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 (

The distinctive red-green dimension of human and nonhuman primate color perception arose relatively recently in the primate lineage with the appearance of separate long (L) and middle (M) wavelength-sensitive cone photoreceptor types. "Midget" ganglion cells of the retina use center-surround receptive field structure to combine L and M cone signals antagonistically and thereby establish a "redgreen, color-opponent" visual pathway. However, the synaptic origin of red-green opponency is unknown, and conflicting evidence for either random or L versus M cone-selective inhibitory circuits has divergent implications for the developmental and evolutionary origins of trichromatic color vision. Here we directly measure the synaptic conductances evoked by selective L or M cone stimulation in the midget ganglion cell dendritic tree and show that L versus M cone opponency arises presynaptic to the midget cell and is transmitted entirely by modulation of an excitatory conductance. L and M cone synaptic inhibition is feedforward and thus occurs in phase with excitation for both cone types. Block of GABAergic and glycinergic receptors does not attenuate or modify L versus M cone antagonism, discounting both presynaptic and postsynaptic inhibition as sources of cone opponency. In sharp contrast, enrichment of retinal pHbuffering capacity, to attenuate negative feedback from horizontal cells that sum L and M cone inputs linearly and without selectivity, completely abolished both the midget cell surround and all chromatic opponency. Thus, red-green opponency appears to arise via outer retinal horizontal cell feedback that is not cone type selective without recourse to any inner retinal L versus M cone inhibitory pathways.

Visual neurons, from retina to cortex, adapt slowly to stimulus contrast. Following a switch from high to low contrast, a neuron rapidly decreases its responsiveness and recovers over 5-20 s. Cortical adaptation arises from an intrinsic cellular mechanism: a sodium-dependent potassium conductance that causes prolonged hyperpolarization. Spiking can drive this mechanism, raising the possibility that the same mechanism exists in retinal ganglion cells. We found that adaptation in ganglion cells corresponds to a slowly recovering afterhyperpolarization (AHP), but, unlike in cortical cells, this AHP is not primarily driven by an intrinsic cellular property: spiking was not sufficient to generate adaptation. Adaptation was strongest following spatial stimuli tuned to presynaptic bipolar cells rather than the ganglion cell; it was driven by a reduced excitatory conductance, and it persisted while blocking GABA and glycine receptors, K((Ca)) channels, or mGluRs. Thus, slow adaptation arises from reduced glutamate release from presynaptic (nonspiking) bipolar cells.

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Summary In the retina, it is not well understood how visual processing depends on AMPA- and NMDA-type glutamate receptors. Here, we investigated how these receptors contribute to contrast coding in identified guinea pig ganglion cell types, in vitro. NMDA-mediated responses were negligible in ON α cells but substantial in OFF α and δ cells. OFF δ cell NMDA receptors were composed of GluN2B subunits. Using a novel deconvolution method, we determined the individual contributions of AMPA, NMDA and inhibitory currents to light responses of each cell type. OFF α and δ cells used NMDA receptors for encoding either the full contrast range (α), including near-threshold responses, or only a high range (δ). However, contrast sensitivity depended substantially on NMDA receptors only in OFF α cells. NMDA receptors contribute to visual contrast coding in a cell-type specific manner. Certain cell types generate excitatory responses using primarily AMPA receptors or disinhibition.