Peripheral GABAergic inhibition of spider mechanosensory afferents

Abstract

Spider mechanosensory neurons receive an extensive network of efferent synapses onto their sensory dendrites, somata and distal axonal regions. The function of these synapses is unknown. Peripheral synapses are also found on crustacean stretch-receptor neurons but not on mechanosensory afferents of other species, although inhibitory GABAergic synapses are a common feature of centrally located axon terminals. Here we investigated the effects of GABA receptor agonists and antagonists on one group of spider mechanosensory neurons, the slit sense organ VS-3, which are accessible to current- and voltage-clamp recordings. Bath application of GABA activated an inward current that depolarized the membrane and increased the membrane conductance leading to impulse inhibition. VS-3 neuron GABA receptors were activated by muscimol and inhibited by picrotoxin but not bicuculline, and their dose-response relationship had an EC(50) of 103.4 microm, features typical for insect ionotropic GABA receptors. Voltage- and current-clamp analysis confirmed that, while the Na(+) channel inhibition resulting from depolarization can lead to impulse inhibition, the increase in membrane conductance (i.e. 'shunting') completely inhibited impulse propagation. This result argues against previous findings from other preparations that GABA-mediated inhibition is caused by a depolarization that inactivates Na(+) conductance, and it supports those findings that assign this role to membrane shunting. Our results show that GABA can rapidly and selectively inhibit specific mechanoreceptors in the periphery. This type of peripheral inhibition may provide spiders with a mechanism for distinguishing between signals from potential prey, predators or mates, and responding with appropriate behaviour to each signal.

Random Stimulation of Spider Mechanosensory Neurons Reveals Long-Lasting Excitation by GABA and Muscimol

“…It would be difficult to replicate the strains and vibrations that naturally excite these neurons, but stimulation with random signals provides a wide range of frequencies and amplitudes, giving a closer approximation to natural stimulation than deterministic step or sinusoidal stimuli. In previous experiments using step electrical stimuli, VS-3 neurons were inhibited by GABA and muscimol, whereas the same agonists had a smaller effect on mechanically stimulated neurons (Gingl et al 2004;Panek et al 2002). Our current results indicate that the VS-3 neuron response to these agonists is much more complex with random stimulation.…”

Contributions of Voltage- and Ca2+-Activated Conductances to GABA-Induced Depolarization in Spider Mechanosensory Neurons

“…In some, the GABA current reversal potentials are less negative than the resting potentials (Obrietan and van den Pol 1995;Panek et al 2002;Reichling et al 1994); in others they are closer to the resting membrane potential (Connors et al 1987). Because of this, there is some controversy about the mechanism of [Ca 2ϩ ] increase.…”

“…There are large differences in the amounts of membrane depolarization associated with GABA-mediated presynaptic inhibition in different neurons, from a few millivolts in locust proprioceptive afferents and crayfish stretch receptor neurons (Burrows and Laurent 1993;Kaila et al 1992) to tens of millivolts in the crab lateral pyloric neurons, crayfish chordotonal organ, and sensory afferents of the spider slit sensilla (Cattaert et al 1992;Panek et al 2002;Swensen et al 2000). These differences are believed to rise from the differences in the intracellular [Cl Ϫ ] in these neurons (Alvarez-Leefmans et al 1998).…”

“…Cellular mechanisms of shunting and depolarization in centrally located afferent terminals have been difficult to unravel. However, GABA has similar effects on the peripherally located parts of arachnid and crustacean mechanosensory neurons making these models more experimentally accessible (Cattaert and El Manira 1999;Panek et al 2002).…”

“…The efferent fibers contain GABA, glutamate, and acetylcholine, which all inhibit the responses of sensory neurons to step mechanical or electrical stimuli (FabianFine et al 2002;Panek and Torkkeli 2005;Panek et al 2002;Widmer et al 2006). Octopamine is also present in some of the efferent fibers and octopamine application has an excitatory effect on neuronal activity (Widmer et al 2005).…”