Abstract
Purpose:
This study was designed to explore the dynamic interactions between rod and cone signaling pathways in primate retina. While previous studies have explored sensitivity of cellular components within the two pathways, little work has focused on exploring the dynamic interactions between these two, heavily-interconnected retinal circuitries.
Methods:
We recorded the neural response to both rod-preferring (i.e. blue flash) and cone-preferring (i.e. red flash) stimuli from neurons in the two pathways. A background illumination of ~20 Rh*/rod/s was present throughout the experiments unless otherwise stated.
Results:
On parasol retinal ganglion cells (RGCs) exhibited an asymmetric response to pairs of red and blue flashes: a red flash response was suppressed by a preceding blue flash but a blue flash was not suppressed by a preceding red flash. Before reaching On parasol RGCs, signals from rod and cone pathways are integrated in the axon terminals of the presynaptic On cone bipolar cells (CBCs). To determine the origin of the signaling asymmetry we recorded red and blue flash responses in On CBCs. Paired flashes did not produce the same asymmetries in the presynaptic neuron that were observed postsynaptically. Interestingly, red and blue flashes produced very different presynaptic voltage responses: blue flashes generated slow responses with larger overshoots (i.e. biphasic), red flashes produced faster responses, often without overshoots. We hypothesized that the On CBC’s overshoot (in voltage) in response to a blue flash suppresses the postsynaptic response to a subsequent red flash by pushing the presynpatic voltage to more negative values, making it harder for red flashes to trigger synaptic release. Indeed blue->red suppression could be overcome postsynaptically by increasing the strength of the red flash, a result not predicted by presynaptic depression.
Conclusions:
Rods and cones are specialized for dim and bright conditions, respectively, but many physiological conditions arise in which both photoreceptors are active. Here we show that the interconnected circuits upstream of RGCs have dynamic asymmetric interactions that occur at synaptic connections between On CBCs and On parasol RGCs. This interaction between pathways is a result of a fundamental difference between signals traversing the respective rod and cone driven-circuitries before converging at the axon terminals of the presynaptic On CBCs.
Keywords: 693 retinal connections, networks, circuitry •
532 gap junctions/coupling •
728 synapse