Organization of efferent peripheral synapses at mechanosensory neurons in spiders

The mechanosensory neurons of arachnids receive diverse synaptic inputs in the periphery. The function of most of these synapses, however, is unknown. We have carried out detailed electron microscopic investigations of the peripheral synapses at sensory neurons in the compound slit sense organ VS-3 of the spider Cupiennius salei. Based on the localization of discrete presynaptic vesicle populations, it is possible to discriminate at least four different synapse types, containing either: (1) small round, electron-lucent vesicles 32 nm in diameter; (2) large round, clear 42-nm vesicles; (3) a mixture of small and large clear, round vesicles, similar in size to those in Type 1 and Type 2 synapses, respectively, and granular and dense-core vesicles; or (4) clear, round 37- to 65-nm vesicles. Combined immunocytochemical labeling at the light and the electron microscopic level suggests that gamma-aminobutyric acid (GABA) is the transmitter in many of the 32-nm vesicle synapses, and glutamate in many of the 42-nm ones. Based on vesicle type and particular synaptic configuration, various forms of presumed efferent synaptic contacts are distinguishable with the sensory neurons, the surrounding glia, and between the putative efferent fibers themselves. These include simple unidirectional synapses, reciprocal synapses, serial synapses, and convergent as well as divergent dyads. These various synaptic microcircuits are suited to serve a variety of functions. Among these are direct postsynaptic inhibition or excitation of the mechanosensory neurons, and disinhibition or sensitization via presynaptic inhibition or excitation. The observed synaptic configurations are compared with those at the crustacean muscle receptor organ. They reveal a remarkable complexity of synaptic microcircuits at spider sensilla and suggest manifold possibilities for subtle, efferent control of sensory activity.