Hostname: page-component-cd9895bd7-gvvz8 Total loading time: 0 Render date: 2024-12-24T16:32:26.111Z Has data issue: false hasContentIssue false
  • English
  • Français

Normal and rebound impulse firing in retinal ganglion cells

Published online by Cambridge University Press:  12 April 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
Get access Rights & Permissions [Opens in a new window]

Abstract

Given that the action potential output of retinal ganglion cells (RGCs) determines the nature of the visual information that is transmitted from the retina, an understanding of their intrinsic impulse firing characteristics is critical for an appreciation of the overall processing of visual information. Recordings from RGCs within an isolated whole-mount retina preparation showed that their normal impulse firing from the resting membrane potential (RMP) was linearly correlated in its frequency with the stimulus intensity. In addition to describing the relationship between the magnitude of the current injection and the resulting impulse frequency (F/I relationship), we have characterized the properties of individual action potentials when they are elicited from the RMP. In contrast, hyperpolarizing below the RMP revealed that RGCs displayed a time dependent anomalous rectification, manifested by the appearance of a depolarizing sag in their voltage response. When an adequate period of hyperpolarization was terminated, a fast phasic period of “rebound excitation” was observed, characterized by a brief phasic burst of impulse activity. When compared to equivalent action potential firing evoked by depolarizing from the RMP, rebound spiking was associated with a lower threshold and shorter latency for impulse activation as well as a prominent, phasic, burst-like doublet, or triplet of impulses. The rebound action potential had a more positive voltage overshoot and displayed a higher peak rate of rise in its upstroke than those correspondingly generated by depolarizing current pulses from the RMP. Blocking sodium spikes with TTX confirmed that the preceding hyperpolarization led to the recruitment and subsequent generation of a transient depolarizing voltage overshoot, which we have termed the net depolarizing overshoot (NDO). We propose that the NDO boosts the generation of sodium spikes by triggering rebound spikes on its upstroke and crest, thus accounting for the observed voltage dependent change in the firing pattern of RGCs.

Keywords

Anode breakThresholdLatencyAnomalous rectificationRebound excitation
Type
Research Article
Information
Visual Neuroscience , Volume 24 , Issue 1 , January 2007 , pp. 79 - 90
Copyright
© 2007 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

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.CrossRefGoogle Scholar
Barnes, S. & Werblin, F. (1986). Gated currents generate single spike activity in amacrine cells of the tiger salamander retina. Proceedings of the National Academy of Sciences of the USA 83, 1509–1512.CrossRefGoogle Scholar
Baylor, D.A. & Fettiplace, R. (1979). Synaptic drive and impulse generation in ganglion cells of turtle retina. Journal of Physiology 288, 107–127.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.CrossRefGoogle Scholar
Benison, G., Keizer, J., Chalupa, L.M. & Robinson, D.W. (2001). Modeling temporal behavior of postnatal cat retinal ganglion cells. Journal of Theoretical Biology 210, 187–199.CrossRefGoogle 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.CrossRefGoogle Scholar
Beurrier, C., Congar, P., Bioulac, B. & Hammond, C. (1999). Subthalamic nucleus neurons switch from single-spike activity to burst-firing mode. Journal of Neuroscience 19, 599–609.Google Scholar
Boiko, T., Van Wart, A., Caldwell, J.H., Levinson, S.R., Trimmer, J.S. & Matthews, G. (2003). Functional specialization of the axon initial segment by isoform-specific sodium channel targeting. Journal of Neuroscience 23, 2306–2313.Google Scholar
Brenner, R., Chen, Q.H., Vilaythong, A., Toney, G.M., Noebels, J.L. & Aldrich, R.W. (2005). BK channel beta4 subunit reduces dentate gyrus excitability and protects against temporal lobe seizures. Nature Neuroscience 8, 1752–1759.CrossRefGoogle 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
Carras, P.L., Coleman, P.A. & Miller, R.F. (1992). Site of action potential initiation in amphibian retinal ganglion cells. Journal of Neurophysiology 67, 292–304.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.CrossRefGoogle 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
Coleman, P.A. & Miller, R.F. (1989). Measurement of passive membrane parameters with whole-cell recording from neurons in the intact amphibian retina. Journal of Neurophysiology 61, 218–230.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.CrossRefGoogle 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.CrossRefGoogle 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
Diamond, J.S. & Copenhagen, D.R. (1995). The relationship between light-evoked synaptic excitation and spiking behaviour of salamander retinal ganglion cells. Journal of Physiology 487 (Pt 3), 711–725.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
Eliasof, S., Barnes, S. & Werblin, F. (1987). The interaction of ionic currents mediating single spike activity in retinal amacrine cells of the tiger salamander. Journal of Neuroscience 7, 3512–3524.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.CrossRefGoogle Scholar
Fedirchuk, B. & Dai, Y. (2004). Monoamines increase the excitability of spinal neurones in the neonatal rat by hyperpolarizing the threshold for action potential production. Journal of Physiology 557, 355–361.CrossRefGoogle 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.CrossRefGoogle Scholar
Fohlmeister, J.F., Coleman, P.A. & Miller, R.F. (1990). Modeling the repetitive firing of retinal ganglion cells. Brain Research 510, 343–345.CrossRefGoogle Scholar
Fohlmeister, J.F. & Miller, R.F. (1997a). Impulse encoding mechanisms of ganglion cells in the tiger salamander retina. Journal of Neurophysiology 78, 1935–1947.Google Scholar
Fohlmeister, J.F. & Miller, R.F. (1997b). Mechanisms by which cell geometry controls repetitive impulse firing in retinal ganglion cells. Journal of Neurophysiology 78, 1948–1964.Google Scholar
Geijo-Barrientos, E. (2000). Subthreshold inward membrane currents in guinea-pig frontal cortex neurons. Neuroscience 95, 965–972.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.CrossRefGoogle 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.CrossRefGoogle Scholar
Greffrath, W., Magerl, W., Disque-Kaiser, U., Martin, E., Reuss, S. & Boehmer, G. (2004). Contribution of Ca2+-activated K+ channels to hyperpolarizing after-potentials and discharge pattern in rat supraoptic neurones. Journal of Neuroendocrinology 16, 577–588.CrossRefGoogle Scholar
Hamasaki, D.I. & Winters, R.W. (1974). A review of the properties of sustained and transient retinal ganglion cells. Experientia 30, 713–719.CrossRefGoogle 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.CrossRefGoogle 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.CrossRefGoogle 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.CrossRefGoogle Scholar
Hidaka, S. & Ishida, A.T. (1998). Voltage-gated Na+ current availability after step- and spike-shaped conditioning depolarizations of retinal ganglion cells. Pflugers Archiv 436, 497–508.CrossRefGoogle Scholar
Hodgkin, A.L. & Huxley, A.F. (1952). A quantitative description of membrane current and its application to conduction and excitation in nerve. Journal of Physiology 117, 500–544.CrossRefGoogle Scholar
Huguenard, J.R. (1996). Low-threshold calcium currents in central nervous system neurons. Annual Review of Physiology 58, 329–348.CrossRefGoogle 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.CrossRefGoogle Scholar
Jahnsen, H. & Llinas, R. (1984). Electrophysiological properties of guinea-pig thalamic neurones: An in vitro study. Journal of Physiology 349, 205–226.CrossRefGoogle 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.CrossRefGoogle Scholar
Kaneda, M. & Kaneko, A. (1991). Voltage-gated sodium currents in isolated retinal ganglion cells of the cat: Relation between the inactivation kinetics and the cell type. Neuroscience Research 11, 261–275.CrossRefGoogle Scholar
Karschin, A. & Lipton, S.A. (1989). Calcium channels in solitary retinal ganglion cells from post-natal rat. Journal of Physiology 418, 379–396.CrossRefGoogle 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.CrossRefGoogle Scholar
Kawai, F. (2002). Ca2+-activated K+ currents regulate odor adaptation by modulating spike encoding of olfactory receptor cells. Biophysical Journal 82, 2005–2015.CrossRefGoogle 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.CrossRefGoogle 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.CrossRefGoogle 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.CrossRefGoogle 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.CrossRefGoogle Scholar
Llinas, R. & Jahnsen, H. (1982). Electrophysiology of mammalian thalamic neurones in vitro. Nature 297, 406–408.CrossRefGoogle Scholar
Llinas, R.R. (1988). The intrinsic electrophysiological properties of mammalian neurons: Insights into central nervous system function. Science 242, 1654–1664.CrossRefGoogle 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.CrossRefGoogle 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. & Johnston, D. (1995). Synaptic activation of voltage-gated channels in the dendrites of hippocampal pyramidal neurons. Science 268, 301–304.CrossRefGoogle 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.CrossRefGoogle 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.CrossRefGoogle Scholar
Melnick, I.V., Santos, S.F. & Safronov, B.V. (2004). Mechanism of spike frequency adaptation in substantia gelatinosa neurones of rat. Journal of Physiology 559, 383–395.CrossRefGoogle Scholar
Miles, G.B., Dai, Y. & Brownstone, R.M. (2005). Mechanisms underlying the early phase of spike frequency adaptation in mouse spinal motoneurones. Journal of Physiology 566, 519–532.CrossRefGoogle 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).
Mobbs, P., Everett, K. & Cook, A. (1992). Signal shaping by voltage-gated currents in retinal ganglion cells. Brain Research 574, 217–223.CrossRefGoogle Scholar
Montoro, R.J., Lopez-Barneo, J. & Jassik-Gerschenfeld, D. (1988). Differential burst firing modes in neurons of the mammalian visual cortex in vitro. Brain Research 460, 168–172.CrossRefGoogle 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
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.CrossRefGoogle 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.CrossRefGoogle Scholar
Perez-Reyes, E. (2003). Molecular physiology of low-voltage-activated T-type calcium channels. Physiological Reviews 83, 117–161.CrossRefGoogle 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.CrossRefGoogle Scholar
Robinson, R.B. & Siegelbaum, S.A. (2003). Hypepolarization activated cationic currents: From molecules to physiological function. Annual Review of Physiology 65, 453–480.CrossRefGoogle 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 (Pt 1), 55–66.Google Scholar
Sheasby, B.W. & Fohlmeister, J.F. (1999). Impulse encoding across the dendritic morphologies of retinal ganglion cells. Journal of Neurophysiology 81, 1685–1698.Google Scholar
Sherman, S.M. (1996). Dual response modes in lateral geniculate neurons: Mechanisms and functions. Visual Neuroscience 13, 205–213.CrossRefGoogle Scholar
Sherman, S.M. (2001). Tonic and burst firing: Dual modes of thalamocortical relay. Trends in Neurosciences 24, 122–126.CrossRefGoogle 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
Slaughter, M.M. & Pan, Z.H. (1992). The physiology of GABAB receptors in the vertebrate retina. Progress in Brain Research 90, 47–60.CrossRefGoogle 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.CrossRefGoogle 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
Tabata, T. & Kano, M. (2002). Heterogeneous intrinsic firing properties of vertebrate retinal ganglion cells. Journal of Neurophysiology 87, 30–41.CrossRefGoogle 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 U S A 93, 13245–13249.CrossRefGoogle Scholar
Velte, T.J. & Masland, R.H. (1999). Action potentials in the dendrites of retinal ganglion cells. Journal of Neurophysiology 81, 1412–1417.Google Scholar
Wang, G.Y., Robinson, D.W. & Chalupa, L.M. (1998). Calcium-activated potassium conductances in retinal ganglion cells of the ferret. Journal of Neurophysiology 79, 151–158.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
Wollner, D.A. & Catterall, W.A. (1986). Localization of sodium channels in axon hillocks and initial segments of retinal ganglion cells. Proceedings of the National Academy of Sciences of the U S A 83, 8424–8428.CrossRefGoogle 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