Mouse photoreceptors are electrically coupled via gap junctions, but the relative importance of rod/rod, cone/cone, or rod/cone coupling is unknown. Furthermore, while connexin36 (Cx36) is expressed by cones, the identity of the rod connexin has been controversial. We report that FACS-sorted rods and cones both express Cx36 but no other connexins. We created rod- and cone-specific Cx36 knockout mice to dissect the photoreceptor network. In the wild type, Cx36 plaques at rod/cone contacts accounted for more than 95% of photoreceptor labeling and paired recordings showed the transjunctional conductance between rods and cones was ~300 pS. When Cx36 was eliminated on one side of the gap junction, in either conditional knockout, Cx36 labeling and rod/cone coupling were almost abolished. We could not detect direct rod/rod coupling, and cone/cone coupling was minor. Rod/cone coupling is so prevalent that indirect rod/cone/rod coupling via the network may account for previous reports of rod coupling.

Mammalian retinas contain about 20 types of ganglion cells that respond to different aspects of the visual scene, including the direction of motion of objects in the visual field. The rabbit retina has long been thought to contain two distinct types of directionally selective (DS) ganglion cell: a bistratified ON-OFF DS ganglion cell that responds to onset and termination of light, and an ON DS ganglion cell, which stratifies only in the ON layer and responds only to light onset. This division is challenged by targeted recordings from rabbit retina, which indicate that ON DS ganglion cells occur in two discriminably different types. One of these is strongly tracer-coupled to amacrine cells; the other is never tracer-coupled. These two types also differ in branching pattern, stratification depth, relative latency, and transience of spiking. The sustained, uncoupled ON DS cell ramifies completely within the lower cholinergic band and responds to nicotine with continuous firing. In contrast, the transient, coupled ON DS ganglion cell stratifies above the cholinergic band and is not positioned to receive major input from cholinergic amacrine cells, consistent with its modest response to the cholinergic agonist nicotine. Much data have accrued that directional responses in the mammalian retina originate via gamma-aminobutyric acid (GABA) release from the dendrites of starburst amacrine cells (Euler et al., 2002). If there is an ON DS ganglion cell that does not stratify in the starburst band, this suggests that its GABA-dependent directional signals may be generated by a mechanism independent of starburst amacrine cells.

In mammalian retinae, the first steps in the process of discrimination of color are mediated by color-opponent neurons that respond with opposite polarity to signals from short (S, blue) and longer wavelength (M, green or L, red) cones. Primates also contain a second system that is different from M and L cones. Although pathways responding to the onset of S-cone stimulation (S-ON) are well known, the existence of bipolar cells and retinal ganglion cells that respond to the offset of S-cone stimulation (S-OFF) has been controversial. We have recorded from and stained three different types of S/M color-opponent ganglion cells in the rabbit retina that are distinguished by the polarity of their responses to S-cone stimulation, the stratification pattern of their dendrites, and the distinct mechanisms underlying their color-opponent responses. We describe an S-ON and an S-OFF pathway formed by amacrine cells inverting the S-ON signal. Most importantly, we also provide both anatomical and physiological evidence for a direct S-OFF pathway dependent on an S-OFF cone bipolar cell. The results indicate a greater diversity of pathways for processing of signals from S-cones than previously suspected.

Neural networks have been shown to support the generation of more than one behavioral motor act. In the nudibranch mollusk Hermissenda, Pavlovian conditioning results in light, the conditioned stimulus (CS), evoking both inhibition of locomotion and foot contraction. The synaptic organization of the eyes and optic ganglion is well documented; however, the characterization of the neural network mediating visually modulated behaviors is incomplete. We have now characterized synaptic connections between identified photoreceptors and a newly identified interneuron (II(b)), identified synaptic projections from type I and type II interneurons to an inhibitory interneuron (III(i)) and to two newly identified pedal neurons, VP1 and VP2. Here we show that VP1 activates ciliary movement on the anterior foot and VP2 innervates the anterior foot and ventral tentacle. Stimulation of the photoreceptors with light produced two effects on the activity of VP1 and VP2. First, light inhibits type I(i) and II(i) interneurons and disinhibits VP1 and VP2. Depolarization of type II(e) interneurons also disinhibits VP1 and VP2. Second, the light-elicited depolarization and increased tonic activity of VP1 and VP2 is produced by excitatory synaptic input from ipsilateral and contralateral type II(b) interneurons. Pedal neurons VP1 and VP2 receive similar synaptic input from type I, II, and III(i) interneurons; this is in agreement with previous research showing that the visual pathway influences both ciliary locomotion and foot movement. The organization of the visual system in Hermissenda provides for the expression of cellular and synaptic plasticity supporting learning without altering the networks ability to carry out the requirements for normal visual processing.