Different Circuits for ON and OFF Retinal Ganglion Cells Cause Different Contrast Sensitivities

The theory of "parallel pathways" predicts that, except for a sign reversal, ON and OFF ganglion cells are driven by a similar presynaptic circuit. To test this hypothesis, we measured synaptic inputs to ON and OFF cells as reflected in the subthreshold membrane potential. We made intracel...

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Bibliographic Details
Published in:The Journal of neuroscience 2003-04, Vol.23 (7), p.2645-2654
Main Authors: Zaghloul, Kareem A, Boahen, Kwabena, Demb, Jonathan B
Format: Article
Language:English
Subjects:
Action Potentials
Afferent Pathways
Aminobutyrates - pharmacology
Animals
Contrast Sensitivity
Culture Techniques
Glutamic Acid - metabolism
Guinea Pigs
Kinetics
Membrane Potentials
Models, Neurological
Neural Inhibition
Photic Stimulation
Retinal Cone Photoreceptor Cells - physiology
Retinal Ganglion Cells - cytology
Retinal Ganglion Cells - drug effects
Retinal Ganglion Cells - physiology
Synaptic Transmission
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Summary:The theory of "parallel pathways" predicts that, except for a sign reversal, ON and OFF ganglion cells are driven by a similar presynaptic circuit. To test this hypothesis, we measured synaptic inputs to ON and OFF cells as reflected in the subthreshold membrane potential. We made intracellular recordings from brisk-transient (Y) cells in the in vitro guinea pig retina and show that ON and OFF cells in fact express significant asymmetries in their synaptic inputs. An ON cell receives relatively linear input that modulates a single excitatory conductance; whereas an OFF cell receives rectified input that modulates both inhibitory and excitatory conductances. The ON pathway, blocked by L-AP-4, tonically inhibits an OFF cell at mean luminance and phasically inhibits an OFF cell during a light increment. Our results suggest that basal glutamate release is high at ON but not OFF bipolar terminals, and inhibition between pathways is unidirectional: ON --> OFF. These circuit asymmetries explain asymmetric contrast sensitivity observed in spiking behavior.
ISSN:0270-6474
1529-2401
DOI:10.1523/jneurosci.23-07-02645.2003