Dendritic excitability and localization of GABA‐mediated inhibition in spider mechanoreceptor neurons

Abstract

GABAergic inhibition of mechanosensory afferent axon terminals is a widespread phenomenon in vertebrates and invertebrates. Spider mechanoreceptor neurons receive efferent innervation on their peripherally located axons, somata and sensory dendrites, and the dendrites have recently been shown to be excitable. Excitability of the spider sensory neurons is inhibited by muscimol and GABA, agonists of ionotropic GABA receptors. Here we asked where in the neurons this inhibition occurs. We found no evidence for inhibition of action potentials in the sensory dendrites, but axonal action potentials were rapidly suppressed by both agonists. Earlier work showed that metabotropic GABA(B) receptors are located on the dendrites and distal somata of the spider sensory neurons, where they modulate voltage-activated conductances and may provide slower, prolonged inhibition. Therefore, GABA released from single peripheral efferents may activate both ionotropic and metabotropic receptor types, providing rapid suppression of axonal activity followed by slower inhibition that eventually prevents action potential initiation in the distal dendrites.

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

“…The present results and the simulated model both show that Na ϩ current is only partially inactivated by the level of depolarization produced by GABA. This is probably also the current responsible for small spontaneous action potentials that have occasionally been observed at the crest of GABA-induced depolarization in VS-3 neurons (Gingl et al 2004).…”

“…GABA-mediated depolarization and inhibition in spider VS-3 neurons is not exactly presynaptic, since it occurs in the peripherally located axosomatic region of these neurons rather that in the axon terminals (Gingl et al 2004). However, the depolarization, shunting, and inhibition are very similar .…”

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

“…Previously, mechanically stimulated VS-3 neurons were shown to generate APs in the distal dendrite, close to the stimulation site (Gingl and French 2003;Gingl et al 2004). To learn whether muscimol-induced changes in firing rate occurred only for dendritic APs, we performed experiments where the VS-3 neuron somata were stimulated directly by the recording electrode.…”

“…When action potential (AP) responses to mechanical stimuli were recorded extracellularly at different locations, the inhibitory response could be detected only at the axonal region, suggesting that the GABA A receptors may be located only at the axons (Gingl et al 2004). In nature, the slits are believed to respond to strains and vibrations that occur in the spider's environment or are elicited by body movements (Barth 2001;Seyfarth 1985).…”

“…Previous investigations showed that the distal dendrites of VS-3 neurons generate APs and that the inhibitory response to GABA A agonists occurs only in the axonal region (Gingl and French 2003;Gingl et al 2004). To learn whether the changes in the dynamic behaviors of dendritic and axosomatic regions are different when the GABA A receptor agonist muscimol is applied, we performed two series of experiments using either mechanical stimuli to generate dendritic APs or electrical stimuli to generate axosomatic APs.…”