Nonlinear interneuronal properties underlie integrative flexibility in a lobster disynaptic sensorimotor pathway.

1. In the lobster Homarus, a single mechanoreceptor neuron (anterior gastric receptor, AGR) associated with muscle gm 1 of the gastric medial tooth has access to motoneurons (GM) innervating this muscle via an excitatory synaptic pathway involving two bilateral interneurons (commissural gastric, CG) (see 31). 2. Studies on in vitro preparations of the stomatogastric nervous system show that despite its apparent simplicity, this disynaptic pathway can express considerable flexibility in information processing, as evident by a wide variety of GM output responses to sensory input from AGR (Fig. 1). 3. This input/output flexibility does not rely on multiple synaptic pathways operating in parallel with the interneuron CG, since it is demonstrated that AGR has access to GM only via CG (Fig. 2). 4. Short AGR impulse trains at different spike frequencies can give rise to similarly brief excitation of GM, or prolonged motoneuron responses. Moreover, graded increases in AGR discharge frequency can lead to a sudden increase in the intensity of GM responsiveness that otherwise grades linearly with receptor firing. Such step changes in gain (both in duration and magnitude) are due to synaptic triggering of regenerative "plateau" depolarizations in CG (Figs. 3 and 4). 5. Sustained tonic discharge in AGR can induce cyclic bursting activity in previously nonrhythmic GM neurons. Furthermore, the frequency of motoneuron bursts increases with the frequency of AGR tonic firing. Such changes in pattern are ascribed to synaptic triggering and modification of regenerative "oscillatory" depolarizations in CG (Fig. 5). 6. Higher levels of AGR firing can result either in strong activation of GM motoneurons or in complete inactivation of GM. This switch in sign of the motor response is dependent on base-line levels of activity in the receptor and is due to the capability of CG to fire action potentials only within a window of membrane potential (Figs. 6-8). The functional outcome of this cellular property of CG is that positive feedback from AGR to GM can be switched to negative feedback via the same excitatory synaptic pathway (Fig. 9). 7. We conclude that flexibility in sensorimotor integration can be an inbuilt feature even of hard-wired neuronal pathways; in the present case, changes in input/output relationships reside with intrinsic properties of an intercalated interneuron (Fig. 10).