Light-evoked hyperpolarizing signals in rods and cones are transmitted to and processed by neurons in the rest of the retina through a complex, but highly organized network of electrical and chemical synapses. In the outer retina, photoreceptors are electrically coupled to one another, and rods and cones send output signals to second-order retinal cells, the horizontal cells (HCs) and bipolar cells (BCs), via chemical synapses. HCs make feedback synapses on cones, and send feedforward synaptic signals to BCs. BCs can be classified into two major types, the on-center (or depolarizing bipolar cells, DBCs) and the off-center (or hyperpolarizing bipolar cells, HBCs). Additionally, they can be further classified according to their relative rod/cone inputs, color opponency, axonal outputs and other parameters. BCs are the first neurons along the visual pathway that exhibit clear center-surround antagonistic receptive field (CSARF) organization, the basic code for spatial information processing in the visual system, and the synaptic circuitry underlying bipolar cell receptive fields will be discussed in this chapter.
Electrical synapses (coupling) between photoreceptors
Electrical coupling between photoreceptors was first discovered in the turtle retina by Baylor et al in 1971. Electron microscopic studies revealed that gap junctions exist between photoreceptors in many vertebrate species. In the primate retina, anatomical data have shown large gap junctions between cones and smaller junctions between rods and cones, suggesting that cone–cone coupling is stronger than rod–cone coupling. , In the turtle and ground squirrel retina, couplings are found between cones of the same spectral sensitivity and between rods; whereas in amphibians, rods are strongly coupled to each other, but cones are not. , Coupling between rods and cones has been observed in turtles, tiger salamander and mammals, but the coupling strength is weaker than that between cones (in turtles) and between rods (in tiger salamander). , Recent evidence has shown that gap junctions between photoreceptors are mediated by connexin 35/36 gap junction proteins ( Fig. 22.1 ) and double patch recordings have revealed detailed properties of electrical synapses between photoreceptors. For example, junctional conductance between salamander rods is linear, with an average value of 500 pS ( Fig. 22.2A ). In ground-squirrel, green–green cone pairs are coupled with an average conductance of 220 pS, whereas coupling is undetectable in blue–green cone pairs ( Fig. 22.2B ). In the monkey retina, coupling has been found between red-cones, between green-cones and between red- and green-cones ( Fig. 22.2C ).
Although most rods are weakly coupled with cones in the tiger salamander retina, a small fraction of rods (10–15%) are strongly coupled with adjacent cones. Voltage responses of these rods (named rod C s) to current injection into a next-neighbor cone are about three to four times larger than those of the other rods. Rod C s behave like hybrids of rods and cones, and one of their functions is to generate off overshoot responses in higher-order retinal neurons under light-adapted conditions.
Photoreceptor coupling decreases resolution (visual acuity) of the visual system by spatially averaging photoreceptor signals over some lateral distance in the retina. However, the advantage of this arrangement is that it improves the signal-to-noise ratio of the photoreceptor output when the retina is uniformly illuminated. This is especially important for the rods to detect dim images under dark-adapted conditions when the voltage noise is high. It can be shown mathematically, however, that photoreceptor coupling decreases the signal-to-noise ratio of the photoreceptor network if the number of illuminated photoreceptors is less than the square root of the number of photoreceptors that are effectively coupled ( Box 22.1 ).
If N photoreceptors are coupled and k photoreceptors are uniformly illuminated, then the average (sample) signal is S = kS 1 /N (where S 1 is the light-evoked signal in one photoreceptor and σ 1 is the noise, or the standard deviation of S 1 from the mean), and the average (sample) variance:
σ ² = var ( S ) = var ( ( 1 / N ) ( S 1 + S 2 + . . . ) ) = ( 1 / ( N 2 ) ) var ( S 1 + S 2 + . . . ) = ( 1 / ( N 2 ) ) ( σ 1 + σ 2 + . . . ) = ( ( σ 1 ) / N ) , and thus σ = ( ( σ 1 ) / ( √ N ) )
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