Gain control of synaptic transfer from second- to third-order neurons of cockroach ocelli

Abstract

Synaptic transmission from second- to third-order neurons of cockroach ocelli occurs in an exponentially rising part of the overall sigmoidal characteristic curve relating pre- and postsynaptic voltage. Because of the nonlinear nature of the synapse, linear responses of second-order neurons to changes in light intensity are half-wave rectified, i.e., the response to a decrement in light is amplified whereas that to an increment in light is compressed. Here I report that the gain of synaptic transmission from second- to third-order neurons changes by ambient light levels and by wind stimulation applied to the cerci. Transfer characteristics of the synapse were studied by simultaneous intracellular recordings of second- and third-order neurons by a sinusoidally modulated light with various mean liminances. With a decrease in the mean luminance (a) the mean membrane potential of second-order neurons was depolarized. (b) the synapse between the second- and third-order neurons operated in a steeper range of the exponential characteristic curve, where the gain to transmit modulatory signals was higher, and (c) the gain of third-order neurons to detect a decrement in light increased. Second-order neurons were depolarized when a wind or tactile stimulus was applied to various parts of the body including the cerci. During a wind-evoked depolarization, the synapse operated in a steeper range of the characteristic curve, which resulted in an increased gain of third-order neurons to detect light decrements. I conclude that the nonlinear nature of the synapse between the second- and third-order neurons provides an opportunity for an adjustment of gain to transmit signals of intensity change. The possibility that a similar gain control occurs in other visual systems and underlies a more advanced visual function, i.e., detection of motion, is discussed.