Quantitative analysis of a directed behavior in the medicinal leech: implications for organizing motor output

The local bend is a directed behavior produced by the leech, Hirudo medicinalis, in response to a light touch. Contraction of longitudinal muscles near the touched location results in a bend directed away from the stimulus. We quantify the relationship between the location of touch around the body perimeter and the behavioral output by using video analysis, muscle tension measurements, and electromyography. On average, the direction of the behavioral output differed from the touch location by <8% of the total body perimeter. We discuss our results in the context of two contrasting behavioral strategies: a Continuous strategy, in which the local bend is directed exactly opposite to stimulus location, and a Categorical strategy, in which there are four distinct bend directions, each elicited by stimuli given in a single quadrant of the body perimeter. To distinguish between these strategies, we delivered two competing stimuli simultaneously. The resulting behavioral output is best described by an average of the effects of each stimulus given alone and thus provides support for the Continuous strategy. We also use a simple model, based on anatomical and physiological data, to predict the responses of the known motor neurons to different stimulus locations. The model shows that the activation of two of the motor neurons (D and V) is inconsistent with a Categorical strategy. However, these neurons are known to be active during the local bend behavior. This result, along with our experimental observations, suggests that the local bend network uses a Continuous strategy to encode stimulus location and produce directed behavioral output.