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Temporal resolution and temporal transfer properties: Gabaergic and cholinergic mechanisms

Published online by Cambridge University Press:  20 December 2007

KONSTANTIN BEHREND ,
BORIS BENKNER  and
CARLOS MORA-FERRER
KONSTANTIN BEHREND
Affiliation:
Institute of Zoology III, Johannes Gutenberg University, Mainz, Germany
BORIS BENKNER
Affiliation:
Institute of Zoology III, Johannes Gutenberg University, Mainz, Germany
CARLOS MORA-FERRER
Affiliation:
Institute of Zoology III, Johannes Gutenberg University, Mainz, Germany
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Abstract

Temporal resolution is a basic property of the visual system and critically depends upon retinal temporal coding properties which are also of importance for directional coding. Whether the temporal coding properties for directional coding derive form inherent properties or critically depend upon the temporal coding mechanisms is unclear. Here, the influence of acetylcholine and GABA upon photopic temporal coding was investigated in goldfish, using flicker stimuli, in a behavioral and an electrophysiological (ERG) approach. The goldfish temporal resolution ability decreased from more than 90% correct choices at 20 Hz flicker frequency to about 65% at 45 Hz flicker frequency with a flicker fusion frequency of approximately 39 Hz. Blockade of GABAa-receptors reduced the flicker fusion frequency to about 23 Hz, not affecting temporal resolution below 20 Hz flicker frequency. Partial blockade of nicotinic acetylcholine receptors reduced the flicker fusion frequency slightly and lowered the temporal resolution ability in the 25–30 Hz range. Blockade of muscarinic acetylcholine receptors had a smaller effect than the partial blockade of nicotinic acetylcholine receptors. In ERG-recordings, blocking GABAa-receptors increased the a- and b-wave amplitude, induced a delay, an increase and a slow fall-off of the d-wave. Blocking GABAc-receptors had little effect. Blocking GABAa- or GABAa/c-receptors changed the temporal resolution, when expressed as a linear filter, from a 3rd degree filter with resonance to a low order low-pass filter with a low upper limit frequency. The temporal transfer properties were barely changed by blocking either nicotinic or muscarinic acteylcholine receptors, although ERG-components increased in amplitude to varying degrees. The behavioral and electrophysiological data indicate the important role of GABA for temporal processing but little involvement of the cholinergic system. It is proposed that the interaction of the GABAergic amacrine cell network and bipolar cells determines the gain of the retinal temporal coding in the upper frequency range.

Keywords

Temporal codingBehaviorERGGABAAcetylcholine
Type
Research Article
Information
Visual Neuroscience , Volume 24 , Issue 6 , November 2007 , pp. 787 - 797
Copyright
2007 Cambridge University Press

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References

REFERENCES

Ariel, M. & Adolph, A.R. (1985). Neurotransmitter inputs to directionally sensitive turtle retinal ganglion cells. Journal of Neurophysiology 54, 1123–1143.CrossRefGoogle Scholar
Ariel, M. & Daw, N.W. (1982). Pharmacological analysis of directionally sensitive rabbit retinal ganglion cells. Journal of Physiology 324, 161–185.CrossRefGoogle Scholar
Bonaventure, N., Jardon, B., Wioland, N., Yucel, H. & Rudolf, G. (1988). On cholinergic mechanisms in the optokinetic nystagmus of the frog: Antagonistic effects of muscarinic and nicotinic systems. Behavioral Brain Research 27, 59–71.CrossRefGoogle Scholar
Borg-Graham, L.J. (2001). The computation of directional selectivity in the retina occurs presynaptic to the ganglion cell. Nature Neuroscience 4, 176–183.CrossRefGoogle Scholar
Dong, C.J. & Werblin, F.S. (1994). Dopamine modulation of GABAC receptor function in an isolated retinal neuron. Journal of Neurophysiology 71, 1258–1260.CrossRefGoogle Scholar
Dong, C.J. & Werblin, F.S. (1998). Temporal contrast enhancement via GABAC feedback at bipolar terminals in the tiger salamander retina. Journal of Neurophysiology 79, 2171–2180.CrossRefGoogle Scholar
Du, J.L. & Yang, X.L. (2000). Subcellular localization and complements of GABA(A) and GABA(C) receptors on bullfrog retinal bipolar cells. Journal of Neurophysiology 84, 666–676.CrossRefGoogle Scholar
Grzywacz, N.M., Amthor, F.R. & Merwine, D K. (1998). Necessity of acetylcholine for retinal directionally selective responses to drifting gratings in rabbit. Journal of Physiology 512, 575–581.CrossRefGoogle Scholar
Hassenstein, B. & Reichardt, W. (1956). Reihenfolgen-Vorzeichenauswertung bei der Bewegungsperzeption des Rüsselkäfers Chlorophanus. Zeitschrift für Naturforschung, B 11, 513–524.Google Scholar
He, S. & Masland, R.H. (1997). Retinal direction selectivity after targeted laser ablation of starburst amacrine cells. Nature 389, 378–382.CrossRefGoogle Scholar
He, S. (2000). Searching for mechanisms of retinal direction selectivity. Keio Journal of Medicine 49, 159–161.CrossRefGoogle Scholar
Koulen, P., Brandstatter, J.H., Kroger, S., Enz, R., Bormann, J. & Wassle, H. (1997). Immunocytochemical localization of the GABA(C) receptor rho subunits in the cat, goldfish, and chicken retina. Journal of Comparative Neurology 380, 520–532.3.0.CO;2-3>CrossRefGoogle Scholar
Lukasiewicz, P.D. & Shields, C.R. (1998). Different combinations of GABAA and GABAC receptors confer distinct temporal properties to retinal synaptic responses. Journal of Neurophysiology 79, 3157–3167.CrossRefGoogle Scholar
Marc, R.E. & Liu, W. (2000). Fundamental GABAergic amacrine cell circuitries in the retina: Nested feedback, concatenated inhibition, and axosomatic synapses. Journal of Comparative Neurology 425, 560–582.3.0.CO;2-D>CrossRefGoogle Scholar
Mora-Ferrer, C. & Behrend, K. (2004a). Cholinergic and GABAergic effects on temporal transfer properties in goldfish examined with the ERG and behavioral experiments. In ARVO, Annual Meeting, Ft. Lauderdale, Florida.
Mora-Ferrer, C. & Behrend, K. (2004b). Dopaminergic modulation of photopic temporal transfer properties in goldfish retina investigated with the ERG. Vision Research 44, 2067–2081.Google Scholar
Mora-Ferrer, C. & Gangluff, V. (2000). D2-dopamine receptor blockade impairs motion detection in goldfish. Visual Neuroscience 17, 177–186.CrossRefGoogle Scholar
Mora-Ferrer, C., Albrecht, C., Benkner, B., Lux, M., Gruber, M. & Behrend, K. (2005a). Effects of Glutamate antagonists on goldfish temporal transfer properties measured with the ERG. Neuroforum Vol. XI.Google Scholar
Mora-Ferrer, C. & Gangluff, V. (2002). D2-dopamine receptor blockade modulates temporal resolution in goldfish. Visual Neuroscience 19, 807–815.CrossRefGoogle Scholar
Mora-Ferrer, C., Hausselt, S., Schmidt Hoffmann, R., Ebisch, B., Schick, S., Wollenberg, K., Schneider, C., Teege, P. & Jurgens, K. (2005b). Pharmacological properties of motion vision in goldfish measured with the optomotor response. Brain Research 1058, 17–29.Google Scholar
Negishi, K. & Drujan, B.D. (1978). Effects of catecholamines on the horizontal cell membrane potential in the fish retina. Sens Processes 2, 388–395.Google Scholar
Negishi, K. & Drujan, B.D. (1979a). Effects of catecholamines and related compounds on horizontal cells in the fish retina. Journal of Neuroscience Research 4, 311–334.Google Scholar
Negishi, K. & Drujan, B.D. (1979b). Effects of some amino acids on horizontal cells in the fish retina. Journal of Neuroscience Research 4, 351–363.Google Scholar
Negishi, K. & Drujan, B.D. (1979c). Similarities in effects of acetylcholine and dopamine on horizontal cells in the fish retina. Journal of Neuroscience Research 4, 335–349.Google Scholar
Negishi, K., Kato, S., Teranishi, T. & Laufer, M. (1978). An electrophysiological study on the cholinergic system in the carp retina. Brain Research 148, 85–93.CrossRefGoogle Scholar
Neumeyer, C. (1984). On spectral sensitivity in the goldfish. Evidence for neural interactions between different “cone mechanisms. Vision Research 24, 1223–1231.CrossRefGoogle Scholar
Neumeyer, C. (1986). Wavelength discrimination in goldfish. Journal of Comparative Physiology A 158, 203–213.CrossRefGoogle Scholar
Neumeyer, C., Wietsma, J.J. & Spekreijse, H. (1991). Separate processing of “color” and “brightness” in goldfish. Vision Research 31, 537–549.CrossRefGoogle Scholar
Pan, Z. & Slaughter, M. (1991). Control of retinal information coding by GABAB receptors. Journal of Neuroscience 11, 1810–1821.CrossRefGoogle Scholar
Schellart, N.A. & Spekreijse, H. (1972). Dynamic characteristics of retinal ganglion cell responses in goldfish. Journal of General Physiology 59, 1–21.CrossRefGoogle Scholar
Smith, R.D., Grzywacz, N.M. & Borg-Graham, L.J. (1996). Is the input to a GABAergic synapse the sole asymmetry in turtle's retinal directional selectivity? Visual Neuroscience 13, 423–439.Google Scholar
Spekreijse, H. & Norton, A.L. (1970). The dynamic characteristics of color-coded S-potentials. Journal of General Physiology 56, 1–15.CrossRefGoogle Scholar
Taylor, W.R. & Vaney, D.I. (2002). Diverse synaptic mechanisms generate direction selectivity in the rabbit retina. Journal of Neuroscience 22, 7712–7720.CrossRefGoogle Scholar
Taylor, W.R. & Vaney, D.I. (2003). New directions in retinal research. Trends in Neuroscience 26, 379–385.CrossRefGoogle Scholar
Watanabe, S. & Murakami, M. (1984). Synaptic mechanisms of directional selectivity in ganglion cells of frog retina as revealed by intracellular recordings. Japanese Journal of Physiology 34, 497–511.CrossRefGoogle Scholar
Watanabe, S., Koizumi, A., Matsunaga, S., Stocker, J.W. & Kaneko, A. (2000). GABA-Mediated inhibition between amacrine cells in the goldfish retina. Journal of Neurophysiology 84, 1826–1834.CrossRefGoogle Scholar
Weng, S., Sun, W. & He, S. (2005). Identification of ON-OFF direction-selective ganglion cells in the mouse retina. Journal of Physiology (London) 562, 915–923.CrossRefGoogle Scholar
Wietsma, J.J. & Spekreijse, H. (1991). Bicuculline produces reversible red-green color blindness in goldfish, as revealed by monocular behavioral testing. Vision Research 31, 2101–2107.CrossRefGoogle Scholar
Witkovsky, P., Gabriel, R., Haycock, J.W. & Meller, E. (2000). Influence of light and neural circuitry on tyrosine hydroxylase phosphorylation in the rat retina. Journal of Chemical Neuroanatomy 19, 105–116.CrossRefGoogle Scholar
Yang, X.L., Li, P., Lu, T., Shen, Y. & Han, M.H. (2001). Physiological and pharmacological characterization of glutamate and GABA receptors on carp retinal neurons. Progress in Brain Research 131, 277–293.CrossRefGoogle Scholar
Yazejian, B. & Fain, G.L. (1993). Whole-cell currents activated at nicotinic acetylcholine receptors on ganglion cells isolated from goldfish retina. Visual Neuroscience 10, 353–361.CrossRefGoogle Scholar
Zhang, J., Jung, C.S. & Slaughter, M.M. (1997). Serial inhibitory synapses in retina. Visual Neuroscience 14, 553–563.CrossRefGoogle Scholar