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Mechanism underlying rebound excitation in retinal ganglion cells

Published online by Cambridge University Press:  01 October 2007

PRATIP MITRA  and
ROBERT F. MILLER
PRATIP MITRA
Affiliation:
Department of Neuroscience, School of Medicine, University of Minnesota, Minneapolis, Minnesota
ROBERT F. MILLER
Affiliation:
Department of Neuroscience, School of Medicine, University of Minnesota, Minneapolis, Minnesota
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Abstract

Retinal ganglion cells (RGCs) display the phenomenon of rebound excitation, which is observed as rebound sodium action potential firing initiated at the termination of a sustained hyperpolarization below the resting membrane potential (RMP). Rebound impulse firing, in contrast to corresponding firing elicited from rest, displayed a lower net voltage threshold, shorter latency and was invariably observed as a phasic burst-like doublet of spikes. The preceding hyperpolarization leads to the recruitment of a Tetrodotoxin-insensitive depolarizing voltage overshoot, termed as the net depolarizing overshoot (NDO). Based on pharmacological sensitivities, we provide evidence that the NDO is composed of two independent but interacting components, including (1) a regenerative low threshold calcium spike (LTCS) and (2) a non-regenerative overshoot (NRO). Using voltage and current clamp recordings, we demonstrate that amphibian RGCs possess the hyperpolarization activated mixed cation channels/current, Ih, and low voltage activated (LVA) calcium channels, which underlie the generation of the NRO and LTCS respectively. At the RMP, the Ih channels are closed and the LVA calcium channels are inactivated. A hyperpolarization of sufficient magnitude and duration activates Ih and removes the inactivation of the LVA calcium channels. On termination of the hyperpolarizing influence, Ih adds an immediate depolarizing influence that boosts the generation of the LTCS. The concerted action of both conductances results in a larger amplitude and shorter latency NDO than either mechanism could achieve on its own. The NDO boosts the generation of conventional sodium spikes which are triggered on its upstroke and crest, thus eliciting rebound excitation.

Keywords

Retinalow voltage activated calcium channelsT-type calcium channelsIhaction potentials
Type
Research Article
Information
Visual Neuroscience , Volume 24 , Issue 5 , September 2007 , pp. 709 - 731
Copyright
© 2007 Cambridge University Press

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References

REFERENCES

Aizenman, C.D. & Linden, D.J. (1999). Regulation of the rebound depolarization and spontaneous firing patterns of deep nuclear neurons in slices of rat cerebellum. Journal of Neurophysiology 82, 1697–1709.Google Scholar
Akopian, A. & Witkovsky, P. (1996). D2 dopamine receptor-mediated inhibition of a hyperpolarization-activated current in rod photoreceptors. Journal of Neurophysiology 76, 1828–1835.Google Scholar
Andersen, P., Eccles, J.C. & Sears, T.A. (1964). The ventro-basal complex of the thalamus: Types of cells, their responses and their functional organization. Journal of Physiology 174, 370–399.Google Scholar
Armstrong, C.M. & Gilly, W.F. (1992). Access resistance and space clamp problems associated with whole-cell patch clamping. Methods in Enzymology 207, 100–122.Google Scholar
Bader, C.R. & Bertrand, D. (1984). Effect of changes in intra- and extracellular sodium on the inward (anomalous) rectification in salamander photoreceptors. Journal of Physiology 347, 611–631.Google Scholar
Bair, W. (1999). Spike timing in the mammalian visual system. Current Opinion in Neurobiology 9, 447–453.Google Scholar
Bal, T. & McCormick, D.A. (1997). Synchronized oscillations in the inferior olive are controlled by the hyperpolarization-activated cation current Ih. Journal of Neurophysiology 77, 3145–3156.Google Scholar
Barnes, S. (1994). After transduction: Response shaping and control of transmission by ion channels of the photoreceptor inner segments. Neuroscience 58, 447–459.Google Scholar
Belgum, J.H., Dvorak, D.R. & McReynolds, J.S. (1982). Light-evoked sustained inhibition in mudpuppy retinal ganglion cells. Vision Research 22, 257–260.Google Scholar
Berry, M.J., Warland, D.K. & Meister, M. (1997). The structure and precision of retinal spike trains. Proceedings of the National Academy of Sciences of the USA 94, 5411–5416.Google Scholar
Bootman, M.D., Collins, T.J., Peppiatt, C.M., Prothero, L.S., Mackenzie, L., De Smet, P., Travers, M., Tovey, S.C., Seo, J.T., Berridge, M.J., Ciccolini, F. & Lipp, P. (2001). Calcium signalling—an overview. Seminars in Cell and Developmental Biology 12, 3–10.Google Scholar
BoSmith, R.E., Briggs, I. & Sturgess, N.C. (1993). Inhibitory actions of ZENECA ZD7288 on whole-cell hyperpolarization activated inward current (If) in guinea-pig dissociated sinoatrial node cells. British Journal of Pharmacology 110, 343–349.Google Scholar
Brown, D.A. & Adams, P.R. (1980). Muscarinic suppression of a novel voltage-sensitive K+ current in a vertebrate neurone. Nature 283, 673–676.Google Scholar
Budde, T., White, J.A. & Kay, A.R. (1994). Hyperpolarization-activated Na+-K+ current (Ih) in neocortical neurons is blocked by external proteolysis and internal TEA. Journal of Neurophysiology 72, 2737–2742.Google Scholar
Christenson, J., Hill, R.H., Bongianni, F. & Grillner, S. (1993). Presence of low voltage activated calcium channels distinguishes touch from pressure sensory neurons in the lamprey spinal cord. Brain Research 608, 58–66.Google Scholar
Christie, B.R., Eliot, L.S., Ito, K., Miyakawa, H. & Johnston, D. (1995). Different Ca2+ channels in soma and dendrites of hippocampal pyramidal neurons mediate spike-induced Ca2+ influx. Journal of Neurophysiology 73, 2553–2557.Google Scholar
Crunelli, V., Lightowler, S. & Pollard, C.E. (1989). A T-type Ca2+ current underlies low-threshold Ca2+ potentials in cells of the cat and rat lateral geniculate nucleus. Journal of Physiology 413, 543–561.Google Scholar
De la Pena, E. & Geijo-Barrientos, E. (2000). Participation of low-threshold calcium spikes in excitatory synaptic transmission in guinea pig medial frontal cortex. European Journal of Neuroscience 12, 1679–1686.Google Scholar
Deschenes, M., Paradis, M., Roy, J.P. & Steriade, M. (1984). Electrophysiology of neurons of lateral thalamic nuclei in cat: Resting properties and burst discharges. Journal of Neurophysiology 51, 1196–1219.Google Scholar
Deschenes, M., Roy, J.P. & Steriade, M. (1982). Thalamic bursting mechanism: An inward slow current revealed by membrane hyperpolarization. Brain Research 239, 289–293.Google Scholar
Destexhe, A., Contreras, D., Steriade, M., Sejnowski, T.J. & Huguenard, J.R. (1996). In vivo, in vitro, and computational analysis of dendritic calcium currents in thalamic reticular neurons. Journal of Neuroscience 16, 169–185.Google Scholar
Destexhe, A., Neubig, M., Ulrich, D. & Huguenard, J. (1998). Dendritic low-threshold calcium currents in thalamic relay cells. Journal of Neuroscience 18, 3574–3588.Google Scholar
DiFrancesco, D. (1982). Block and activation of the pace-maker channel in calf purkinje fibres: Effects of potassium, caesium and rubidium. Journal of Physiology 329, 485–507.Google Scholar
DiFrancesco, D., Ferroni, A., Mazzanti, M. & Tromba, C. (1986). Properties of the hyperpolarizing-activated current (if) in cells isolated from the rabbit sino-atrial node. Journal of Physiology 377, 61–88.Google Scholar
Dowling, J.E. & Werblin, F.S. (1969). Organization of retina of the mudpuppy, Necturus maculosus. I. Synaptic structure. Journal of Neurophysiology 32, 315–338.Google Scholar
Eller, P., Berjukov, S., Wanner, S., Huber, I., Hering, S., Knaus, H.G., Toth, G., Kimball, S.D. & Striessnig, J. (2000). High affinity interaction of mibefradil with voltage-gated calcium and sodium channels. British Journal of Pharmacology 130, 669–677.Google Scholar
Eng, D.L., Gordon, T.R., Kocsis, J.D. & Waxman, S.G. (1990). Current-clamp analysis of a time-dependent rectification in rat optic nerve. Journal of Physiology 421, 185–202.Google Scholar
Felix, R., Sandoval, A., Sanchez, D., Gomora, J.C., De la Vega-Beltran, J.L., Trevino, C.L. & Darszon, A. (2003). ZD7288 inhibits low-threshold Ca2+ channel activity and regulates sperm function. Biochemical and Biophysical Research Communications 311, 187–192.Google Scholar
Foehring, R.C. & Waters, R.S. (1991). Contributions of low-threshold calcium current and anomalous rectifier (Ih) to slow depolarizations underlying burst firing in human neocortical neurons in vitro. Neuroscience Letters 124, 17–21.Google Scholar
Fohlmeister, J.F. & Miller, R.F. (1997). Impulse encoding mechanisms of ganglion cells in the tiger salamander retina. Journal of Neurophysiology 78, 1935–1947.Google Scholar
Funahashi, M., Mitoh, Y., Kohjitani, A. & Matsuo, R. (2003). Role of the hyperpolarization-activated cation current (Ih) in pacemaker activity in area postrema neurons of rat brain slices. Journal of Physiology 552, 135–148.Google Scholar
Gerber, U., Greene, R.W. & McCarley, R.W. (1989). Repetitive firing properties of medial pontine reticular formation neurones of the rat recorded in vitro. Journal of Physiology 410, 533–560.Google Scholar
Gillessen, T. & Alzheimer, C. (1997). Amplification of EPSPs by low Ni2+- and amiloride-sensitive Ca2+ channels in apical dendrites of rat CA1 pyramidal neurons. Journal of Neurophysiology 77, 1639–1643.Google Scholar
Gordon, T.R., Kocsis, J.D. & Waxman, S.G. (1990). Electrogenic pump (Na+/K+-ATPase) activity in rat optic nerve. Neuroscience 37, 829–837.Google Scholar
Greene, R.W., Haas, H.L. & McCarley, R.W. (1986). A low threshold calcium spike mediates firing pattern alterations in pontine reticular neurons. Science 234, 738–740.Google Scholar
Gutierrez, C., Cox, C.L., Rinzel, J. & Sherman, S.M. (2001). Dynamics of low-threshold spike activation in relay neurons of the cat lateral geniculate nucleus. Journal of Neuroscience 21, 1022–1032.Google Scholar
Hagiwara, N. & Irisawa, H. (1989). Modulation by intracellular Ca2+ of the hyperpolarization-activated inward current in rabbit single sino-atrial node cells. Journal of Physiology 409, 121–141.Google Scholar
Halliwell, J.V. & Adams, P.R. (1982). Voltage-clamp analysis of muscarinic excitation in hippocampal neurons. Brain Research 250, 71–92.Google Scholar
Hamasaki, D.I. & Winters, R.W. (1974). A review of the properties of sustained and transient retinal ganglion cells. Experientia 30, 713–719.Google Scholar
Hamill, O.P., Marty, A., Neher, E., Sakmann, B. & Sigworth, F.J. (1981). Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Archiv 391, 85–100.Google Scholar
Harris, N.C. & Constanti, A. (1995). Mechanism of block by ZD 7288 of the hyperpolarization-activated inward rectifying current in guinea pig substantia nigra neurons in vitro. Journal of Neurophysiology 74, 2366–2378.Google Scholar
Heady, T.N., Gomora, J.C., Macdonald, T.L. & Perez-Reyes, E. (2001). Molecular pharmacology of T-type Ca2+ channels. Japanese Journal of Pharmacology 85, 339–350.Google Scholar
Henderson, D. & Miller, R.F. (2003). Evidence for low-voltage-activated (LVA) calcium currents in the dendrites of tiger salamander retinal ganglion cells. Visual Neuroscience 20, 141–152.Google Scholar
Henderson, D. & Miller, R.F. (2007). Low-voltage activated calcium currents in ganglion cells of the tiger salamander retina: Experiment and simulation. Visual Neuroscience 24, 37–51.Google Scholar
Henze, D.A. & Buzsaki, G. (2001). Action potential threshold of hippocampal pyramidal cells in vivo is increased by recent spiking activity. Neuroscience 105, 121–130.Google Scholar
Hestrin, S. (1987). The properties and function of inward rectification in rod photoreceptors of the tiger salamander. Journal of Physiology 390, 319–333.Google Scholar
Hodgkin, A.L. & Huxley, A.F. (1952). A quantitative description of membrane current and its applications to conduction and excitation in nerve. Journal of Physiology (Lond) 117, 500–544.Google Scholar
Hughes, S.W., Cope, D.W. & Crunelli, V. (1998). Dynamic clamp study of Ih modulation of burst firing and delta oscillations in thalamocortical neurons in vitro. Neuroscience 87, 541–550.Google Scholar
Huguenard, J.R. (1996). Low-threshold calcium currents in central nervous system neurons. Annual Review of Physiology 58, 329–348.Google Scholar
Huguenard, J.R. & Prince, D.A. (1994). Intrathalamic rhythmicity studied in vitro: Nominal T-current modulation causes robust antioscillatory effects. Journal of Neuroscience 14, 5485–5502.Google Scholar
Ishida, A.T. (1995). Ion channel components of retinal ganglion cells. Progress in Retinal and Eye Research 15, 261–280.Google Scholar
Ishida, A.T. (1998). Transient and persistent Na, Ca and mixed-cation currents in retinal ganglion cells. In Development and Organization of the Retina, eds. Chalupa, L.M. & Finlay, B.L., pp. 201–225. New York: Plenum.
Ishida, A.T. (2000). Deactivation, recovery from inactivation, and modulation of extra-synaptic ion currents in fish retinal ganglion cells. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 355, 1191–1194.Google Scholar
Jahnsen, H. & Llinas, R. (1984). Electrophysiological properties of guinea-pig thalamic neurones: An in vitro study. Journal of Physiology 349, 205–226.Google Scholar
Johnston, D., Magee, J.C., Colbert, C.M. & Cristie, B.R. (1996). Active properties of neuronal dendrites. Annual Review of Neuroscience 19, 165–186.Google Scholar
Karschin, A. & Lipton, S.A. (1989). Calcium channels in solitary retinal ganglion cells from post-natal rat. Journal of Physiology 418, 379–396.Google Scholar
Karst, H., Joels, M. & Wadman, W.J. (1993). Low-threshold calcium current in dendrites of the adult rat hippocampus. Neuroscience Letters 164, 154–158.Google Scholar
Kawai, F., Kurahashi, T. & Kaneko, A. (1996). T-type Ca2+ channel lowers the threshold of spike generation in the newt olfactory receptor cell. Journal of General Physiology 108, 525–535.Google Scholar
Kawai, F., Kurahashi, T. & Kaneko, A. (1997). Quantitative analysis of Na+ and Ca2+ current contributions on spike initiation in the newt olfactory receptor cell. Japanese Journal of Physiology 47, 367–376.Google Scholar
Kawai, F. & Miyachi, E. (2001). Enhancement by T-type Ca2+ currents of odor sensitivity in olfactory receptor cells. Journal of Neuroscience 21, RC144.Google Scholar
Koyano, K., Funabiki, K. & Ohmori, H. (1996). Voltage-gated ionic currents and their roles in timing coding in auditory neurons of the nucleus magnocellularis of the chick. Neuroscience Research 26, 29–45.Google Scholar
Larkman, P.M. & Kelly, J.S. (2001). Modulation of the hyperpolarisation-activated current, Ih, in rat facial motoneurones in vitro by ZD-7288. Neuropharmacology 40, 1058–1072.Google Scholar
Lee, S.C., Hayashida, Y. & Ishida, A.T. (2003). Availability of low-threshold Ca2+ current in retinal ganglion cells. Journal of Neurophysiology 90, 3888–3901.Google Scholar
Lee, S.C. & Ishida, A.T. (2007). Ih without Kir in adult rat retinal ganglion cells. Journal of Neurophysiology 97, 3790–3799.Google Scholar
Liu, Y. & Lasater, E.M. (1994). Calcium currents in turtle retinal ganglion cells. I. The properties of T- and L-type currents. Journal of Neurophysiology 71, 733–742.Google Scholar
Llinas, R. (1990). Intrinsic electrical properties of nerve cells and their role in network oscillation. Cold Spring Harbor Symposia on Quantitative Biology 55, 933–938.Google Scholar
Llinas, R., Greenfield, S.A. & Jahnsen, H. (1984). Electrophysiology of pars compacta cells in the in vitro substantia nigra: A possible mechanism for dendritic release. Brain Research 294, 127–132.Google Scholar
Llinas, R. & Jahnsen, H. (1982). Electrophysiology of mammalian thalamic neurones in vitro. Nature 297, 406–408.Google Scholar
Llinas, R.R. (1988). The intrinsic electrophysiological properties of mammalian neurons: Insights into central nervous system function. Science 242, 1654–1664.Google Scholar
Llinas, R.R. & Alonso, A. (1992). Electrophysiology of the mammillary complex in vitro. I. Tuberomammillary and lateral mammillary neurons. Journal of Neurophysiology 68, 1307–1320.Google Scholar
Lorincz, A., Notomi, T., Tamas, G., Shigemoto, R. & Nusser, Z. (2002). Polarized and compartment-dependent distribution of HCN1 in pyramidal cell dendrites. Nature Neuroscience 5, 1185–1193.Google Scholar
Maccaferri, G. & McBain, C.J. (1996). The hyperpolarization-activated current (Ih) and its contribution to pacemaker activity in rat CA1 hippocampal stratum oriens-alveus interneurones. Journal of Physiology 497, 119–130.Google Scholar
Magee, J.C. (1998). Dendritic hyperpolarization-activated currents modify the integrative properties of hippocampal CA1 pyramidal neurons. Journal of Neuroscience 18, 7613–7624.Google Scholar
Magee, J.C., Christofi, G., Miyakawa, H., Christie, B., Lasser-Ross, N. & Johnston, D. (1995). Subthreshold synaptic activation of voltage-gated Ca2+ channels mediates a localized Ca2+ influx into the dendrites of hippocampal pyramidal neurons. Journal of Neurophysiology 74, 1335–1342.Google Scholar
Magee, J.C. & Johnston, D. (1995). Synaptic activation of voltage-gated channels in the dendrites of hippocampal pyramidal neurons. Science 268, 301–304.Google Scholar
Margolis, D.J. & Detwiler, P.B. (2007). Different mechanisms generate maintained activity in ON and OFF retinal ganglion cells. Journal of Neuroscience 27, 5994–6005.Google Scholar
Martin, R.L., Lee, J.H., Cribbs, L.L., Perez-Reyes, E. & Hanck, D.A. (2000). Mibefradil block of cloned T-type calcium channels. Journal of Pharmacology and Experimental Therapeutics 295, 302–308.Google Scholar
Mayer, M.L. & Westbrook, G.L. (1983). A voltage-clamp analysis of inward (anomalous) rectification in mouse spinal sensory ganglion neurones. Journal of Physiology 340, 19–45.Google Scholar
McCormick, D.A. & Bal, T. (1997). Sleep and arousal: Thalamocortical mechanisms. Annual Review of Neuroscience 20, 185–215.Google Scholar
McCormick, D.A. & Feeser, H.R. (1990). Functional implications of burst firing and single spike activity in lateral geniculate relay neurons. Neuroscience 39, 103–113.Google Scholar
McDonough, S.I. & Bean, B.P. (1998). Mibefradil inhibition of T-type calcium channels in cerebellar purkinje neurons. Molecular Pharmacology 54, 1080–1087.Google Scholar
McNulty, M.M. & Hanck, D.A. (2004). State-dependent mibefradil block of Na+ channels. Molecular Pharmacology 66, 1652–1661.Google Scholar
Miller, R.F., Frumkes, T.E., Slaughter, M. & Dacheux, R.F. (1981). Physiological and pharmacological basis of GABA and glycine action on neurons of mudpuppy retina. II. Amacrine and ganglion cells. Journal of Neurophysiology 45, 764–782.Google Scholar
Mitra, P. & Miller, R.F. (2003). How retinal ganglion cells encode anodal break excitation: The role of T-type Ca2+ and Ih channels. Association for Research in Vision and Ophthalmology (E-Abstract 5197).Google Scholar
Mitra, P. & Miller, R.F. (2007). Normal and rebound impulse firing in retinal ganglion cells. Visual Neuroscience 24, 79–90.Google Scholar
Mitra, P. & Slaughter, M.M. (2002). Mechanism of generation of spontaneous miniature outward currents (SMOCs) in retinal amacrine cells. Journal of General Physiology 119, 355–372.Google Scholar
Mouginot, D., Bossu, J.L. & Gahwiler, B.H. (1997). Low-threshold Ca2+ currents in dendritic recordings from Purkinje cells in rat cerebellar slice cultures. Journal of Neuroscience 17, 160–170.Google Scholar
Mulle, C., Madariaga, A. & Deschenes, M. (1986). Morphology and electrophysiological properties of reticularis thalami neurons in cat: In vivo study of a thalamic pacemaker. Journal of Neuroscience 6, 2134–2145.Google Scholar
Muller, W. & Lux, H.D. (1993). Analysis of voltage-dependent membrane currents in spatially extended neurons from point-clamp data. Journal of Neurophysiology 69, 241–247.Google Scholar
O'Brien, B.J., Isayama, T., Richardson, R. & Berson, D.M. (2002). Intrinsic physiological properties of cat retinal ganglion cells. Journal of Physiology 538, 787–802.Google Scholar
Pape, H.C. (1996). Queer current and pacemaker: The hyperpolarization-activated cation current in neurons. Annual Review of Physiology 58, 299–327.Google Scholar
Perez-Reyes, E. (1998). Molecular characterization of a novel family of low voltage-activated, T-type, calcium channels. Journal of Bioenergetics and Biomembranes 30, 313–318.Google Scholar
Perez-Reyes, E. (1999). Three for T: Molecular analysis of the low voltage-activated calcium channel family. Cellular and Molecular Life Sciences 56, 660–669.Google Scholar
Perez-Reyes, E. (2003). Molecular Physiology of Low-Voltage-Activated T-type Calcium Channels. Physiological Reviews 83, 117–161.Google Scholar
Ranjan, R., Chiamvimonvat, N., Thakor, N.V., Tomaselli, G.F. & Marban, E. (1998). Mechanism of anode break stimulation in the heart. Biophysical Journal 74, 1850–1863.Google Scholar
Robbins, J., Reynolds, A.M., Treseder, S. & Davies, R. (2003). Enhancement of low-voltage-activated calcium currents by group II metabotropic glutamate receptors in rat retinal ganglion cells. Molecular and Cellular Neurosciences 23, 341–350.Google Scholar
Robinson, R.B. & Siegelbaum, S.A. (2003). Hyperpolarization activated cationic currents: From molecules to physiological function. Annual Review of Physiology 65, 453–480.Google Scholar
Russo, R.E. & Hounsgaard, J. (1996). Burst-generating neurones in the dorsal horn in an in vitro preparation of the turtle spinal cord. Journal of Physiology 493, 55–66.Google Scholar
Santoro, B. & Tibbs, G.R. (1999). The HCN gene family: Molecular basis of the hyperpolarization-activated pacemaker channels. Annals of the New York Academy of Sciences 868, 741–764.Google Scholar
Scott, R.H., Wootton, J.F. & Dolphin, A.C. (1990). Modulation of neuronal T-type calcium channel currents by photoactivation of intracellular guanosine 5'-O(3-thio) triphosphate. Neuroscience 38, 285–294.Google Scholar
Sherman, S.M. (1996). Dual response modes in lateral geniculate neurons: Mechanisms and functions. Visual Neuroscience 13, 205–213.Google Scholar
Sherman, S.M. (2001). Tonic and burst firing: Dual modes of thalamocortical relay. Trends in Neurosciences 24, 122–126.Google Scholar
Slaughter, M.M. & Bai, S.H. (1989). Differential effects of baclofen on sustained and transient cells in the mudpuppy retina. Journal of Neurophysiology 61, 374–381.Google Scholar
Solomon, J.S. & Nerbonne, J.M. (1993). Hyperpolarization-activated currents in isolated superior colliculus-projecting neurons from rat visual cortex. Journal of Physiology 462, 393–420.Google Scholar
Soltesz, I., Lightowler, S., Leresche, N., Jassik-Gerschenfeld, D., Pollard, C.E. & Crunelli, V. (1991). Two inward currents and the transformation of low-frequency oscillations of rat and cat thalamocortical cells. Journal of Physiology 441, 175–197.Google Scholar
Spruston, N., Jaffe, D.B., Williams, S.H. & Johnston, D. (1993). Voltage- and space-clamp errors associated with the measurement of electrotonically remote synaptic events. Journal of Neurophysiology 70, 781–802.Google Scholar
Sundgren-Andersson, A.K. & Johansson, S. (1998). Calcium spikes and calcium currents in neurons from the medial preoptic nucleus of rat. Brain Research 783, 194–209.Google Scholar
Suzuki, S. & Rogawski, M.A. (1989). T-type calcium channels mediate the transition between tonic and phasic firing in thalamic neurons. Proceedings of the National Academy of Sciences of the USA 86, 7228–7232.Google Scholar
Tabata, T. & Ishida, A.T. (1996). Transient and sustained depolarization of retinal ganglion cells by Ih. Journal of Neurophysiology 75, 1932–1943.Google Scholar
Taylor, W.R., Mittman, S. & Copenhagen, D.R. (1996). Passive electrical cable properties and synaptic excitation of tiger salamander retinal ganglion cells. Visual Neuroscience 13, 979–990.Google Scholar
Ulrich, D. & Huguenard, J.R. (1996). Gamma-aminobutyric acid type B receptor-dependent burst-firing in thalamic neurons: A dynamic clamp study. Proceedings of the National Academy of Sciences of the USA 93, 13245–13249.Google Scholar
Vaquero, C.F., Pignatelli, A., Partida, G.J. & Ishida, A.T. (2001). A dopamine- and protein kinase A-dependent mechanism for network adaptation in retinal ganglion cells. Journal of Neuroscience 21, 8624–8635.Google Scholar
Velte, T.J. & Miller, R.F. (1995). Dendritic integration in ganglion cells of the mudpuppy retina. Visual Neuroscience 12, 165–175.Google Scholar
Velte, T.J. & Miller, R.F. (1996). Computer simulations of voltage clamping retinal ganglion cells through whole-cell electrodes in the soma. Journal of Neurophysiology 75, 2129–2143.Google Scholar
Werblin, F.S. & Dowling, J.E. (1969). Organization of the retina of the mudpuppy, Necturus maculosus. II. Intracellular recording. Journal of Neurophysiology 32, 339–355.Google Scholar
Womble, M.D. & Moises, H.C. (1993). Hyperpolarization-activated currents in neurons of the rat basolateral amygdala. Journal of Neurophysiology 70, 2056–2065.Google Scholar
Zhan, X.J., Cox, C.L., Rinzel, J. & Sherman, S.M. (1999). Current clamp and modeling studies of low-threshold calcium spikes in cells of the cat's lateral geniculate nucleus. Journal of Neurophysiology 81, 2360–2373.Google Scholar
Zhan, X.J., Cox, C.L. & Sherman, S.M. (2000). Dendritic depolarization efficiently attenuates low-threshold calcium spikes in thalamic relay cells. Journal of Neuroscience 20, 3909–3914.Google Scholar
Zhou, Z. & Lipsius, S.L. (1993). Effect of isoprenaline on If current in latent pacemaker cells isolated from cat right atrium: Ruptured vs. perforated patch whole-cell recording methods. Pflugers Archiv 423, 442–447.Google Scholar