Peripheral Synapses at Identified Mechanosensory Neurons in Spiders: Three-Dimensional Reconstruction and GABA Immunocytochemistry

Abstract

The mechanosensory organs of arachnids receive diverse peripheral inputs. Little is known about the origin, distribution, and function of these chemical synapses, which we examined in lyriform slit sense organ VS-3 of the spider Cupiennius salei. The cuticular slits of this organ are each associated with two large bipolar mechanosensory neurons with different adaptation rates. With intracellular recording, we have now been able to correlate directly the staining intensity of a neuron for acetylcholinesterase with its adaptation rate, thus allowing us simply to stain a neuron to identify its functional type. All rapidly adapting neurons stain more heavily than slowly adapting neurons. Immunostaining of whole-mount preparations reveals GABA-like immunoreactive fibers forming numerous varicosities at the surface of all sensory neurons in VS-3; peripheral GABA-like immunoreactive somata are lacking. Sectioning the leg nerve procures rapid degeneration of most fiber profiles, confirming that the fibers are efferent. Punctate synapsin-like immunoreactivity colocalizes to these varicosities, although some synapsin-like immunoreactive puncta are GABA-immunonegative. Fibers with similar immunoreactivities are also associated with trichobothria, tactile hairs, internal joint receptors, i.e. other types of spider mechanosensory organs. In organ VS-3, immunoreactivity is most dense across the initial axon segment. The exact distribution of peripheral synapses was reconstructed from a 10-microm-long electron micrograph series of the dendritic, somatic, and initial axon regions of acetylcholinesterase-stained VS-3 neurons. These reveal a pattern similar to that of the synapsin-like immunoreactivity. Two different types of synapse were distinguished on the basis of their presynaptic vesicle populations. Many peripheral synapses thus appear to derive from efferent GABA-like immunoreactive fibers and probably provide centrifugal inhibitory control of primary mechanosensory activities.

Organization of efferent peripheral synapses at mechanosensory neurons in spiders

“…The peripheral synapses are formed by several fine fibers that make en passant contacts with the main peripheral segments of the sensory neurons (i.e., the dendrite, soma, and initial axon segment), as well as with each other and with glial processes (Fabian-Fine et al, 1999c). We found strong evidence that these fine fibers are of central origin (Fabian-Fine et al, 1999c), and are thus presumed to be efferent. We assume they are capable of exerting centrifugal control over the mechanosensory neurons in the same way that occurs at many receptors of different nervous systems (Livingston, 1959).…”

Activation of GABAA receptors modulates all stages of mechanoreception in spider mechanosensory neurons

“…Arachnids and crustaceans have networks of efferent synaptic contacts onto distal parts of mechanosensory neurons (Elekes and Florey 1987;Fabian-Fine et al 1999, 2002Torkkeli and Panek 2002), allowing modulation of afferent signals at the earliest stages. In vertebrates, peripheral modulation occurs at least in muscle spindles and auditory outer hair cells and may be a widespread phenomenon, as shown by the sympathetic sensitivity of some mechanoreceptors (Loewenstein 1956) and GABA effects in vagal mechanoreceptors (Page and Blackshaw 1999), Pacinian corpuscles (Pawson et al 2009), and cat primary afferent terminals (Carlton et al 1999).…”

Spider Peripheral Mechanosensory Neurons Are Directly Innervated and Modulated by Octopaminergic Efferents

“…However, peripheral synapses that use other transmitters have previously been identified in the spider mechanosensilla (Fabian-Fine et al, 1999b, making it possible that these colocations are only accidental.…”

“…In the tropical wandering spider Cupiennius salei, many of the efferent fibers are GABAergic (Fabian-Fine et al, 1999b), and the mechanosensory neurons are modulated by GABA acting on both ionotropic and metabotropic GABA receptors (Panek et al, 2002(Panek et al, , 2003. The large variety of synaptic contacts between the efferent fibers and sensory neurons, between the efferent fibers and glial cells, and between the efferent neurons themselves (Fabian-Fine et al, 2000) suggest that other transmitters also affect these mechanosensilla.…”