STRUCTURAL AND FUNCTIONAL-CHARACTERIZATION OF A MUSCLE TENDON PROPRIOCEPTOR IN LOBSTER

A morphological and electrophysiological study was made on a unique pr imary mechanosensory neuron, the anterior gastric receptor (AGR), prev iously shown to arise from powerstroke muscle gm1 of the gastric mill system in the lobster foregut. Ultrastructural analysis of horseradish peroxidase injected AGR demonstrated that its peripheral dendrites do not ramify in muscle but are confined strictly to the connective tiss ue/epidermal interface in the tendon of gm1. These terminals are rich in mitochondria and at their very endings are free of glial cell wrapp ing, suggesting that they are the site at which mechanotransduction oc curs. Extracellular axonal recordings from an in vitro neuromuscular p reparation consisting of the gm1 muscle still attached to the stomatog astric nervous system, revealed that AGR is activated by passive stret ch of gm1. The response to ramp stimuli displays dynamic and static co mponents, both of which increase with the amplitude of applied stretch , while the dynamic component is also velocity sensitive. AGR is also activated by muscle contraction here elicited either by application of exogenous acetylcholine, the excitatory neurotransmitter for gm1, or by electrical stimulation of the motoneurons (GM) themselves. Consiste nt with a receptor lying in-series with its muscle, therefore, the eff ective stimulus of AGR in vivo is probably an increase in tension exer ted on the tendon during active muscle contraction. In neuromuscular p reparations including the bilateral commissural ganglia, stretching gm 1 reflexly activates GM motoneurons at low stimulus strengths but lead s to an inactivation of GM motoneurons at high stimulus strengths. Thi s is consistent with earlier findings that both responses can be elici ted by direct electrical stimulation of AGR. The functional implicatio ns of AGR's anatomical relationship with muscle gm1, the receptor's re sponse properties, and its central effects on motor output to gm1 are discussed. Comparison is also drawn between this first reported exampl e of a true tendon receptor in invertebrates and muscle receptors of v ertebrates. (C) 1995 Wiley-Liss, Inc.