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 pe ripheral synapses at sensory neurons in the compound slit sense organ VS-3 of the spider Cupiennius salei. Based on the localization of discrete presy naptic vesicle populations, it is possible to discriminate at least. four d ifferent synapse types, containing either: (1) small round, electron-lucent vesicles 32 nm in diameter; (2) large round, clear 42-nm vesicles; (3) a m ixture of small and large clear, round vesicles, similar in size to those i n Type 1 and Type 2 synapses, respectively, and granular and dense-core ves icles; or (4) clear, round 37- to 65-nm vesicles. Combined immunocytochemic al labeling at the light and the electron microscopic level suggests that g amma-aminobutyric acid (GABA) is the transmitter in many of the 32-nm vesic le 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 surroun ding glia, and between the putative efferent fibers themselves. These inclu de simple unidirectional synapses, reciprocal synapses, serial synapses, an d convergent as well as divergent dyads. These various synaptic microcircui ts are suited to serve a variety of functions. Among these are direct posts ynaptic inhibition or excitation of the mechanosensory neurons, and disinhi bition or sensitization via presynaptic inhibition or excitation. The obser ved synaptic configurations are compared with those at the crustacean muscl e receptor organ. They reveal a remarkable complexity of synaptic microcirc uits at spider sensilla and suggest manifold possibilities for subtle, effe rent control of sensory activity. (C) 2000 Wiley-Liss, Inc.