Muscarinic modulation of high frequency oscillations in pedunculopontine neurons

Frontiers in Neurology

Volumn 4 NOV, Issue , 2013, Pages

  Kezunovic, Nebojsa ^a   Hyde, James ^a   Goitia, Belen ^b   Bisagno, Veronica ^b   Urbano, Francisco J ^b   Garcia Rill, Edgar ^a  

^a UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

^b INSTITUTO DE FISIOLOGÍA   (Argentina)

Author keywords

5' thio diphosphate trilithium salt; 5' thio triphosphate trilithium salt; Calcium channels; Carbachol; G proteins; Gamma oscillations; Muscarinic receptors

Indexed keywords

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;

EID: 84889661344     PISSN: None     EISSN: 16642295     Source Type: Journal    
DOI: 10.3389/fneur.2013.00176     Document Type: Article

References (49)

1. Garcia-Rill E. Reticular activating system. In: Stickgold R, Walker M, editors. The Neuroscience of Sleep. Oxford: Elsevier (2009). p. 133-9.
2. Simon C, Kezunovic N, Ye M, Hyde J, Hayar A, Williams DK, et al. Gamma band unit and population responses in the pedunculopontine nucleus. J Neurophysiol (2010) 104:463-74. doi: 10.1152/jn.00242.2010
3. Kezunovic N, Urbano FJ, Simon C, Hyde J, Smith K, Garcia-Rill E. Mechanism behind gamma band activity in pedunculopontine nucleus (PPN). Eur J Neurosci (2011) 34:404-15. doi:10.1111/j.1460-9568.2011.07766.x
4. Semba K, Fibiger HC. Afferent connections of the laterodorsal and the pedunculopontine tegmental nuclei in the rat: a retro- and antero-grade transport and immunohistochemical study. J Comp Neurol (1992) 323:387-410. doi:10.1002/cne.903230307
5. Fernández-Fernández JM, Abogadie FC, Milligan G, Delmas P, Brown DA. 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. Eur J Neurosci (2001) 14:283-92. doi:10.1046/j.0953-816x.2001.01642.x
6. Zhu JJ, Uhlrich DJ. Cellular mechanisms underlying two muscarinic receptor-mediated depolarizing responses in relay cells of the rat lateral geniculate nucleus. Neuroscience (1998) 87:767-81. doi:10.1016/S0306-4522(98)00209-7
7. Luebke JI, McCarley RW, Greene RW. Inhibitory action of muscarinic agonists on neurons in the rat laterodorsal tegmental nucleus in vitro. J Neurosci (1993) 70:2128-35.
8. Leonard CS, Llinas R. Serotonergic and cholinergic inhibition of mesopontine cholinergic neurons controlling REM sleep: an in vitro electrophysiological study. Neuroscience (1994) 59:309-30. doi:10.1016/0306-4522(94)90599-1
9. Vilaro MT, Wiederhold KH, Palacios JM, 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. Neuroscience (1992) 47:367-93. doi:10.1016/0306-4522(92)90253-X
10. Vilaro MT, Palacios JM, 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. Brain Res Mol Brain Res (1994) 21:30-46. doi:10.1016/0169-328X(94)90375-1
11. Ye M, Hayar A, Strotman B, Garcia-Rill E. Cholinergic modulation of fast inhibitory and excitatory transmission to pedunculopontine thalamic projecting neurons. J Neurophysiol (2010) 103:2417-32. doi:10.1152/jn.01143.2009
12. Bean BP. Neurotransmitter inhibition of neuronal calcium currents by changes in channel voltage dependence. Nature (1989) 340:153-6. doi:10.1038/340153a0
13. Kuo CC, Bean BP. G-protein modulation of ion permeation through N-type calcium channels. Nature (1993) 365:258-62. doi:10.1038/365258a0
14. Ikeda SR. Voltage-dependent modulation of N-type calcium channels by G-protein beta gamma subunits. Nature (1996) 380:255-8. doi:10.1038/380255a0
15. Herlitze S, Garcia DE, Mackie K, Hille B, Scheuer T, Catterall WA. Modulation of Ca2+ channels by G-protein beta gamma subunits. Nature (1996) 380:258-62. doi:10.1038/380258a0
16. Kammermeier PJ, Ruiz-Velasco V, Ikeda SR. A voltage-independent calcium current inhibitory pathway activated by muscarinic agonists in rat sympathetic neurons requires both Ga q/11 and Gß?. J Neurosci (2000) 20:5623-9.
17. Hille B. Modulation of ion-channel function by G-protein-coupled receptors. Trends Neurosci (1994) 17:531-6. doi:10.1016/0166-2236(94)90157-0
18. Jouvet-Mounier D, Astic L, Lacote D. Ontogenesis of the states of sleep in rat, cat, and guinea pig during the first postnatal month. Dev Psychobiol (1970) 2:216-39. doi:10.1002/dev.420020407
19. Garcia-Rill E, Charlesworth A, Heister D, Ye M, Hayar A. The developmental decrease in REM sleep: the role of transmitters and electrical coupling. Sleep (2008) 31:673-90.
20. Wang HL, Morales M. Pedunculopontine and laterodorsal tegmental nuclei contain distinct populations of cholinergic, glutamatergic and GABAergic neurons in the rat. Eur J Neurosci (2009) 29:340-58. doi:10.1111/j.1460-9568.2008.06576.x
21. Hyde J, Kezunovic N, Urbano FJ, Garcia-Rill E. Spatiotemporal properties of high speed calcium oscillations in the pedunculopontine nucleus. J Appl Physiol (2013). [Epub ahead of print]. doi:10.1152/japplphysiol.00762.2013
22. 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. Neuroscience (1988) 25:47-67. doi:10.1016/0306-4522(88)90007-3
23. 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. Exp Brain Res (1988) 70:166-80.
24. 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. Neuroscience (1988) 25:47-67. doi:10.1016/0306-4522(88)90006-1
25. Dringenberg HC, Vanderwolf CH. Involvement of direct and indirect pathways in electrocorticographic activation. Neurosci Biobehav Rev (1998) 22:243-57. doi:10.1016/S0149-7634(97)00012-2
26. Good CH, Bay KD, Buchanan R, Skinner RD, Garcia-Rill E. Muscarinic and nicotinic responses in the developing pedunculopontine nucleus (PPN). Brain Res (2007) 1129:147-55. doi:10.1016/j.brainres.2006.10.046
27. Ye M, Hayar A, Gracia-Rill E. Cholinergic responses and intrinsic membrane properties of developing thalamic parafascicular neurons. J Neurophysiol (2009) 2:774-85. doi:10.1152/jn.91132.2008
28. Kezunovic N, Hyde J, Simon C, Urbano FJ, Williams K, Garcia-Rill E. Gamma band activity in the developing parafascicular nucleus (Pf). J Neurophysiol (2012) 107:772-84. doi:10.1152/jn.00677.2011
29. Beech DJ, Bernheim L, Hille B. Pertussis toxin and voltage dependence distinguish multiple pathways modulating calcium channels of rat sympathetic neurons. Neuron (1992) 8:97-106. doi:10.1016/0896-6273(92)90111-P
30. Mathie A, Bernheim L, Hille B. Inhibition of N- and L-type calcium channels by muscarinic receptor activation in rat sympathetic neurons. Neuron (1992) 8:907-14. doi:10.1016/0896-6273(92)90205-R
31. Mintz IM, Bean BP. GABAB receptor inhibition of P-type Ca2+ channels in central neurons. Neuron (1993) 10:889-98. doi:10.1016/0896-6273(93)90204-5
32. Iegorova O, Fisyunov A, Krishtal O. G-protein-independent modulation of P-type calcium channels by mu-opioids in Purkinje neurons of rat. Neurosci Lett (2010) 480:106-11. doi:10.1016/j.neulet.2010.06.015
33. Datta S, Siwek DF. Single cell activity patterns of pedunculopontine tegmentum neurons across the sleep-wake cycle in the freely moving rats. J Neurosci Res (2002) 70:79-82. doi:10.1002/jnr.10405
34. 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. Eur J Neurosci (2001) 10:1963-76. doi:10.1046/j.0953-816x.2001.01562.x
35. Gray CM, Singer W. Stimulus-specific neuronal oscillations in orientation columns of cat visual cortex. Proc Nat Acad Sci U S A (1989) 86:1698-702. doi:10.1073/pnas.86.5.1698
36. Gray CM, Konig P, Engel AK, Singer W. Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties. Nature (1989) 338:334-7. doi:10.1038/338334a0
37. Llinás R, Paré D. Of dreaming and wakefulness. Neuroscience (1991) 44:521-35. doi:10.1016/0306-4522(91)90075-Y
38. Llinas R, Ribary U. Coherent 40-Hz oscillation characterizes dream state in humans. Proc Natl Acad Sci U S A (1993) 90:2078-81. doi:10.1073/pnas.90.5.2078
39. Singer W. Consciousness and the structure of neuronal representations. Philos Trans R Soc Lond B Biol Sci (1998) 353:1829-40. doi:10.1098/rstb.1998.0335
40. 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. Proc Nat Acad Sci U S A (1991) 88:897-901. doi:10.1073/pnas.88.8.3510-c
41. Singer W. Synchronization of cortical activity and its putative role in information processing and learning. Annu Rev Physiol (1993) 55:349-74. doi:10.1146/annurev.ph.55.030193.002025
42. Whittington MA, Stanford IM, Colling SB, Jeffreys JGR, Traub RD. Spatiotemporal patterns of gamma frequency oscillations tetanically induced in the rat hippocampal slice. J Physiol (1997) 502:591-607. doi:10.1111/j.1469-7793.1997.591bj.x
43. Middleton SJ, Racca C, Cunningham MO, Traub RD, Monyer H, Knopfel T, et al. High-frequency network oscillations in cerebellar cortex. Neuron (2008) 58:763-74. doi:10.1016/j.neuron.2008.03.030
44. Nakamura TY, Jeromin A, Mikoshiba K, Wakabayashi S. Neuronal calcium sensor-1 promotes immature heart function and hypertrophy by enhancing Ca2+ signals. Circ Res (2011) 109:512-23. doi:10.1161/CIRCRESAHA.111.248864
45. Ng A, Krogh M, Toresson H. Dendritic EGFP-STIM1 activation after type I metabotropic glutamate and muscarinic acetylcholine receptor stimulation in hippocampal neuron. J Neurosci Res (2011) 89:1235-44. doi:10.1002/jnr.22648
46. Barry RJ, Clarke AR, Hajos M, McCarthy R, Selikowitz M, Dupuy FE. Resting-state EEG gamma activity in children with attention-deficit/hyperactivity disorder. Clin Neurophysiol (2010) 121:1871-7. doi:10.1016/j.clinph.2010.04.022
47. Ozerdem A, Guntenkin B, Atagun I, Turp B, Basar E. Reduced long distance gamma (28-48 Hz) coherence in euthymic patients with bipolar disorder. J Affect Disord (2011) 132:325-32. doi:10.1016/j.jad.2011.02.028
48. Uhlhaas PJ, Singer W. Abnormal neural oscillations and synchrony in schizophrenia. Nat Rev Neurosci (2010) 11:100-13. doi:10.1038/nrn2774
49. Spencer KM, Nestor PG, Niznikiewicz MA, Salisbury DF, Shenton ME, McCarley RW. Abnormal neural synchrony in schizophrenia. J Neurosci (2003) 23:7407-11.