Widespread inhibition proportional to excitation controls the gain of a leech behavioral circuit

Abstract

Changing gain in a neuronal system has important functional consequences, but the underlying mechanisms have been elusive. Models have suggested a variety of neuronal and systems properties to accomplish gain control. Here, we show that the gain of the neuronal network underlying local bending behavior in leeches depends on widespread inhibition. Using behavioral analysis, intracellular recordings, and voltage-sensitive dye imaging, we compared the effects of blocking just the known lateral inhibition with blocking all GABAergic inhibition. This revealed an additional source of inhibition, which was widespread and increased in proportion to increasing stimulus intensity. In a model of the input/output functions of the three-layered local bending network, we showed that inhibiting all interneurons in proportion to the stimulus strength produces the experimentally observed change in gain. This relatively simple mechanism for controlling behavioral gain could be prevalent in vertebrate as well as invertebrate nervous systems.