Serotonergic/cholinergic muscle receptor cells in the crab stomatogastric nervous system. I. Identification and characterization of the gastropyloric receptor cells.

1. Serotonin (5-hydroxytryptamine) immunohistochemistry was used to locate and anatomically describe a set of four muscle receptor cells in the stomatogastric nervous system of the crabs Cancer borealis and Cancer irroratus. We found that these sensory cells, which we named gastropyloric receptor (GPR) cells, are the sole source of serotonergic inputs to the stomatogastric ganglion (STG) in these species. Thus any endogenous serotonergic modulation of the central pattern generators (CPGs) in the STG must be afferent and not descending from other ganglia. 2. There are two bilateral pairs of GPR cells. Each pair consists of two cell types (GPR1 and GPR2) based on differences in muscle innervation and physiological response characteristics. GPR2 responds in a mostly tonic fashion to increases in muscle tension caused by passive stretch or motor neuron-evoked contraction, whereas GPR1 responds more phasically and adapts more rapidly. Both GPR cell types project to the midline STG and terminate in each of the bilaterally paired commissural ganglia (COGs). 3. The GPR cells have sensory endings unlike any described for other muscle receptor cells: the terminals enter invaginations of the muscle surface and end near the z-bands of the muscle. These novel structures may be involved in the sensory transduction process. 4. The GPR cells may contain acetylcholine in addition to serotonin, as indicated by the presence of choline acetyltransferase (ChAT) in GPR2 (Table 1) and probably GPR1 as well. 5. The GPR cells have no direct effect on muscle properties or neuromuscular transmission: excitatory junctional potential (EJP) amplitude and motor neuron-evoked tension are unaffected by GPR stimulation. However, very low concentrations of exogenously applied serotonin do cause an increase in motor neuron-evoked muscle tension, probably reflecting a hormonal action of the amine. 6. The activity of GPR2 was monitored in a semi-intact preparation. GPR2 is active in phase with normal movements of the gastric mill. GPR2 is also capable of endogenous rhythmic activity. This indicates that even in the absence of mechanical stimulation, the GPR cells may still provide patterned input to the CPGs in the STG. 7. The GPR cells are proprioceptive cells that use serotonin and acetylcholine as cotransmitters. It is important to characterize these cells to understand the role of serotonergic modulation in the production of motor programs by stomatogastric CPGs.