Effect of 4-aminopyridine-sensitive potassium current on high frequency tonic firing of the rat retinal ganglion cells
Kuznetsov KI, Maslov VIu, Fedulova SA, Veselovs'kyĭ MS
- O.O.Bogomoletz Institute of Physiology, National Academy of Sciences of Ukraine, Kyiv, Ukraine
- International Center Molecular Physiology, National Academy of Sciences of Ukraine, Kyiv, Ukraine
DOI: https://doi.org/10.15407/fz56.06.022
Abstract
High frequency firing properties of the rat retinal ganglion cells and role of 4-AP-sensitive potassium current in firing generation were studied using whole cell patch-clamp techniques. Potassium channel blocker 4-AP (0,2 mM) reduced depolarization-evoked firing rate by 62% (from 50 ± 5, n = 12 to 19 ± 2 Hz, n = 7). Single action potential parameters were affected: half-width was increased by 133% (from 1,2 ± 0,1, n = 12 to 2,8 ± 0,3 ms, n = 7), decay slope was decreased by 63% (from 102 ± 11, n = 12 to 38 ± 7 mV/ms, n = 7) and afterhyperpolarization amplitude by 83% (from 18 ± 2, n = 12 to 3 ± 2 mV, n = 7). 4-AP application (0,2 mM) reduced potassium current amplitude of the retinal neurons. 4-AP-sensitive current was obtained by digital subtraction of current that was registered in the presence of the blocker from control current records (1,61 ± 0,22 nA, n = 6). 4-AP-sensitive current was equal to 0,40 ± 0,09 nA (n = 6). Thus, moderate (25%) reducing of potassium current amplitude leads to essential changes in firing properties of retinal neurons. 4-AP-sensitive residual current was similar to Kv3.1/Kv3.2 potassium currents that were described in literature previously. Moreover, we excluded the possibility of 4-AP influence on Kv1 channels by specific blocker a-dendrotoxin (100 nM) application. Such applications significantly affected neither firing frequency nor single action potential parameters. The data obtained suggest that 4-AP-sensitive current plays a key role in high frequency firing generation in the rat retinal ganglion cells. We assume that the 4-AP-sensitive current is mediated by Kv3.1/Kv3.2 conductance.
Keywords:
retinal ganglion cell, high frequency tonic firing, 4-AP
References
- Coetzee W. A., Amarillo Y, Chiu J., Chow A., Lau D., McCormack T., Moreno H., Nadal M. S., Ozaita A., Pountney D., Saganich M., Vega-Saenz d. M., Rudy B. Molecular diversity of K+ channels . Ann. N.Y.Acad.Sci. 1999. 868. P. 233-285.
CrossRef
PubMed
- Dallas M. L., Atkinson L., Milligan C. J., Morris N. P., Lewis D. I., Deuchars S. A., Deuchars J. Localization and function of the Kv3.1b subunit in the rat medulla oblongata: focus on the nucleus tractus solitarii . J.Physiol. 2005. 562, N 3. P. 655-672.
CrossRef
PubMed PubMedCentral
- Erisir A., Lau D., Rudy B., Leonard C. S. Function of specific K(+) channels in sustained high-frequency firing of fast-spiking neocortical interneurons . J.Neuro-physiol. 1999. 82, N 5. P. 2476-2489.
CrossRef
PubMed
- Gutman G. A., Chandy K. G., Grissmer S., Lazdunski M., McKinnon D., Pardo L. A., Robertson G. A., Rudy B., Sanguinetti M. C, Stuhmer W., Wang X. International Union of Pharmacology. LIII. Nomenclature and molecular relationships of voltage-gated potassium channels . Pharmacol.Rev. 2005. 57, N 4. P. 473-508.
CrossRef
PubMed
- Henne J., Jeserich G. Maturation of spiking activity in trout retinal ganglion cells coincides with upregulation of Kv3.1- and BK-related potassium channels . J.Neurosci.Res. 2004. 75, N 1. P. 44-54.
CrossRef
PubMed
- Holtje M., Brunk I., Grosse J., Beyer E., Veh R. W., Bergmann M., Grosse G., Ahnert-Hilger G. Differential distribution of voltage-gated potassium channels Kv1.1 Kv1.6 in the rat retina during development . J.Neurosci.Res. 2007. 85, N 1. P. 19-33.
CrossRef
PubMed
- Koeberle P. D., Wang Y., Schlichter L. C. Kv1.1 and Kv1.3 channels contribute to the degeneration of retinal ganglion cells after optic nerve transection in vivo .Cell Death and Diff. 2010. 17, N 1. P. 134-144.
CrossRef
- Lien C. C., Jonas P. Kv3 potassium conductance is necessary and kinetically optimized for high-frequency action potential generation in hippocampal interneu-rons . J.Neurosci. 2003. 23, N 6.- P. 2058-2068.
CrossRef
PubMed PubMedCentral
- Martina M., Metz A. E., Bean B. P. Voltage-dependent potassium currents during fast spikes of rat cerebellar Purkinje neurons: inhibition by BDS-I toxin . J.Neurophysiol. 2007. 97, N 1. P. 563-571.
CrossRef
PubMed
- O'Brien B. J., Isayama T., Richardson R., Berson D. M. Intrinsic physiological properties of cat retinal ganglion cells . J.Physiol. 2002. 538, N 3. P. 787-802.
CrossRef
PubMed PubMedCentral
- Rudy B., Chow A., Lau D., Amarillo Y., Ozaita A., Saganich M., Moreno H., Nadal M. S., Hernandez-Pineda R., Hernandez-Cruz A., Erisir A., Leonard C, Vega-Saenz d. M. Contributions of Kv3 channels to neuronal excitability . Ann.N.Y.Acad.Sci. 1999. 868. P. 304-343.
CrossRef
PubMed
- Rudy B., McBain C. J. Kv3 channels: voltage-gated K+ channels designed for high-frequency repetitive firing . Trends Neurosci. 2001. 24, N 9. P. 517-526.
CrossRef
- Wang G. Y., Ratto G., Bisti S., Chalupa L. M. Functional development of intrinsic properties in ganglion cells of the mammalian retina . J.Neurophysiol. 1997. 78, N 6.- P. 2895-2903.
CrossRef
PubMed
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