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Slow light and dark adaptation of horizontal cells in the Xenopus retina: A role for endogenous dopamine

Published online by Cambridge University Press:  02 June 2009

Paul Witkovsky  and
Xiao-Ping Shi
Paul Witkovsky
Affiliation:
Daniel B. Kirby Eye Institute, Department of Ophthalmology, New York University Medical Center, New York Department of Physiology and Biophysics, New York University Medical Center
Xiao-Ping Shi
Affiliation:
Daniel B. Kirby Eye Institute, Department of Ophthalmology, New York University Medical Center, New York
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Abstract

A role for endogenous dopamine in the control of rod and contributions to a second-order retinal neuron, the horizontal cell (HC) was studied in the Xenopus retina. Relative rod and cone contributions were estimated from HC responses to scotopically balanced 491- and 650-nm flashes. In eyecups prepared in light then placed in darkness, cone input to the HC slowed and diminished on a time scale of hours. The decline in cone input was balanced by a slow growth of rod input to the HC. Administration of D-amphetamine, a dopamine releasing agent, restored the light-adapted waveform.

The kinetics of slow light adaptation were examined by recording HC responses from eyecups that had been dark-adapted previously for 11–14 h. When test flashes fell on a dark field, cone input to the HC grew for 2–4 h, reached a plateau, and later declined. If, however, flashes were superimposed on a weak background field, cone input to the HC continued to increase monotonically at about 10%/h. This increase was abolished by superfusion with a nonspecific dopamine receptor blocker, cis-flupenthixol (50 μM), resulting in the complete suppression of cone-to-horizontal cell synaptic transfer and the enhancement of rod-to-horizontal cell communication. Subcutaneous injection of reserpine, a drug that depletes dopamine stores (2 mg/kg on 1–4 successive days), or intraocular injection of the dopamine neurotoxin, 6-hydroxydopamine (10–30 μg) slowed and reduced the amplitude of cone input to the HC, even in completely light-adapted eyes. Subsequent treatment with D-amphetamine (5–50 μM) or dopamine (10 μM) partially restored the normal response.

Our experimental findings are consistent with the following hypothesis. Weak light is sufficient to stimulate dopamine release; dopamine augments cone-to-horizontal cell synaptic transfer and reduces rod-to-horizontal cell communication. The rapid kinetics of the fully light-adapted response depend on the presence of dopamine. Thus, dopamine appears to be an intraretinal signal for slow light adaptation.

Keywords

Light adaptationDark aptationDopamineHorizontal cellXenopus
Type
Research Article
Information
Visual Neuroscience , Volume 5 , Issue 4 , October 1990 , pp. 405 - 413
Copyright
Copyright © Cambridge University Press 1990

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