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Physiological response properties of displaced amacrine cells of the adult ferret retina

Published online by Cambridge University Press:  23 June 2004

SALLY W. ABOELELA
Affiliation:
Oregon Health & Science University, Department of Physiology and Pharmacology L334, Portland
DAVID W. ROBINSON
Affiliation:
Center for Research on Occupational and Environmental Toxicology, L606, Portland

Abstract

The ganglion cell layer (GCL) of the mammalian retina contains a large number of neurons called displaced amacrine cells (DACs) that do not project to the optic nerve. However, with the exception of the rabbit starburst amacrine cell little is known regarding the function of this large population due to the difficulty experienced in making physiological recordings from these neurons. We have overcome these difficulties and have used whole-cell patch-clamp techniques to examine the intrinsic membrane properties of DACs in the ferret retina. Our results indicate a large degree of diversity in their intrinsic membrane properties. In response to maintained depolarizing current injection, DACs responded with graded depolarization or by eliciting either transient or sustained bursts of spiking activity. At the resting membrane potential, 10% of the DACs generated spontaneous spikes in either an apparently random manner or at the peak of intrinsic waves of depolarization. The resting membrane activity of the remaining DACs recorded could be classified into three groups that were quiescent (28%), had robust uncorrelated synaptic activity (30%), or underwent slow waves of depolarization (42%). Diversity was also revealed in the membrane currents recorded in voltage-clamp where some DACs were quiescent (19%), or exhibited robust nonrhythmic synaptic events (42%). The remaining DACs exhibited waves of oscillatory activity (39%), characterized by either rhythmic bursts of synaptic events (17%) or slow inward currents (22%). Bath application of 50 μM biccuculine or 150 μM picrotoxin had no effect on the waves of activity, however, the gap junction blocker, carbenoxolone (100 μm), blocked both oscillatory patterns. By including Lucifer yellow and biocytin in the recording pipette, it was possible to determine the morphology of recorded neurons and group them based on dendritic extent as small-, medium-, or large-field DACs. There were few relationships between these morphologically defined groups and their intrinsic membrane properties. The present study provides the first in-depth examination of the intrinsic membrane properties of DACs in the ferret retina and provides new insights into the potential roles these neurons play in the processing of visual information in the mammalian retina.

Type
Research Article
Copyright
2004 Cambridge University Press

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References

REFERENCES

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. (1996). Effect of spike blockade on the receptive-field size of amacrine and ganglion cells in the rabbit retina. Journal of Neurophysiology 75, 18781893.CrossRefGoogle Scholar
Bloomfield, S.A., Xin, D., & Osborne, T. (1997). Light-induced modulation of coupling between AII amacrine cells in the rabbit retina. Visual Neuroscience 14, 565576.CrossRefGoogle Scholar
Daw, N.W., Jensen, R.J., & Brunken, W.J. (1990). Rod pathways in mammalian retinae. Trends in Neurosciences 13, 110115.CrossRefGoogle Scholar
Ellias, S.A. & Stevens, J.K. (1980). The dendritic varicosity: A mechanism for electrically isolating the dendrites of cat retinal amacrine cells? Brain Research 196, 365372.Google Scholar
Famiglietti, E.V., Jr. (1983a). ‘Starburst’ amacrine cells and cholinergic neurons: Mirror-symmetric on and off amacrine cells of rabbit retina. Brain Research 261, 138144.Google Scholar
Famiglietti, E.V., Jr. (1983b). On and off pathways through amacrine cells in mammalian retina: The synaptic connections of “starburst” amacrine cells. Vision Research 23, 12651279.Google Scholar
Famiglietti, E.V. (1992). Dendritic co-stratification of ON and ON-OFF directionally selective ganglion cells with starburst amacrine cells in rabbit retina. Journal of Comparative Neurology 324, 322335.CrossRefGoogle Scholar
Hampson, E.C., Vaney, D.I., & Weiler, R. (1992). Dopaminergic modulation of gap junction permeability between amacrine cells in mammalian retina. Journal of Neuroscience 12, 49114922.Google Scholar
Hartveit, E. (1999). Reciprocal synaptic interactions between rod bipolar cells and amacrine cells in the rat retina. Journal of Neurophysiology 81, 29232936.CrossRefGoogle Scholar
Hayden, S.A., Mills, J.W., & Masland, R.M. (1980). Acetylcholine synthesis by displaced amacrine cells. Science 210, 435437.CrossRefGoogle Scholar
Hughes, A. & Vaney, D.I. (1980). Coronate cells: Displaced amacrines of the rabbit retina? Journal of Comparative Neurology 189, 169189.Google Scholar
Hughes, A. & Wieniawa-Narkiewicz, E. (1980). A newly identified population of presumptive microneurones in the cat retinal ganglion cell layer. Nature 284, 468470.CrossRefGoogle Scholar
Kolb, H., Nelson, R., & Mariani, A. (1981). Amacrine cells, bipolar cells and ganglion cells of the cat retina: A Golgi study. Vision Research 21, 10811114.CrossRefGoogle Scholar
MacNeil, M.A., Heussy, J.K., Dacheux, R.F., Raviola, E., & Masland, R.H. (1999). The shapes and numbers of amacrine cells: Matching of photofilled with Golgi-stained cells in the rabbit retina and comparison with other mammalian species. Journal of Comparative Neurology 413, 305326.3.0.CO;2-E>CrossRefGoogle Scholar
Masland, R.H. (1988). Amacrine cells. Trends in Neurosciences 11, 405410.CrossRefGoogle Scholar
McBain, C.J. & Fisahn, A. (2001). Interneurons unbound. Nature Reviews Neuroscience 2, 1123.CrossRefGoogle Scholar
Meister, M., Wong, R.O., Baylor, D.A., & Shatz, C.J. (1991). Synchronous bursts of action potentials in ganglion cells of the developing mammalian retina. Science 252, 939943.CrossRefGoogle Scholar
Menger, N. & Wassle, H. (2000). Morphological and physiological properties of the A17 amacrine cell of the rat retina. Visual Neuroscience 17(5), 769780.CrossRefGoogle Scholar
Miller, R.F. & Bloomfield, S.A. (1983). Electroanatomy of a unique amacrine cell in the rabbit retina. Proceedings of the National Academy of Sciences of the U.S.A. 80, 30693073.CrossRefGoogle Scholar
Nelson, R. & Kolb, H. (1985). A17: A broad-field amacrine cell in the rod system of the cat retina. Journal of Neurophysiology 54, 592614.CrossRefGoogle Scholar
Perry, V.H. (1981). Evidence for an amacrine cell system in the ganglion cell layer of the rat retina. Neuroscience 6, 931944.CrossRefGoogle Scholar
Pourcho, R.G. (1982). Dopaminergic amacrine cells in the cat retina. Brain Research 252, 101109.CrossRefGoogle Scholar
Shields, C.R., Tran, M.N., Wong, R.O., & Lukasiewicz, P.D. (2000). Distinct ionotropic GABA receptors mediate presynaptic and postsynaptic inhibition in retinal bipolar cells. Journal of Neuroscience 20, 26732682.Google Scholar
Skinner, F.K., Zhang, L., Velazquez, J.L., & Carlen, P.L. (1999). Bursting in inhibitory interneuronal networks: A role for gap-junctional coupling. Journal of Neurophysiology 81, 12741283.CrossRefGoogle Scholar
Strettoi, E., Raviola, E., & Dacheux, R.F. (1992). Synaptic connections of the narrow-field, bistratified rod amacrine cell (AII) in the rabbit retina. Journal of Comparative Neurology 325, 152168.CrossRefGoogle Scholar
Taylor, W.R. (1996). Response properties of long-range axon-bearing amacrine cells in the dark-adapted rabbit retina. Visual Neuroscience 13(4), 599604.CrossRefGoogle Scholar
Taylor, W.R. & Vaney, D.I. (2002). Diverse synaptic mechanisms generate direction selectivity in the rabbit retina. Journal of Neuroscience 22, 77127720.Google Scholar
Traub, R.D., Kopell, N., Bibbig, A., Buhl, E.H., LeBeau, F.E., & Whittington, M.A. (2001). Gap junctions between interneuron dendrites can enhance synchrony of gamma oscillations in distributed networks. Journal of Neuroscience 21, 94789486.Google Scholar
Vaney, D.I. (1984). ‘Coronate’ amacrine cells in the rabbit retina have the ‘starburst’ dendritic morphology. Proceedings of the Royal Society B (London) 220, 501508.CrossRefGoogle Scholar
Vaney, D.I., Peichi, L., & Boycott, B.B. (1981). Matching populations of amacrine cells in the inner nuclear and ganglion cell layers of the rabbit retina. Journal of Comparative Neurology 199, 373391.CrossRefGoogle Scholar
Vaney, D.I. & Taylor, W.R. (2002). Direction selectivity in the retina. Current Opinions in Neurobiology 12(4), 405410.CrossRefGoogle Scholar
Vaney, D.I., Young, H.M., & Gynther, I.C. (1991). The rod circuit in the rabbit retina. Visual Neuroscience 7, 141154.CrossRefGoogle Scholar
Volgyi, B., Xin, D., Amarillo, Y., & Bloomfield, S.A. (2001). Morphology and physiology of the polyaxonal amacrine cells in the rabbit retina. Journal of Comparative Neurology 440(1), 109125.CrossRefGoogle Scholar
Wassle, H., Chun, M.H., & Muller, F. (1987). Amacrine cells in the ganglion cell layer of the cat retina. Journal of Comparative Neurology 265, 391408.CrossRefGoogle Scholar
Wingate, R.J.T., Fitzgibbon, T., Thompson, I.D. (1992). Lucifer Yellow, Retrograde Tracers, and Fractal Analysis Characterise Adult Ferret Retinal Ganglion Cells. Journal of Comparative Neurology 323, 449474.CrossRefGoogle Scholar
Wong, R.O. (1999). Retinal waves and visual system development. Annual Review of Neuroscience 22, 2947.CrossRefGoogle Scholar
Wong, R.O. & Hughes, A. (1987). The morphology, number, and distribution of a large population of confirmed displaced amacrine cells in the adult cat retina. Journal of Comparative Neurology 255, 159177.CrossRefGoogle Scholar
Wong, R.O. & Oakley, D.M. (1996). Changing patterns of spontaneous bursting activity of on and off retinal ganglion cells during development. Neuron 16, 10871095.CrossRefGoogle Scholar
Wong, R.O., Chernjavsky, A., Smith, S.J., & Shatz, C.J. (1995). Early functional neural networks in the developing retina. Nature 374, 716718.CrossRefGoogle Scholar
Wong, W.T., Myhr, K.L., Miller, E.D., & Wong, R.O. (2000). Developmental changes in the neurotransmitter regulation of correlated spontaneous retinal activity. Journal of Neuroscience 20, 351360.Google Scholar
Zhang, Y., Perez Velazquez, J.L., Tian, G.F., Wu, C.P., Skinner, F.K., Carlen, P.L., & Zhang, L. (1998). Slow oscillations (≤1 Hz) mediated by GABAergic interneuronal networks in rat hippocampus. Journal of Neuroscience 18, 92569268.Google Scholar
Zhou, Z.J. (1998). Direct participation of starburst amacrine cells in spontaneous rhythmic activities in the developing mammalian retina. Journal of Neuroscience 18, 41554165.Google Scholar