Interactions between intrinsic membrane and emerging network properties determine signal processing in central vestibular neurons

Experimental Brain Research

Volumn 210, Issue 3-4, 2011, Pages 437-449

  Rossert C ^a   Straka, H ^a  

^a UNIVERSITY OF MUNICH   (Germany)

Author keywords

Band pass filter; Impedance; Inhibition; Ion channel; Low pass filter; Membrane properties; Phasic; Potassium adaptation; Resonance; Tonic

Indexed keywords

ION CHANNEL;

CELL DIFFERENTIATION; CELL INTERACTION; CELL MEMBRANE; CELL TYPE; CENTRAL VESTIBULAR NEURON; CONFERENCE PAPER; DEVELOPMENT; FROG; HAPLORHINI; HEAD MOVEMENT; INNER EAR; INTRINSIC MEMBRANE; MEDIAL VESTIBULAR NUCLEUS; MOTION; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; RODENT; SENSORIMOTOR FUNCTION; SIGNAL PROCESSING; VESTIBULAR SYSTEM;

ACTION POTENTIALS; AFFERENT PATHWAYS; ANIMALS; CELL MEMBRANE; EAR, INNER; ELECTRIC STIMULATION; HUMANS; MODELS, NEUROLOGICAL; NEURAL INHIBITION; SENSORY RECEPTOR CELLS; SIGNAL TRANSDUCTION;

EID: 79954887054     PISSN: 00144819     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00221-011-2585-3     Document Type: Conference Paper

References (68)

1. DE Angelaki KE Cullen 2008 Vestibular system: the many facets of a multimodal sense Annu Rev Neurosci 31 125 150 18338968 10.1146/annurev.neuro.31. 060407.125555 1:CAS:528:DC%2BD1cXpt12nsr0%3D
2. AL Babalian PP Vidal 2000 Floccular modulation of vestibuloocular pathways and cerebellum-related plasticity: an in vitro whole brain study J Neurophysiol 84 2514 2528 11067994 1:STN:280:DC%2BD3M%2FmvFOjuw%3D%3D
3. A Babalian N Vibert G Assie M Serafin M Mühlethaler PP Vidal 1997 Central vestibular networks in the guinea-pig: functional characterization in the isolated whole brain in vitro Neuroscience 81 405 426 9300431 10.1016/S0306-4522(97)00069-9 1:CAS:528:DyaK2sXmtVKmtr0%3D (Pubitemid 27381997)
4. MW Bagnall RJ Stevens S du Lac 2007 Transgenic mouse lines subdivide medial vestibular nucleus neurons into discrete, neurochemically distinct populations J Neurosci 27 2318 2330 17329429 10.1523/JNEUROSCI.4322-06.2007 1:CAS:528:DC%2BD2sXjsVymsL4%3D (Pubitemid 46340951)
5. MW Bagnall LE McElvain M Faulstich S du Lac 2008 Frequency-independent synaptic transmission supports a linear vestibular behavior Neuron 60 343 352 18957225 10.1016/j.neuron.2008.10.002 1:CAS:528:DC%2BD1cXhtlCgtrjF
6. R Baker 1998 From genes to behavior in the vestibular system Otolaryngol Head Neck Surg 119 263 275 9743082 10.1016/S0194-5998(98)70061-0 1:STN:280:DyaK1cvhsVSitg%3D%3D (Pubitemid 28425612)
7. J Benda AVM Herz 2003 A universal model for spike-frequency adaptation Neural Comput 15 2523 2564 14577853 10.1162/089976603322385063 (Pubitemid 37211573)
8. M Beraneck M Hachemaoui E Idoux L Ris A Uno E Godaux P Vidal LE Moore N Vibert 2003 Long-term plasticity of ipsilesional medial vestibular nucleus neurons after unilateral labyrinthectomy J Neurophysiol 90 184 203 12649317 10.1152/jn.01140.2002 (Pubitemid 36859171)
9. M Beraneck E Idoux A Uno PP Vidal LE Moore N Vibert 2004 Unilateral labyrinthectomy modifies the membrane properties of contralesional vestibular neurons J Neurophysiol 92 1668 1684 15140902 10.1152/jn.00158.2004 (Pubitemid 39100664)
10. M Beraneck S Pfanzelt I Vassias M Rohregger N Vibert P Vidal LE Moore H Straka 2007 Differential intrinsic response dynamics determine synaptic signal processing in frog vestibular neurons J Neurosci 27 4283 4296 17442812 10.1523/JNEUROSCI.5232-06.2007 1:CAS:528:DC%2BD2sXkvFCjsbk%3D (Pubitemid 46640714)
11. Beraneck M, Lambert FM, Straka H (2008) Membrane properties of central vestibular neurons in larval Xenopus: eco-physiological adaptations to locomotor strategy. Soc Neurosci Abstr 34: 169.12
12. S Biesdorf D Malinvaud I Reichenberger S Pfanzelt H Straka 2008 Differential inhibitory control of semicircular canal nerve afferent-evoked inputs in second-order vestibular neurons by glycinergic and GABAergic circuits J Neurophysiol 99 1758 1769 18256163 10.1152/jn.01207.2007 1:CAS:528: DC%2BD1cXlsFejsrc%3D (Pubitemid 351550071)
13. RHI Blanks W Precht 1976 Functional characterization of primary vestibular afferents in the frog Exp Brain Res 25 369 390 954899 10.1007/BF00241728 1:STN:280:DyaE283lslGgsg%3D%3D
14. DM Broussard 2010 Dynamics of glutamatergic synapses in the medial vestibular nucleus of the mouse Eur J Neurosci 29 502 517 10.1111/j.1460-9568. 2008.06604.x
15. AJ Camp RJ Callister AM Brichta 2006 Inhibitory synaptic transmission differs in mouse type A and B medial vestibular nucleus neurons in vitro J Neurophysiol 95 3208 3218 16407430 10.1152/jn.01001.2005 1:CAS:528: DC%2BD28XkslyisLo%3D
16. RA Clendaniel DM Lasker LB Minor 2002 Differential adaptation of the linear and nonlinear components of the horizontal vestibuloocular reflex in squirrel monkeys J Neurophysiol 88 3534 3540 12466466 10.1152/jn.00404.2002 (Pubitemid 35448727)
17. MB Dutia 2010 Mechanisms of vestibular compensation: recent advances Curr Opin Otolaryngol Head Neck Surg 18 420 424 20693901 10.1097/MOO. 0b013e32833de71f
18. AH Epema NM Gerrits J Voogd 1988 Commissural and intrinsic connections of the vestibular nuclei in the rabbit: a retrograde labeling study Exp Brain Res 71 129 146 2458274 10.1007/BF00247528 1:STN:280:DyaL1czivFaqtA%3D%3D
19. B Ermentrout 1998 Linearization of F-I curves by adaptation Neural Comput 10 1721 1729 9744894 10.1162/089976698300017106 1:STN:280:DyaK1cvis1ektg%3D%3D (Pubitemid 128463680)
20. K Ezure MS Cohen VJ Wilson 1983 Response of cat semicircular canal afferents to sinusoidal polarizing currents: implications for input-output properties of second-order neurons J Neurophysiol 49 639 648 6834091 1:STN:280:DyaL3s7mtlegsA%3D%3D (Pubitemid 13116986)
21. JP Gallagher MR Lewis PS Gallagher 1985 An electrophysiological investigation of the rat medial vestibular nucleus in vitro Prog Clin Biol Res 176 293 304 2987975 1:STN:280:DyaL2M3hs1OhtQ%3D%3D
22. G Gamkrelidze C Giaume KD Peusner 1998 The differential expression of low-threshold sustained potassium current contributes to the distinct firing patterns in embryonic central vestibular neurons J Neurosci 18 1449 1464 9454854 1:CAS:528:DyaK1cXptlyjtg%3D%3D (Pubitemid 28082430)
23. G Gamkrelidze C Giaume KD Peusner 2000 Firing properties and dendrotoxin-sensitive sustained potassium current in vestibular nuclei neurons of the hatchling chick Exp Brain Res 134 398 401 11045364 10.1007/s002210000501 1:CAS:528:DC%2BD3cXnsFylt70%3D
24. AH Gittis S du Lac 2006 Intrinsic and synaptic plasticity in the vestibular system Curr Opin Neurobiol 16 385 390 16842990 10.1016/j.conb.2006. 06.012 1:CAS:528:DC%2BD28Xns1Grsbs%3D (Pubitemid 44142274)
25. AH Gittis S du Lac 2007 Firing properties of GABAergic versus non-GABAergic vestibular nucleus neurons conferred by a differential balance of potassium currents J Neurophysiol 97 3986 3996 17392422 10.1152/jn.00141.2007 1:CAS:528:DC%2BD2sXosF2hsb4%3D (Pubitemid 47080633)
26. AH Gittis SH Moghadam S du Lac 2010 Mechanisms of sustained high firing rates in two classes of vestibular nucleus neurons: differential contributions of resurgent Na, Kv3, and BK currents J Neurophysiol 104 1625 1634 20592126 10.1152/jn.00378.2010 1:CAS:528:DC%2BC3cXht1yhtr%2FP
27. JM Goldberg 2000 Afferent diversity and the organization of central vestibular pathways Exp Brain Res 130 277 297 10706428 10.1007/s002210050033 1:STN:280:DC%2BD3c7mvV2ntw%3D%3D (Pubitemid 30088269)
28. JM Goldberg CE Smith C Fernandez 1984 Relation between discharge regularity and responses to externally applied galvanic currents in vestibular nerve afferents of the squirrel monkey J Neurophysiol 51 1236 1256 6737029 1:STN:280:DyaL2c3ktF2gsg%3D%3D (Pubitemid 14076770)
29. JM Goldberg SM Highstein AK Moschovakis C Fernandez 1987 Inputs from regularly and irregularly discharging vestibular nerve afferents to secondary neurons in the vestibular nuclei of the squirrel monkey. I. An electrophysiological analysis J Neurophysiol 58 700 718 3681391 1:STN:280:DyaL1c%2FmtFGguw%3D%3D (Pubitemid 18015360)
30. A Gottesman-Davis M Shao JC Hirsch KD Peusner 2010 Electrophysiological properties of morphologically-identified medial vestibular nucleus neurons projecting to the abducens nucleus in the chick embryo Neuroscience 172 494 509 20971163 10.1016/j.neuroscience.2010.10.038
31. S Grassi A Frondaroli VE Pettorossi 2002 Different metabotropic glutamate receptors play opposite roles in synaptic plasticity of the rat medial vestibular nuclei J Physiol (Lond) 543 795 806 10.1113/jphysiol.2002.023424 1:CAS:528:DC%2BD38Xns1OhsL4%3D
32. SM Highstein JM Goldberg AK Moschovakis C Fernández 1987 Inputs from regularly and irregularly discharging vestibular nerve afferents to secondary neurons in the vestibular nuclei of the Squirrel monkey: II. Correlation with output pathways of secondary neurons J Neurophysiol 58 714 739
33. AR Johnston NK MacLeod MB Dutia 1994 Ionic conductances contributing to spike repolarization and after-potentials in rat medial vestibular nucleus neurones J Physiol 481 61 77 7531769 1:CAS:528:DyaK2MXisVWmtL4%3D (Pubitemid 24361348)
34. SG Lisberger FA Miles LM Optican 1983 Frequency-selective adaptation: evidence for channels in the vestibulo-ocular reflex? J Neurosci 3 1234 1244 6602209 1:STN:280:DyaL3s3hsFChsQ%3D%3D (Pubitemid 13032652)
35. McElvain LE, Bagnall MW, Sakatos A, du Lac S (2010) Bidirectional plasticity gated by hyperpolarization controls the gain of postsynaptic firing responses at central vestibular nerve synapses. Neuron 68:763-775
36. Menzies JRW, Porrill J, Dutia M, Dean P (2010) Synaptic plasticity in medial vestibular nucleus neurons: comparison with computational requirements of VOR adaptation. PLoS ONE 5(10): e13182. doi: 10.1371/journal.pone.0013182
37. LB Minor JM Goldberg 1991 Vestibular-nerve inputs to the vestibulo-ocular reflex: a functional-ablation study in the squirrel monkey J Neurosci 11 1636 1648 2045879 1:STN:280:DyaK3M3lvFajsA%3D%3D
38. LB Minor DM Lasker DD Backous TE Hullar 1999 Horizontal vestibuloocular reflex evoked by high-acceleration rotations in the squirrel monkey. I. Normal responses J Neurophysiol 82 1254 1270 10482745 1:STN:280:DyaK1MvhsVahsg%3D%3D (Pubitemid 29439693)
39. M Pessia I Servettini R Panichi L Guasti S Grassi A Arcangeli E Wanke VE Pettorossi 2008 ERG voltage-gated K + channels regulate excitability and discharge dynamics of the medial vestibular nucleus neurones J Physiol 586 4877 4890 18718985 10.1113/jphysiol.2008.155762 1:CAS:528:DC%2BD1cXhtlamur7M
40. VE Pettorossi M Dutia A Frondaroli C Dieni S Grassi 2003 Long-term potentiation and depression after unilateral labyrinthectomy in the medial vestibular nucleus of rats Acta Otolaryngol 123 182 186 12701737 10.1080/0036554021000028093 (Pubitemid 36359788)
41. KD Peusner C Giaume 1997 Ontogeny of electrophysiological properties and dendritic pattern in second-order chick vestibular neurons J Comp Neurol 384 621 633 9259493 10.1002/(SICI)1096-9861(19970811)384:4<621::AID-CNE9>3.0. CO;2-4 1:STN:280:DyaK2svgt1Chuw%3D%3D (Pubitemid 27319056)
42. K Peusner G Gamkrelidze C Giaume 1998 Potassium currents and excitability in second-order auditory and vestibular neurons J Neurosci Res 53 511 520 9726422 10.1002/(SICI)1097-4547(19980901)53:5<511::AID-JNR1>3.0.CO;2-C 1:CAS:528:DyaK1cXlsFOmtrs%3D (Pubitemid 28380792)
43. S Pfanzelt C Rössert M Rohregger S Glasauer LE Moore H Straka 2008 Differential dynamic processing of afferent signals in frog tonic and phasic second-order vestibular neurons J Neurosci 28 10349 10362 18842894 10.1523/JNEUROSCI.3368-08.2008 1:CAS:528:DC%2BD1cXht1GksLfN
44. A Popratiloff C Giaume KD Peusner 2003 Developmental change in expression and subcellular localization of two Shaker-related potassium channel proteins (Kv1.1 and Kv1.2) in the chick tangential vestibular nucleus J Comp Neurol 461 466 482 12746863 10.1002/cne.10702 1:CAS:528:DC%2BD3sXltFGlur0%3D (Pubitemid 36637056)
45. R Ramachandran SG Lisberger 2008 Neural substrate of modified and unmodified pathways for learning in monkey vestibuloocular reflex J Neurophysiol 100 1868 1878 18667542 10.1152/jn.90498.2008
46. L Ris M Hachemaoui N Vibert E Godaux PP Vidal LE Moore 2001 Resonance of spike discharge modulation in neurons of the guinea pig medial vestibular nucleus J Neurophysiol 86 703 716 11495944 1:STN:280:DC%2BD3MvltVegsA%3D%3D (Pubitemid 32738561)
47. C Rössert S Pfanzelt H Straka S Glasauer 2009 Modeling of intrinsic and synaptic properties to reveal the cellular and network contribution for vestibular signal processing Ann NY Acad Sci 1164 451 454 19645946 10.1111/j.1749-6632.2009.03766.x
48. C Rössert H Straka S Glasauer LE Moore 2009 Frequency-domain analysis of intrinsic neuronal properties using high-resistant electrodes Front Neurosci 3 64 10.3389/neuro.17.002.2009 20582288
49. Y Saito S Ozawa 2007 Membrane properties of rat medial vestibular nucleus neurons in vivo Neurosci Res 59 215 223 17720270 10.1016/j.neures.2007.06.1479 1:CAS:528:DC%2BD2sXhtVOgsL7E (Pubitemid 47429778)
50. Y Saito T Takazawa S Ozawa 2008 Relationship between afterhyperpolarization profiles and the regularity of spontaneous firings in rat medial vestibular nucleus neurons Eur J Neurosci 28 288 298 18702700 10.1111/j.1460-9568.2008.06338.x
51. C Sekirnjak S du Lac 2006 Physiological and anatomical properties of mouse medial vestibular nucleus neurons projecting to the oculomotor nucleus J Neurophysiol 95 3012 3023 16436481 10.1152/jn.00796.2005
52. C Sekirnjak B Vissel J Bollinger M Faulstich S du Lac 2003 Purkinje cell synapses target physiologically unique brainstem neurons J Neurosci 23 6392 6398 12867525 1:CAS:528:DC%2BD3sXlvVCgsLY%3D (Pubitemid 36875642)
53. M Serafin C de Waele A Khateb PP Vidal M Mühlethaler 1991 Medial vestibular nucleus in the guinea-pig. II. Ionic basis of the intrinsic membrane properties in brainstem slices Exp Brain Res 84 426 433 1648506 10.1007/BF00231465 1:STN:280:DyaK3M3ptlamuw%3D%3D
54. M Serafin C de Waele A Khateb PP Vidal M Mühlethaler 1991 Medial vestibular nucleus in the guinea-pig. I. Intrinsic membrane properties in brainstem slices Exp Brain Res 84 417 425 2065749 10.1007/BF00231464 1:STN:280:DyaK3M3ptlamug%3D%3D
55. M Shao JC Hirsch C Giaume KD Peusner 2004 Spontaneous synaptic activity in chick vestibular nucleus neurons during the perinatal period Neuroscience 127 81 90 15219671 10.1016/j.neuroscience.2004.04.055 1:CAS:528: DC%2BD2cXlt1ags7w%3D (Pubitemid 38829154)
56. M Shao JC Hirsch KD Peusner 2006 Emergence of action potential generation and synaptic transmission in vestibular nucleus neurons J Neurophysiol 96 1215 1226 16775212 10.1152/jn.00180.2006 (Pubitemid 44371516)
57. M Shao A Popratiloff J Yi A Lerner JC Hirsch KD Peusner 2009 Adaptation of chicken vestibular nucleus neurons to unilateral vestibular ganglionectomy Neuroscience 161 988 1007 19375485 10.1016/j.neuroscience.2009.04.027 1:CAS:528:DC%2BD1MXmvF2gsb4%3D
58. MR Smith AB Nelson S du Lac 2002 Regulation of firing response gain by calcium-dependent mechanisms in vestibular nucleus neurons J Neurophysiol 87 2031 2042 11929921 (Pubitemid 34670765)
59. H Straka N Dieringer 1996 Uncrossed disynaptic inhibition of second-order vestibular neurons and its interaction with monosynaptic excitation from vestibular nerve afferent fibers in the frog J Neurophysiol 76 3087 3101 8930257 1:CAS:528:DyaK28XntFWgur0%3D (Pubitemid 26378085)
60. H Straka N Dieringer 2000 Convergence pattern of uncrossed excitatory and inhibitory semicircular canal-specific inputs onto second-order vestibular neurons of frogs Exp Brain Res 135 462 473 11156310 10.1007/s002210000544 1:STN:280:DC%2BD3M7jvVGhsw%3D%3D
61. H Straka N Dieringer 2004 Basic organization principles of the VOR: lessons from frogs Prog Neurobiol 73 259 309 15261395 10.1016/j.pneurobio.2004. 05.003 1:STN:280:DC%2BD2czmtVKrsA%3D%3D (Pubitemid 38903189)
62. H Straka S Holler F Goto 2002 Patterns of canal and otolith afferent input convergence in frog second-order vestibular neurons J Neurophysiol 88 2287 2301 12424270 10.1152/jn.00370.2002 1:STN:280:DC%2BD38nmsVSjsg%3D%3D (Pubitemid 35346034)
63. H Straka M Beraneck M Rohregger LE Moore P Vidal N Vibert 2004 Second-order vestibular neurons form separate populations with different membrane and discharge properties J Neurophysiol 92 845 861 15044516 10.1152/jn.00107.2004 1:STN:280:DC%2BD2czntl2qsg%3D%3D (Pubitemid 38931951)
64. H Straka N Vibert PP Vidal LE Moore MB Dutia 2005 Intrinsic membrane properties of vertebrate vestibular neurons: function, development and plasticity Prog Neurobiol 76 349 392 16263204 10.1016/j.pneurobio.2005.10.002 1:CAS:528:DC%2BD2MXht1arsL7O (Pubitemid 41636777)
65. H Straka FM Lambert S Pfanzelt M Beraneck 2009 Vestibulo-ocular signal transformation in frequency-tuned channels Ann N Y Acad Sci 1164 37 44 19645878 10.1111/j.1749-6632.2008.03740.x
66. T Takazawa Y Saito K Tsuzuki S Ozawa 2004 Membrane and firing properties of glutamatergic and GABAergic neurons in the rat medial vestibular nucleus J Neurophysiol 92 3106 3120 15240763 10.1152/jn.00494.2004 1:CAS:528: DC%2BD2cXpvFahsbw%3D (Pubitemid 40340516)
67. Y Uchino M Sasaki H Sato R Bai E Kawamoto 2008 Otolith and canal integration on single vestibular neurons in cats Exp Brain Res 164 271 285 10.1007/s00221-005-2341-7 (Pubitemid 41124212)
68. A Uno E Idoux M Beraneck P Vidal LE Moore VJ Wilson N Vibert 2003 Static and dynamic membrane properties of lateral vestibular nucleus neurons in guinea pig brain stem slices J Neurophysiol 90 1689 1703 12761276 10.1152/jn.00201.2003 1:CAS:528:DC%2BD3sXotVelu7o%3D (Pubitemid 37129378)