Astic, L., Lacote, D., Ontogenesis of the states of sleep in rat, cat, and guinea pig during the first postnatal month (1970) Dev Psychobiol, 2, pp. 216-239. , doi:10.1002/dev.420020407
  • Garcia-Rill, E., Charlesworth, A., Heister, D., Ye, M., Hayar, A., The developmental decrease in REM sleep: the role of transmitters and electrical coupling (2008) Sleep, 31, pp. 673-690
  • Wang, H.L., Morales, M., Pedunculopontine and laterodorsal tegmental nuclei contain distinct populations of cholinergic, glutamatergic and GABAergic neurons in the rat (2009) Eur J Neurosci, 29, pp. 340-358. , doi:10.1111/j.1460-9568.2008.06576.x
  • Hyde, J., Kezunovic, N., Urbano, F.J., Garcia-Rill, E., Spatiotemporal properties of high speed calcium oscillations in the pedunculopontine nucleus (2013) J Appl Physiol, , [Epub ahead of print]. doi:10.1152/japplphysiol.00762.2013
  • Pare, D., Smith, Y., Parent, A., Steriade, M., Projections of brainstem core cholinergic and non-cholinergic neurons of cat to intralaminar and reticular thalamic nuclei (1988) Neuroscience, 25, pp. 47-67. , doi:10.1016/0306-4522(88)90007-3
  • Smith, Y., Pare, D., Deschenes, M., Parent, A., Steriade, M., Cholinergic and non-cholinergic projections from the upper brainstem core to the visual thalamus in the cat (1988) Exp Brain Res, 70, pp. 166-180
  • Steriade, M., Pare, D., Parent, A., Smith, Y., Projections of cholinergic and non-cholinergic neurons of the brainstem core to relay and associational thalamic nuclei in the cat and macaque monkey (1988) Neuroscience, 25, pp. 47-67. , doi:10.1016/0306-4522(88)90006-1
  • Dringenberg, H.C., Vanderwolf, C.H., Involvement of direct and indirect pathways in electrocorticographic activation (1998) Neurosci Biobehav Rev, 22, pp. 243-257. , doi:10.1016/S0149-7634(97)00012-2
  • Good, C.H., Bay, K.D., Buchanan, R., Skinner, R.D., Garcia-Rill, E., Muscarinic and nicotinic responses in the developing pedunculopontine nucleus (PPN) (2007) Brain Res, 1129, pp. 147-155. , doi:10.1016/j.brainres.2006.10.046
  • Ye, M., Hayar, A., Gracia-Rill, E., Cholinergic responses and intrinsic membrane properties of developing thalamic parafascicular neurons (2009) J Neurophysiol, 2, pp. 774-785. , doi:10.1152/jn.91132.2008
  • Kezunovic, N., Hyde, J., Simon, C., Urbano, F.J., Williams, K., Garcia-Rill, E., Gamma band activity in the developing parafascicular nucleus (Pf) (2012) J Neurophysiol, 107, pp. 772-784. , doi:10.1152/jn.00677.2011
  • Beech, D.J., Bernheim, L., Hille, B., Pertussis toxin and voltage dependence distinguish multiple pathways modulating calcium channels of rat sympathetic neurons (1992) Neuron, 8, pp. 97-106. , doi:10.1016/0896-6273(92)90111-P
  • Mathie, A., Bernheim, L., Hille, B., Inhibition of N- and L-type calcium channels by muscarinic receptor activation in rat sympathetic neurons (1992) Neuron, 8, pp. 907-914. , doi:10.1016/0896-6273(92)90205-R
  • Mintz, I.M., Bean, B.P., GABAB receptor inhibition of P-type Ca2+ channels in central neurons (1993) Neuron, 10, pp. 889-898. , doi:10.1016/0896-6273(93)90204-5
  • Iegorova, O., Fisyunov, A., Krishtal, O., G-protein-independent modulation of P-type calcium channels by mu-opioids in Purkinje neurons of rat (2010) Neurosci Lett, 480, pp. 106-111. , doi:10.1016/j.neulet.2010.06.015
  • Datta, S., Siwek, D.F., Single cell activity patterns of pedunculopontine tegmentum neurons across the sleep-wake cycle in the freely moving rats (2002) J Neurosci Res, 70, pp. 79-82. , doi:10.1002/jnr.10405
  • Deurveilher, S., Hennevin, E., Lesions of the pedunculopontine tegmental nucleus reduce paradoxical sleep (PS) propensity: evidence from a short-term PS deprivation study in rats (2001) Eur J Neurosci, 10, pp. 1963-1976. , doi:10.1046/j.0953-816x.2001.01562.x
  • Gray, C.M., Singer, W., Stimulus-specific neuronal oscillations in orientation columns of cat visual cortex (1989) Proc Nat Acad Sci U S A, 86, pp. 1698-1702. , doi:10.1073/pnas.86.5.1698
  • Gray, C.M., Konig, P., Engel, A.K., Singer, W., Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties (1989) Nature, 338, pp. 334-337. , doi:10.1038/338334a0
  • Llinás, R., Paré, D., Of dreaming and wakefulness (1991) Neuroscience, 44, pp. 521-535. , doi:10.1016/0306-4522(91)90075-Y
  • Llinas, R., Ribary, U., Coherent 40-Hz oscillation characterizes dream state in humans (1993) Proc Natl Acad Sci U S A, 90, pp. 2078-2081. , doi:10.1073/pnas.90.5.2078
  • Singer, W., Consciousness and the structure of neuronal representations (1998) Philos Trans R Soc Lond B Biol Sci, 353, pp. 1829-1840. , doi:10.1098/rstb.1998.0335
  • Llinas, R., Grace, A., Yarom, Y., In vitro neurons in mammalian cortical layer 4 exhibit intrinsic oscillatory activity in the 10- to 50-Hz frequency range (1991) Proc Nat Acad Sci U S A, 88, pp. 897-901. , doi:10.1073/pnas.88.8.3510-c
  • Singer, W., Synchronization of cortical activity and its putative role in information processing and learning (1993) Annu Rev Physiol, 55, pp. 349-374. , doi:10.1146/annurev.ph.55.030193.002025
  • Whittington, M.A., Stanford, I.M., Colling, S.B., Jeffreys, J.G.R., Traub, R.D., Spatiotemporal patterns of gamma frequency oscillations tetanically induced in the rat hippocampal slice (1997) J Physiol, 502, pp. 591-607. , doi:10.1111/j.1469-7793.1997.591bj.x
  • Middleton, S.J., Racca, C., Cunningham, M.O., Traub, R.D., Monyer, H., Knopfel, T., High-frequency network oscillations in cerebellar cortex (2008) Neuron, 58, pp. 763-774. , doi:10.1016/j.neuron.2008.03.030
  • Nakamura, T.Y., Jeromin, A., Mikoshiba, K., Wakabayashi, S., Neuronal calcium sensor-1 promotes immature heart function and hypertrophy by enhancing Ca2+ signals (2011) Circ Res, 109, pp. 512-523. , doi:10.1161/CIRCRESAHA.111.248864
  • Ng, A., Krogh, M., Toresson, H., Dendritic EGFP-STIM1 activation after type I metabotropic glutamate and muscarinic acetylcholine receptor stimulation in hippocampal neuron (2011) J Neurosci Res, 89, pp. 1235-1244. , doi:10.1002/jnr.22648
  • Barry, R.J., Clarke, A.R., Hajos, M., McCarthy, R., Selikowitz, M., Dupuy, F.E., Resting-state EEG gamma activity in children with attention-deficit/hyperactivity disorder (2010) Clin Neurophysiol, 121, pp. 1871-1877. , doi:10.1016/j.clinph.2010.04.022
  • Ozerdem, A., Guntenkin, B., Atagun, I., Turp, B., Basar, E., Reduced long distance gamma (28-48 Hz) coherence in euthymic patients with bipolar disorder (2011) J Affect Disord, 132, pp. 325-332. , doi:10.1016/j.jad.2011.02.028
  • Uhlhaas, P.J., Singer, W., Abnormal neural oscillations and synchrony in schizophrenia (2010) Nat Rev Neurosci, 11, pp. 100-113. , doi:10.1038/nrn2774
  • Spencer, K.M., Nestor, P.G., Niznikiewicz, M.A., Salisbury, D.F., Shenton, M.E., McCarley, R.W., Abnormal neural synchrony in schizophrenia (2003) J Neurosci, 23, pp. 7407-7411

Citas:

---------- APA ----------
Kezunovic, N., Hyde, J., Goitia, B., Bisagno, V., Urbano, F.J. & Garcia-Rill, E. (2013) . Muscarinic modulation of high frequency oscillations in pedunculopontine neurons. Frontiers in Neurology, 4 NOV.
http://dx.doi.org/10.3389/fneur.2013.00176
---------- CHICAGO ----------
Kezunovic, N., Hyde, J., Goitia, B., Bisagno, V., Urbano, F.J., Garcia-Rill, E. "Muscarinic modulation of high frequency oscillations in pedunculopontine neurons" . Frontiers in Neurology 4 NOV (2013).
http://dx.doi.org/10.3389/fneur.2013.00176
---------- MLA ----------
Kezunovic, N., Hyde, J., Goitia, B., Bisagno, V., Urbano, F.J., Garcia-Rill, E. "Muscarinic modulation of high frequency oscillations in pedunculopontine neurons" . Frontiers in Neurology, vol. 4 NOV, 2013.
http://dx.doi.org/10.3389/fneur.2013.00176
---------- VANCOUVER ----------
Kezunovic, N., Hyde, J., Goitia, B., Bisagno, V., Urbano, F.J., Garcia-Rill, E. Muscarinic modulation of high frequency oscillations in pedunculopontine neurons. Front. Neurol. 2013;4 NOV.
http://dx.doi.org/10.3389/fneur.2013.00176