Relationship between afterhyperpolarization profiles and the regularity of spontaneous firings in rat medial vestibular nucleus neurons
Abstract
Our previous in vivo and in vitro whole‐cell patch‐clamp recording studies demonstrated that neurons in the medial vestibular nucleus (MVN) could be characterized on the basis of three electrophysiological properties: afterhyperpolarization (AHP) profile; firing pattern; and response pattern to hyperpolarizing current pulses. In the present study, to clarify which types of the classified MVN neurons correspond to neurons with regular or irregular firing, we investigated their spike discharge patterns using whole‐cell patch‐clamp recording in both in vivo and in vitro preparations. The discharge regularity was related to AHP profiles, and we found that: (i) the coefficient of variation (CV) of interspike intervals during spike discharges was smaller in neurons exhibiting AHP with a slow component [AHP(s+)] than in those without a slow component [AHP(s−)], or with a slow AHP component preceded by afterdepolarization (ADP) [AHP(s+) with ADP]; (ii) the blockade of Ca 2+‐dependent K+ channels by 100 n m apamin abolished the slow component and increased the CV in neurons exhibiting AHP(s+); and (iii) the modulation of firing (firing gain) in response to ramp current was larger in neurons exhibiting AHP(s−) than in the other two neuronal types. These results suggest that neurons exhibiting AHP(s+) are regularly discharging neurons with small firing gains to stimulus, neurons exhibiting AHP(s+) with ADP are irregularly discharging neurons with small firing gains, and neurons exhibiting AHP(s−) are irregularly discharging neurons with large firing gains. The regular firing of neurons exhibiting AHP(s+) is attributed to the activation of apamin‐sensitive Ca 2+‐dependent K+ channels.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
One principal feedback mechanism in the control of the frequency and patterning of neuronal firing is afterhyperpolarization (AHP).
“One principal feedback mechanism in the control of the frequency and patterning of neuronal firing is afterhyperpolarization, or AHP [74–76].”
From Chronic unpredictable stress induces depression-related behaviors by suppressing AgRP neuron activity (2021) · cites this paper as [75]
Cites
Pan, L., Gurevich, E. V., & Gurevich, V. V. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m209532200 · Cited by 1,758 · see citing works
[6] Correction for liquid junction potentials in patch clamp experiments
Neher, E. (1992) · Methods in Enzymology · doi:10.1016/0076-6879(92)07008-c · Cited by 1,132 · see citing works
Small-Conductance, Calcium-Activated Potassium Channels from Mammalian Brain
Kohler, M.-L., Hirschberg, B., Bond, C. T., Kinzie, J. M., Marrion, N. V., Maylie, J., & Adelman, J. P. (1996) · Science · doi:10.1126/science.273.5282.1709 · Cited by 946 · see citing works
Ca2+-activated K+ currents in neurones: types, physiological roles and modulation
Sah, P. (1996) · Trends in Neurosciences · doi:10.1016/s0166-2236(96)80026-9 · Cited by 892 · see citing works
Goldberg, J. M., Smith, C. E., & Fernandez, C. (1984) · Journal of Neurophysiology · doi:10.1152/jn.1984.51.6.1236 · Cited by 661 · see citing works
TONIC AND KINETIC RESPONSES OF CAT'S VESTIBULAR NEURONS TO HORIZONTAL ANGULAR ACCELERATION
Shimazu, H., & Precht, W. (1965) · Journal of Neurophysiology · doi:10.1152/jn.1965.28.6.991 · Cited by 610 · see citing works
Fernandez, C., & Goldberg, J. M. (1976) · Journal of Neurophysiology · doi:10.1152/jn.1976.39.5.996 · Cited by 606 · see citing works
Physiology of Peripheral Neurons Innervating Semicircular Canals of the Squirrel Monkey
Goldberg, J. M., & Fernandez, C. (1971) · Journal of Neurophysiology · doi:10.1152/jn.1971.34.4.676 · Cited by 542 · see citing works
Margrie, T. W., Brecht, M., & Sakmann, B. J. (2002) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-002-0831-z · Cited by 525 · see citing works
Duensing, F., & Schaefer, K. ‐. (1958) · European Archives of Psychiatry and Clinical Neuroscience · doi:10.1007/bf00941383 · Cited by 437 · see citing works
Fuchs, A. F., & Kimm, J. (1975) · Journal of Neurophysiology · doi:10.1152/jn.1975.38.5.1140 · Cited by 426 · see citing works
Afferent diversity and the organization of central vestibular pathways
Goldberg, J. M. (2000) · Experimental Brain Research · doi:10.1007/s002210050033 · Cited by 415 · see citing works
Maggi, C. A., & Meli, A. (1986) · Cellular and Molecular Life Sciences · doi:10.1007/bf01952426 · Cited by 409 · see citing works
Signals in vestibular nucleus mediating vertical eye movements in the monkey
Tomlinson, R. D., & Robinson, D. A. (1984) · Journal of Neurophysiology · doi:10.1152/jn.1984.51.6.1121 · Cited by 308 · see citing works
Medial vestibular nucleus in the guinea-pig
Serafin, M., de Waele, C., Khateb, A., Vidal, P. P., & Mühlethaler, M. (1991) · Experimental Brain Research · doi:10.1007/bf00231464 · Cited by 287 · see citing works
Medial vestibular nucleus in the guinea-pig
Serafin, M., de Waele, C., Khateb, A., Vidal, P. P., & Mühlethaler, M. (1991) · Experimental Brain Research · doi:10.1007/bf00231465 · Cited by 279 · see citing works
Neuron activity in monkey vestibular nuclei during vertical vestibular stimulation and eye movements
Chubb, M. C., Fuchs, A. F., & Scudder, C. A. (1984) · Journal of Neurophysiology · doi:10.1152/jn.1984.52.4.724 · Cited by 272 · see citing works
Keller, E. L., & Daniels, P. D. (1975) · Experimental Neurology · doi:10.1016/0014-4886(75)90041-2 · Cited by 247 · see citing works
Long-Lasting Increases in Intrinsic Excitability Triggered by Inhibition
Nelson, A., Krispel, C. M., Sekirnjak, C., & du Lac, S. (2003) · Neuron · doi:10.1016/s0896-6273(03)00641-x · Cited by 239 · see citing works
Miles, F. A. (1974) · Brain Research · doi:10.1016/0006-8993(74)90963-9 · Cited by 237 · see citing works
Intrinsic membrane properties of vertebrate vestibular neurons: Function, development and plasticity
Straka, H., Vibert, N., Vidal, P. P., Moore, L. E., & Dutia, M. B. (2005) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2005.10.002 · Cited by 228 · see citing works
Yagi, T., Simpson, N. E., & Markham, C. H. (1977) · Experimental Brain Research · doi:10.1007/bf00237647 · Cited by 198 · see citing works
Iwamoto, Y., Kitama, T., & YOSHIDA, K. T. (1990) · Journal of Neurophysiology · doi:10.1152/jn.1990.63.4.902 · Cited by 189 · see citing works
Response dynamics of horizontal canal afferents in barbiturate-anesthetized cats
Tomko, D. L., Peterka, R. J., Schor, R. H., & O’Leary, D. P. (1981) · Journal of Neurophysiology · doi:10.1152/jn.1981.45.3.376 · Cited by 184 · see citing works
Frequency-selective adaptation: evidence for channels in the vestibulo- ocular reflex?
Lisberger, S. G., Miles, F. A., & Lm, O. (1983) · Journal of Neuroscience · doi:10.1523/jneurosci.03-06-01234.1983 · Cited by 164 · see citing works
Regulation of Firing Response Gain by Calcium-Dependent Mechanisms in Vestibular Nucleus Neurons
Smith, M. R., Nelson, A., & du Lac, S. (2002) · Journal of Neurophysiology · doi:10.1152/jn.00821.2001 · Cited by 147 · see citing works
Johnston, A. R., MacLeod, N. K., & Dutia, M. B. (1994) · The Journal of Physiology · doi:10.1113/jphysiol.1994.sp020419 · Cited by 132 · see citing works
Vestibular integrators in the oculomotor system
Fukushima, K., & Kaneko, C. R. S. (1995) · Neuroscience Research · doi:10.1016/0168-0102(95)00904-8 · Cited by 120 · see citing works
Beraneck, M., Hachemaoui, M., Idoux, E., Ris, L., Uno, A., Godaux, E., Vidal, P., Moore, L. E., & Vibert, N. (2003) · Journal of Neurophysiology · doi:10.1152/jn.01140.2002 · Cited by 119 · see citing works
A stochastic afterhyperpolarization model of repetitive activity in vestibular afferents
Smith, C. E., & Goldberg, J. M. (1986) · Biological Cybernetics · doi:10.1007/bf00337114 · Cited by 117 · see citing works
Lisberger, S., & Miles, F. (1980) · Journal of Neurophysiology · doi:10.1152/jn.1980.43.6.1725 · Cited by 113 · see citing works
Bagnall, M. W., Stevens, R. J. N., & du Lac, S. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.4322-06.2007 · Cited by 101 · see citing works
The repetitive impulse discharge of a simple neurone model compared to that of spinal motoneurones
Kernell, D. (1968) · Brain Research · doi:10.1016/0006-8993(68)90157-1 · Cited by 100 · see citing works
Babalian, A. L., Vibert, N., Assié, G., Serafin, M., Mühlethaler, M., & Vidal, P. (1997) · Neuroscience · doi:10.1016/s0306-4522(97)00069-9 · Cited by 87 · see citing works
Morphophysiology of the Vestibular Periphery
Lysakowski, A., & Goldberg, J. M. (2004) · Springer handbook of auditory research · doi:10.1007/0-387-21567-0_3 · Cited by 86 · see citing works
The postnatal development of functional properties of central vestibular neurons in the rat
Lannou, J., Precht, W., & Cazin, L. (1979) · Brain Research · doi:10.1016/0006-8993(79)91002-3 · Cited by 79 · see citing works
The neural integrators of the mammalian saccadic system
Moschovakis, A. K. (1997) · Frontiers in bioscience · doi:10.2741/a212 · Cited by 73 · see citing works
Takazawa, T., Saito, Y., Tsuzuki, K., & Ozawa, S. (2004) · Journal of Neurophysiology · doi:10.1152/jn.00494.2004 · Cited by 69 · see citing works
Self-citationChen-Huang, C., McCREA, R. A., & Goldberg, J. M. (1997) · Experimental Brain Research · doi:10.1007/pl00005650 · Cited by 68 · see citing works
SOME THOUGHTS ABOUT THE THREE NEURONS IN THE VESTIBULAR OCULAR REFLEX*
Baker, R. G. V., Evinger, C. L., & McCREA, R. A. (1981) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1981.tb30869.x · Cited by 65 · see citing works
Dutia, M. B., & Johnston, A. R. (1998) · Experimental Brain Research · doi:10.1007/s002210050266 · Cited by 61 · see citing works
de Waele, C., Serafin, M., Khateb, A., Yabe, T., Vidal, P. P., & Mühlethaler, M. (1993) · Experimental Brain Research · doi:10.1007/bf00229780 · Cited by 56 · see citing works
Resonance of Spike Discharge Modulation in Neurons of the Guinea Pig Medial Vestibular Nucleus
Ris, L., Hachemaoui, M., Vibert, N., Godaux, E., Vidal, P. P., & Moore, L. E. (2001) · Journal of Neurophysiology · doi:10.1152/jn.2001.86.2.703 · Cited by 48 · see citing works
Graf, W. M., Baker, J. F., & Peterson, B. W. (1993) · Journal of Neurophysiology · doi:10.1152/jn.1993.70.6.2425 · Cited by 48 · see citing works
Idoux, E., Serafin, M., Fort, P., Vidal, P., Beraneck, M., Vibert, N., Mühlethaler, M., & Moore, L. E. (2006) · Journal of Neurophysiology · doi:10.1152/jn.01355.2005 · Cited by 42 · see citing works
Chapter 2 Repetitive Impulse Firing in Motoneurons: Facts and Perspectives
Kernell, D. (1999) · Progress in brain research · doi:10.1016/s0079-6123(08)62841-1 · Cited by 40 · see citing works
Intrinsic membrane properties and dynamics of medial vestibular neurons: a simulation
Av-Ron, E., & Vidal, P. (1999) · Biological Cybernetics · doi:10.1007/s004220050533 · Cited by 39 · see citing works
Intrinsic Physiological and Pharmacological Properties of Central Vestibular Neurons
Vidal, P. P., Vibert, N., Serafin, M., Babalian, A. L., M�hlethaler, M., & de Waele, C. (1998) · KARGER eBooks · doi:10.1159/000059058 · Cited by 38 · see citing works
Muscarinic regulation of spontaneously active medial vestibular neurons in vitro
Ujihara, H., Akaike, A., Sasa, M., et al. (1989) · Neuroscience Letters · doi:10.1016/0304-3940(89)90227-9 · Cited by 31 · see citing works
Membrane properties of excitatory and inhibitory neurons in the rat prepositus hypoglossi nucleus
Shino, M., Ozawa, S., Furuya, N., & Saito, Y. (2008) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2008.06204.x · Cited by 25 · see citing works
Self-citationStauffer, E. K., McDonagh, J. C., Hornby, T. G., et al. (2006) · Journal of Comparative Physiology A · doi:10.1007/s00359-006-0198-2 · Cited by 17 · see citing works
Membrane properties of rat medial vestibular nucleus neurons in vivo
Saito, Y., & Ozawa, S. (2007) · Neuroscience Research · doi:10.1016/j.neures.2007.06.1479 · Cited by 15 · see citing works
Self-citationSpontaneous activity of otolith-related vestibular nuclear neurons in the decerebrate rat
Lai, C. H., & Chan, Y. (1996) · Brain Research · doi:10.1016/s0006-8993(96)00843-8 · Cited by 14 · see citing works
In Vivo‐in Vitro Correlations in the Central Vestibular System: A Bridge Too Far?a
Vidal, P., Babalian, A. L., Vibert, N., et al. (1996) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1996.tb15717.x · Cited by 13 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Fang, X., Jiang, S., Wang, J., Bai, Y., Kim, C. S., Blake, D., Weintraub, N. L., Lei, Y., & Lu, X.-Y. (2021) · Molecular Psychiatry · doi:10.1038/s41380-020-01004-x · Cited by 95 · see citing works
- Authors
- Saito, Y., Takazawa, T., & Ozawa, S.
- Affiliations
- Gunma University (JP)
- Venue
- European Journal of Neuroscience
- Publisher
- Wiley
- Published
- 2008-07
- Volume
- 28
- Issue
- 2
- Pages
- 288-298
- ISSN
- 0953-816X (ISSN-L)
- 1460-9568
- OpenAlex
- W2148990678
- Cited by
- 27
- References
- 54
- Citations by year
- 2025: 1 · 2024: 1 · 2021: 2 · 2019: 2 · 2018: 2 · 2017: 1 · 2016: 1 · 2015: 2 · 2014: 2 · 2013: 2 · 2012: 4
- FWCI
- 0.82
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- European Journal of Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Brain Science Foundation
- Ministry of Education, Culture, Sports, Science and Technology
- Japan Society for the Promotion of Science
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ion channel regulation and function
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Neuroscience of respiration and sleep
- Keywords
- medial vestibular nucleus, afterhyperpolarization, slow afterhyperpolarization, afterdepolarizations, interspike interval coefficient of variation, apamin, calcium-activated potassium channels, vestibular neurons
- MeSH terms
- Action Potentials, Animals, Apamin, Electrophysiology, Neurons, Reaction Time, Vestibular Nuclei, Rats, Wistar, Patch-Clamp Techniques, Rats, Small-Conductance Calcium-Activated Potassium Channels, In Vitro Techniques
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
