Electrophysiological basis for the spatial dependence of the inhibitory coupling in the Limulus retina

A technique for measuring, with total optical isolation, the inhibition between two individual receptor units in the Limulus lateral eye is described. The extracellular responses of pairs of units were recorded, using light piping microelectrodes. The inhibitory coupling between two units was found to be nonlinear and describable by a simple hyperbolic equation written in terms of saturation rate (S), half saturation (H), and threshold (ft). By plotting reciprocal frequencies, the data could be linearized and compared for different pairs of units. The magnitude of inhibition (in terms of S and H) was found to decrease monotonically as the anatomical distance between receptors increased. An electrical model of the inhibitory system was developed which accounts for many of the properties of the observed inhibitory interactions. Using the equations from the model and the experimental data, it is shown that the "electrical distances" (which are computed in terms of space constants lambda) of the inhibitory synapses from the impulse-generating region of the test unit are directly related to the anatomical distance between receptors. It is also shown that "synaptic strength" is relatively constant with separation. The electrical distances of the inhibitory synapses range from about 0.1lambda to 0.25lambda for adjacent units to greater than 0.5lambda for units seven to nine receptors away. It is concluded that the nonlinear character of the inhibitory coupling is attributable to synaptic effects, and that the decrease of inhibition with distance between receptors is caused primarily by an increase in the electrical distance of the inhibitory synapses from the test unit.