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The Journal of Neuroscience, April 16, 2008, 28(16):4136-4150; doi:10.1523/JNEUROSCI.4274-07.2008

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Behavioral/Systems/Cognitive
Disinhibition Combines with Excitation to Extend the Operating Range of the OFF Visual Pathway in Daylight

Michael B. Manookin,¹ Deborah Langrill Beaudoin,² Zachary Raymond Ernst,² Leigh J. Flagel,² and Jonathan B. Demb^1,2,3

¹Neuroscience Program and Departments of ²Ophthalmology and Visual Sciences and ³Molecular, Cellular, and Developmental Biology, University of Michigan, Ann Arbor, Michigan 48105

Correspondence should be addressed to Dr. Jonathan B. Demb, Kellogg Eye Center, University of Michigan, 1000 Wall Street, Ann Arbor, MI 48105. Email: jdemb{at}umich.edu

Cone signals divide into parallel ON and OFF bipolar cell pathways, which respond to objects brighter or darker than the background and release glutamate onto the corresponding type of ganglion cell. It is assumed that ganglion cell excitatory responses are driven by these bipolar cell synapses. Here, we report an additional mechanism: OFF ganglion cells were driven in part by the removal of synaptic inhibition (disinhibition). The disinhibition played a relatively large role in driving responses at low contrasts. The disinhibition persisted in the presence of CNQX and D-AP-5. Furthermore, the CNQX/D-AP-5-resistant response was blocked by L-AP-4, meclofenamic acid, quinine, or strychnine but not by bicuculline. Thus, the disinhibition circuit was driven by the ON pathway and required gap junctions and glycine receptors but not ionotropic glutamate or GABA_A receptors. These properties implicate the AII amacrine cell, better known for its role in rod vision, as a critical circuit element through the following pathway: cone ON cone bipolar cell AII cell OFF ganglion cell. Rods could also drive this circuit through their gap junctions with cones. Thus, to light decrement, AII cells, driven by electrical synapses with ON cone bipolar cells, would hyperpolarize and reduce glycine release to excite OFF ganglion cells. To light increment, the AII circuit would directly inhibit OFF ganglion cells. These results show a new role for disinhibition in the retina and suggest a new role for the AII amacrine cell in daylight vision.

Key words: A2 amacrine cell; circuitry; whole-cell recording; patch clamp; retinal; Y-cell

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Received Sept. 18, 2007; revised Jan. 30, 2008; accepted March 6, 2008.

Correspondence should be addressed to Dr. Jonathan B. Demb, Kellogg Eye Center, University of Michigan, 1000 Wall Street, Ann Arbor, MI 48105. Email: jdemb{at}umich.edu

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