Muscarinic modulation of M and h currents in gerbil spherical bushy cells


Autoři: Charlène Gillet aff001;  Stefanie Kurth aff002;  Thomas Kuenzel aff001
Působiště autorů: Auditory Neurophysiology Group, Department of Chemosensation, RWTH Aachen University, Worringerweg, Aachen, Germany aff001;  Department of Chemosensation, RWTH Aachen University, Worringerweg, Aachen, Germany aff002
Vyšlo v časopise: PLoS ONE 15(1)
Kategorie: Research Article
doi: 10.1371/journal.pone.0226954

Souhrn

Descending cholinergic fibers innervate the cochlear nucleus. Spherical bushy cells, principal neurons of the anterior part of the ventral cochlear nucleus, are depolarized by cholinergic agonists on two different time scales. A fast and transient response is mediated by alpha-7 homomeric nicotinic receptors while a slow and long-lasting response is mediated by muscarinic receptors. Spherical bushy cells were shown to express M3 receptors, but the receptor subtypes involved in the slow muscarinic response were not physiologically identified yet. Whole-cell patch clamp recordings combined with pharmacology and immunohistochemistry were performed to identify the muscarinic receptor subtypes and the effector currents involved. Spherical bushy cells also expressed both M1 and M2 receptors. The M1 signal was stronger and mainly somatic while the M2 signal was localized in the neuropil and on the soma of bushy cells. Physiologically, the M-current was observed for the gerbil spherical bushy cells and was inhibited by oxotremorine-M application. Surprisingly, long application of carbachol showed only a transient depolarization. Even though no muscarinic depolarization could be detected, the input resistance increased suggesting a decrease in the cell conductance that matched with the closure of M-channels. The hyperpolarization-activated currents were also affected by muscarinic activation and counteracted the effect of the inactivation of M-current on the membrane potential. We hypothesize that this double muscarinic action might allow adaptation of effects during long durations of cholinergic activation.

Klíčová slova:

Action potentials – Analysis of variance – Auditory pathway – Depolarization – Cholinergics – Membrane potential – Carbachol – Hyperpolarization


Zdroje

1. Schofield BR, Motts SD, Mellott JG. Cholinergic cells of the pontomesencephalic tegmentum: connections with auditory structures from cochlear nucleus to cortex. Hear Res. 2011; 279: 85–95. doi: 10.1016/j.heares.2010.12.019 21195150

2. Guinan JJ. Olivocochlear efferents: anatomy, physiology, function, and the measurement of efferent effects in humans. Ear Hear. 2006; 27: 589–607. doi: 10.1097/01.aud.0000240507.83072.e7 17086072

3. Baashar A, Robertson D, Mulders WHAM. A novel method for selectively labelling olivocochlear collaterals in the rat. Hear Res. 2015; 325: 35–41. doi: 10.1016/j.heares.2015.02.011 25814172

4. Baashar A, Robertson D, Yates NJ, Mulders WHAM. Targets of olivocochlear collaterals in cochlear nucleus of rat and guinea pig. J Comp Neurol. 2019; doi: 10.1002/cne.24681

5. Gillet C, Goyer D, Kurth S, Griebel H, Kuenzel T. Cholinergic innervation of principal neurons in the cochlear nucleus of the Mongolian gerbil. J Comp Neurol. 2018; 526: 1647–1661. doi: 10.1002/cne.24433 29574885

6. Horváth M, Kraus KS, Illing RB. Olivocochlear neurons sending axon collaterals into the ventral cochlear nucleus of the rat. J Comp Neurol. 2000; 422: 95–105. 10842220

7. Kishan AU, Lee CC, Winer JA. Patterns of olivocochlear axonal branches. Open J Neurosci. 2011; 1: 2. 22348198

8. Mellott JG, Motts SD, Schofield BR. Multiple origins of cholinergic innervation of the cochlear nucleus. Neuroscience. 2011; 180: 138–147. doi: 10.1016/j.neuroscience.2011.02.010 21320579

9. Fujino K, Oertel D. Cholinergic modulation of stellate cells in the mammalian ventral cochlear nucleus. J Neurosci. 2001; 21: 7372–7383. doi: 10.1523/JNEUROSCI.21-18-07372.2001 11549747

10. Goyer D, Kurth S, Gillet C, Keine C, Rübsamen R, Kuenzel T. Slow Cholinergic Modulation of Spike Probability in Ultra-Fast Time-Coding Sensory Neurons. eNeuro. 2016; doi: 10.1523/ENEURO.0186-16.2016 27699207

11. Brown DA, Adams PR. Muscarinic suppression of a novel voltage-sensitive K+ current in a vertebrate neurone. Nature. 1980; 283: 673–676. doi: 10.1038/283673a0 6965523

12. Adams PR, Brown DA, Constanti A. Pharmacological inhibition of the M-current. J Physiol. 1982; 332: 223–262. doi: 10.1113/jphysiol.1982.sp014411 6760380

13. Dannenberg H, Young K, Hasselmo M. Modulation of Hippocampal Circuits by Muscarinic and Nicotinic Receptors. Front Neural Circuits. 2017; 11: 102. doi: 10.3389/fncir.2017.00102 29321728

14. Brown DA, Passmore GM. Neural KCNQ (Kv7) channels. Br J Pharmacol. 2009; 156: 1185–1195. doi: 10.1111/j.1476-5381.2009.00111.x 19298256

15. Bista P, Pawlowski M, Cerina M, Ehling P, Leist M, Meuth P, et al. Differential phospholipase C-dependent modulation of TASK and TREK two-pore domain K+ channels in rat thalamocortical relay neurons. J Physiol. 2015; 593: 127–144. doi: 10.1113/jphysiol.2014.276527 25556792

16. Leao KE, Leao RN, Sun H, Fyffe REW, Walmsley B. Hyperpolarization-activated currents are differentially expressed in mice brainstem auditory nuclei. J Physiol. 2006; 576: 849–864. doi: 10.1113/jphysiol.2006.114702 16916913

17. Chen C. Hyperpolarization-activated current (Ih) in primary auditory neurons. Hear Res. 1997; 110: 179–190. doi: 10.1016/s0378-5955(97)00078-6 9282900

18. Pape HC. Queer current and pacemaker: the hyperpolarization-activated cation current in neurons. Annu Rev Physiol. 1996; 58: 299–327. doi: 10.1146/annurev.ph.58.030196.001503 8815797

19. Shaikh AG, Finlayson PG. Hyperpolarization-activated (I(h)) conductances affect brainstem auditory neuron excitability. Hear Res. 2003; 183: 126–136. doi: 10.1016/s0378-5955(03)00224-7 13679144

20. Novella Romanelli M, Sartiani L, Masi A, Mannaioni G, Manetti D, Mugelli A, et al. HCN Channels Modulators: The Need for Selectivity. Curr Top Med Chem. 2016; 16: 1764–1791. doi: 10.2174/1568026616999160315130832 26975509

21. Zhao Z, Zhang K, Liu X, Yan H, Ma X, Zhang S, et al. Involvement of HCN Channel in Muscarinic Inhibitory Action on Tonic Firing of Dorsolateral Striatal Cholinergic Interneurons. Front Cell Neurosci. 2016; 10: 71. doi: 10.3389/fncel.2016.00071 27047336

22. Smith DI, Kraus N. Postnatal development of the auditory brainstem response (ABR) in the unanesthetized gerbil. Hear. Res. 1987; 27:157–164. doi: 10.1016/0378-5955(87)90016-5 3610844

23. Schneggenburger R, Meyer AC, Neher E. Released fraction and total size of a pool of immediately available transmitter quanta at a calyx synapse. Neuron 1999; 23:399–409. doi: 10.1016/s0896-6273(00)80789-8 10399944

24. Manis PB, Marx SO. Outward currents in isolated ventral cochlear nucleus neurons. J. Neurosci. 1991; 11:2865–2880. doi: 10.1523/JNEUROSCI.11-09-02865.1991 1880553

25. Clements JD, Bekkers JM. Detection of spontaneous synaptic events with an optimally scaled template. Biophys J. 1997; 73: 220–229. doi: 10.1016/S0006-3495(97)78062-7 9199786

26. Bernheim L, Mathie A, Hille B. Characterization of muscarinic receptor subtypes inhibiting Ca2+ current and M current in rat sympathetic neurons. Proc Natl Acad Sci U S A. 1992; 89: 9544–9548. doi: 10.1073/pnas.89.20.9544 1329101

27. Hamilton SE, Loose MD, Qi M, Levey AI, Hille B, McKnight GS, et al. Disruption of the m1 receptor gene ablates muscarinic receptor-dependent M current regulation and seizure activity in mice. Proc Natl Acad Sci U S A. 1997; 94: 13311–13316. doi: 10.1073/pnas.94.24.13311 9371842

28. Marrion NV, Smart TG, Marsh SJ, Brown DA. Muscarinic suppression of the M-current in the rat sympathetic ganglion is mediated by receptors of the M1-subtype. Br J Pharmacol. 1989; 98: 557–573. doi: 10.1111/j.1476-5381.1989.tb12630.x 2819334

29. Selyanko AA, Hadley JK, Wood IC, Abogadie FC, Jentsch TJ, Brown DA. Inhibition of KCNQ1-4 potassium channels expressed in mammalian cells via M1 muscarinic acetylcholine receptors. J Physiol. 2000; 522: 349–355. doi: 10.1111/j.1469-7793.2000.t01-2-00349.x 10713961

30. Zwart R, Reed H, Clarke S, Sher E. A novel muscarinic receptor-independent mechanism of KCNQ2/3 potassium channel blockade by Oxotremorine-M. Eur J Pharmacol. 2016; 791: 221–228. doi: 10.1016/j.ejphar.2016.08.037 27590358

31. Jones CK, Byun N, Bubser M. Muscarinic and Nicotinic Acetylcholine Receptor Agonists and Allosteric Modulators for the Treatment of Schizophrenia. Neuropsychopharmacology. 2012; 37: 16–42. doi: 10.1038/npp.2011.199 21956443

32. Hadley JK, Passmore GM, Tatulian L, Al-Qatari M, Ye F, Wickenden AD, et al. Stoichiometry of expressed KCNQ2/KCNQ3 potassium channels and subunit composition of native ganglionic M channels deduced from block by tetraethylammonium. J Neurosci. 2003; 23: 5012–5019. doi: 10.1523/JNEUROSCI.23-12-05012.2003 12832524

33. Wang HS, Pan Z, Shi W, Brown BS, Wymore RS, Cohen IS, et al. KCNQ2 and KCNQ3 potassium channel subunits: molecular correlates of the M-channel. Science. 1998; 282: 1890–1893. doi: 10.1126/science.282.5395.1890 9836639

34. Manis PB, Marx SO. Outward currents in isolated ventral cochlear nucleus neurons. J Neurosci. 1991; 11: 2865–2880.

35. Liu L, Zhao R, Bai Y, Stanish LF, Evans JE, Sanderson MJ, et al. M1 Muscarinic Receptors Inhibit L-type Ca2+ Current and M-Current by Divergent Signal Transduction Cascades. J Neurosci. 2006; 26: 11588–11598. doi: 10.1523/JNEUROSCI.2102-06.2006 17093080

36. Rouse ST, Hamilton SE, Potter LT, Nathanson NM, Conn PJ. Muscarinic-induced modulation of potassium conductances is unchanged in mouse hippocampal pyramidal cells that lack functional M1 receptors. Neurosci Lett. 2000; 278: 61–64. doi: 10.1016/s0304-3940(99)00914-3 10643801

37. Sartiani L, Mannaioni G, Masi A, Novella Romanelli M, Cerbai E. The Hyperpolarization-Activated Cyclic Nucleotide-Gated Channels: from Biophysics to Pharmacology of a Unique Family of Ion Channels. Pharmacol Rev. 2017; 69: 354–395. doi: 10.1124/pr.117.014035 28878030

38. Hájos N, Papp EC, Acsády L, Levey AI, Freund TF. Distinct interneuron types express m2 muscarinic receptor immunoreactivity on their dendrites or axon terminals in the hippocampus. Neuroscience. 1998; 82: 355–376. doi: 10.1016/s0306-4522(97)00300-x 9466448

39. Pian P, Bucchi A, Robinson RB, Siegelbaum SA. Regulation of gating and rundown of HCN hyperpolarization-activated channels by exogenous and endogenous PIP2. J Gen Physiol. 2006; 128: 593–604. doi: 10.1085/jgp.200609648 17074978

40. Liao Z, Lockhead D, Larson ED, Proenza C. Phosphorylation and modulation of hyperpolarization-activated HCN4 channels by protein kinase A in the mouse sinoatrial node. J Gen Physiol. 2010; 136: 247–258. doi: 10.1085/jgp.201010488 20713547

41. Williams AD, Jung S, Poolos NP. Protein kinase C bidirectionally modulates Ih and hyperpolarization-activated cyclic nucleotide-gated (HCN) channel surface expression in hippocampal pyramidal neurons. J Physiol. 2015; 593: 2779–2792. doi: 10.1113/JP270453 25820761

42. Trybulski EJ, Zhang J, Kramss RH, Mangano RM. The synthesis and biochemical pharmacology of enantiomerically pure methylated oxotremorine derivatives. J Med Chem. 1993; 36:3533–3541. doi: 10.1021/jm00075a007 8246221

43. Buskila Y, Kékesi O, Bellot-Saez A, Seah W, Berg T, Trpceski M, Yerbury JJ, Ooi L. Dynamic interplay between H-current and M-current controls motoneuron hyperexcitability in amyotrophic lateral sclerosis. Cell Death Dis. 2019; 10: 310. doi: 10.1038/s41419-019-1538-9 30952836

44. Bellingham MC, Lim R, Walmsley B. Developmental changes in EPSC quantal size and quantal content at a central glutamatergic synapse in rat. J. Physiol. 1998; 511: 861–869. doi: 10.1111/j.1469-7793.1998.861bg.x 9714866


Článek vyšel v časopise

PLOS One


2020 Číslo 1