Hostname: page-component-7bb8b95d7b-w7rtg Total loading time: 0 Render date: 2024-09-17T14:11:54.385Z Has data issue: false hasContentIssue false

Narrow and wide field amacrine cells fire action potentials in response to depolarization and light stimulation

Published online by Cambridge University Press:  19 July 2007

STEPHANIE J. HEFLIN
Affiliation:
Program in Neuroscience, Boston University, Boston Massachusetts
PAUL B. COOK
Affiliation:
Program in Neuroscience, Boston University, Boston Massachusetts Biology Department, Boston University, Boston Massachusetts

Abstract

Action potentials in amacrine cells are important for lateral propagation of signals across the inner retina, but it is unclear how many subclasses of amacrine cells contain voltage-gated sodium channels or can fire action potentials. This study investigated the ability of amacrine cells with narrow (< 200 μm) and wide (> 200 μm) dendritic fields to fire action potentials in response to depolarizing current injections and light stimulation. The pattern of action potentials evoked by current injections revealed two distinct classes of amacrine cells; those that responded with a single action potential (single-spiking cells) and those that responded with repetitive action potentials (repetitive-spiking cells). Repetitive-spiking cells differed from single-spiking cells in several regards: Repetitive-spiking cells were more often wide field cells, while single-spiking cells were more often narrow field cells. Repetitive-spiking cells had larger action potential amplitudes, larger peak voltage-gated NaV currents lower action potential thresholds, and needed less current to induce action potentials. However, there was no difference in the input resistance, holding current or time constant of these two classes of cells. The intrinsic capacity to fire action potentials was mirrored in responses to light stimulation; single-spiking amacrine cells infrequently fired action potentials to light steps, while repetitive-spiking amacrine cells frequently fired numerous action potentials. These results indicate that there are two physiologically distinct classes of amacrine cells based on the intrinsic capacity to fire action potentials.

Type
Research Article
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

Awatramani, G.B. & Slaughter, M.M. (2000). Origin of transient and sustained responses in ganglion cells of the retina. Journal of Neuroscience 20, 70677095.Google Scholar
Barlow, H.B. (1953). Summation of inhibition in the frog's retina. Journal of Physiology (London) 119, 6988.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 Science USA 83, 15091512.CrossRefGoogle Scholar
Belgum, J.H., Dvorak, D.R. & McReynolds, J.S. (1984). Strychnine blocks transient but not sustained inhibition in mudpuppy retinal ganglion cells. Journal of Physiology (London) 354, 273286.CrossRefGoogle Scholar
Bieda, M.C. & Copenhagen, D.R. (1999). Sodium action potentials are not required for light-evoked release of GABA or glycine from retinal amacrine cells. Journal of Neurophysiology 81, 30923095.CrossRefGoogle Scholar
Bloomfield, S.A. (1992). Relationship between receptive and dendritic field size of amacrine cells in the rabbit retina. Journal of Neurophysiology 68, 711725.CrossRefGoogle Scholar
Bloomfield, S.A. & Dacheux, R.F. (2001). Rod vision: Pathways and processing in the mammalian retina. Progress in Retinal Eye Research 20, 351384.CrossRefGoogle Scholar
Bloomfield, S.A. & Xin, D. (2000). Surround inhibition of mammalian AII amacrine cells is generated in the proximal retina. Journal of Physiology (London) 523, 771783.CrossRefGoogle 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, 23062313.Google Scholar
Boos, R., Schneider, H. & Wassle, H. (1993). Voltage- and transmitter-gated currents of all-amacrine cells in a slice preparation of the rat retina. Journal of Neuroscience 13, 28742888.Google Scholar
Catterall, W.A. (2000). From ionic currents to molecular mechanisms: The structure and function of voltage-gated sodium channels. Neuron 26, 1325.CrossRefGoogle Scholar
Chavez, A.E., Singer, J.H. & Diamond, J.S. (2006). Fast neurotransmitter release triggered by Ca influx through AMPA-type glutamate receptors. Nature 443, 705708.CrossRefGoogle Scholar
Cook, P.B., Lukasiewicz, P.D. & McReynolds, J.S. (1998). Action potentials are required for the lateral transmission of glycinergic transient inhibition in the amphibian retina. Journal of Neuroscience 18, 23012308.Google Scholar
Cook, P.B. & McReynolds, J.S. (1998). Lateral inhibition in the inner retina is important for spatial tuning of ganglion cells. Nature Neuroscience 1, 714719.CrossRefGoogle Scholar
Cook, P.B. & Werblin, F.S. (1994). Spike initiation and propagation in wide field transient amacrine cells of the salamander retina. Journal of Neuroscience 14, 38523861.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, 35123524.CrossRefGoogle Scholar
Famiglietti, E.V., Jr. & Kolb, H. (1976). Structural basis for ON-and OFF-center responses in retinal ganglion cells. Science 194, 193195.CrossRefGoogle Scholar
Famiglietti, E.V., Jr. & Kolb, H. (1975). A bistratified amacrine cell and synaptic circuitry in the inner plexiform layer of the retina. Brain Research 84, 293300.CrossRefGoogle Scholar
Fenwick, E.M., Marty, A. & Neher, E. (1982). A patch-clamp study of bovine chromaffin cells and of their sensitivity to acetylcholine. Journal of Physiology 331, 577597.CrossRefGoogle Scholar
Flores-Herr, N., Protti, D.A. & Wassle, H. (2001). Synaptic currents generating the inhibitory surround of ganglion cells in the mammalian retina. Journal of Neuroscience 21, 48524863.Google Scholar
Fohlmeister, J.F. & Miller, R.F. (1997a). Impulse encoding mechanisms of ganglion cells in the tiger salamander retina. Journal of Neurophysiology 78, 19351947.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, 19481964.Google Scholar
Goldin, A.L. (2002). Evolution of voltage-gated Na+ channels. Journal of Experimental Biology 205, 575584.Google Scholar
Habermann, C.J., O'Brien, B.J., Wassle, H. & Protti, D.A. (2003). AII amacrine cells express L-type calcium channels at their output synapses. Journal of Neuroscience 23, 69046913.Google Scholar
Ichinose, T., Shields, C.R. & Lukasiewicz, P.D. (2005). Sodium channels in transient retinal bipolar cells enhance visual responses in ganglion cells. Journal of Neuroscience 25, 18561865.Google Scholar
Kaneko, A. (1973). Receptive field organization of bipolar and amacrine cells in the goldfish retina. Journal of Physiology (London) 235, 133153.CrossRefGoogle Scholar
Lukasiewicz, P. & Werblin, F. (1988). Slowly inactivating potassium current truncates spike activity in ganglion cells of the tiger salamander retina. Journal of Neuroscience 8, 44704481.CrossRefGoogle Scholar
Maguire, G. (1999). Rapid desensitization converts prolonged glutamate release into a transient EPSC at ribbon synapses between retinal bipolar and amacrine cells. European Journal of Neuroscience 11, 353362.CrossRefGoogle Scholar
Maguire, G., Lukasiewicz, P. & Werblin, F. (1989). Amacrine cell interactions underlying the response to change in the tiger salamander retina. Journal of Neuroscience 9, 726735.CrossRefGoogle Scholar
Miller, R.F. & Dacheux, R.F. (1976a). Synaptic organization and ionic basis of on and off channels in mudpuppy retina. I. Intracellular analysis of chloride-sensitive electrogenic properties of receptors, horizontal cells, bipolar cells, and amacrine cells. Journal of General Physiology 67, 639659.Google Scholar
Miller, R.F. & Dacheux, R.F. (1976b). Dendritic and somatic spikes in mudpuppy amacrine cells: Identification and TTX sensitivity. Brain Research 104, 157162.Google Scholar
Miller, R.F. & Dacheux, R.F. (1983). Intracellular chloride in retinal neurons: Measurement and meaning. Vision Research 23, 399411.CrossRefGoogle Scholar
Miller, R.F., Staff, N.P. & Velte, T.J. (2006). Form and function of ON-OFF amacrine cells in the amphibian retina. Journal of Neurophysiology 95, 31713190.CrossRefGoogle Scholar
Olveczky, B.P., Baccus, S.A. & Meister, M. (2003). Segregation of object and background motion in the retina. Nature 423, 401408.CrossRefGoogle Scholar
Pang, J.J., Gao, F. & Wu, S.M. (2002). Segregation and integration of visual channels: Layer-by-layer computation of ON-OFF signals by amacrine cell dendrites. Journal of Neuroscience 22, 46934701.CrossRefGoogle Scholar
Pang, J.J., Gao, F. & Wu, S.M. (2004). Stratum-by-stratum projection of light response attributes by retinal bipolar cells of Ambystoma. Journal of Physiology 558, 249262.CrossRefGoogle Scholar
Roska, B., Nemeth, E. & Werblin, F. (1998). Response to change is facilitated by a three-neuron disinhibitory pathway in the tiger salamander retina. Journal of Neuroscience 18, 34513459.Google Scholar
Roska, B. & Werblin, F. (2001). Vertical interactions across tens parallel, stacked representations in the mammalian retina. Nature 410, 583587.CrossRefGoogle Scholar
Roska, B. & Werblin, F. (2003). Rapid global shifts in natural scenes block spiking in specific ganglion cell types. Nature Neuroscience 6, 600608.CrossRefGoogle Scholar
Schwartz, E.A. (1973). Organization of on-off cells in the retina of the turtle. Journal of Physiology (London) 230, 114.CrossRefGoogle Scholar
Shields, C.R. & Lukasiewicz, P.D. (2003). Spike-dependent GABA inputs to bipolar cell axon terminals contribute to lateral inhibition of retinal ganglion cells. Journal of Neurophysiology 89, 24492458.CrossRefGoogle Scholar
Taylor, W.R. (1999). TTX attenuates surround inhibition in rabbit retinal ganglion cells. Visual Neuroscience 16, 285290.Google Scholar
Thibos, L.N. & Werblin, F.S. (1978). The properties of surround antagonism elicited by spinning windmill patterns in the mudpuppy retina. Journal of Physiology (London) 278, 101116.CrossRefGoogle Scholar
Tian, N., Hwang, T.N. & Copenhagen, D.R. (1998). Analysis of excitatory and inhibitory spontaneous synaptic activity in mouse retinal ganglion cells. Journal of Neurophysiology 80, 13271340.CrossRefGoogle Scholar
Veruki, M.L. & Hartveit, E. (2002a). AII (Rod) amacrine cells form a network of electrically coupled interneurons in the mammalian retina. Neuron 33, 935946.Google Scholar
Veruki, M.L. & Hartveit, E. (2002b). Electrical synapses mediate signal transmission in the rod pathway of the mammalian retina. Journal of Neuroscience 22, 1055810566.Google Scholar
Volgyi, B., Xin, D. & Bloomfields, S.A. (2002). Feedback inhibition in the inner plexiform layer underlies the surround-mediated responses of AII amacrine cells in the mammalian retina. Journal of Physiology 539, 603614.CrossRefGoogle Scholar
Wassle, H. (2004). Parallel processing in the mammalian retina. Nature Review Neuroscience 5, 747757.CrossRefGoogle Scholar
Werblin, F.S. (1972). Lateral interactions at inner plexiform layer of vertebrate retina: Antagonistic responses to change. Science 175, 10081010.CrossRefGoogle Scholar
Werblin, F.S. & Dowling, J.E. (1969). Organization of the retina of the mudpuppy, Necturus maculosus. II. Intracellar recording. Journal of Neurophysiology 32, 339355.Google Scholar
Wunk, D.F. & Werblin, F.S. (1979). Synaptic inputs to the ganglion cells in the tiger salamander retina. Journal of General Physiology 73, 265286.CrossRef
Yang, C.Y., Lukasiewicz, P., Maguire, G., Werblin, F.S. & Yazulla, S. (1991). Amacrine cells in the tiger salamander retina: morphology, physiology, and neurotransmitter identification. Journal of Comparative Neurology 312, 1932.CrossRefGoogle Scholar