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

Abstract

Octopamine is a chemical relative of noradrenaline providing analogous neurohumoral control of diverse invertebrate physiological processes. There is also evidence for direct octopaminergic innervation of some insect peripheral tissues. Here, we show that spider peripheral mechanoreceptors are innervated by octopamine-containing efferents. The mechanosensory neurons have octopamine receptors colocalized with synapsin labeling in the efferent fibers. In addition, octopamine enhances the electrical response of the sensory neurons to mechanical stimulation.Spider peripheral mechanosensilla receive extensive efferent innervation. Many efferent fibers in the legs of Cupiennius salei are GABAergic, providing inhibitory control of sensory neurons, but there is also evidence for other neurotransmitters. We used antibody labeling to show that some efferents contain octopamine and that octopamine receptors are concentrated on the axon hillocks and proximal soma regions of all mechanosensory neurons in the spider leg. Synaptic vesicles in efferent neurons were concentrated in similar areas.Octopamine, or its precursor tyramine, increased responses of mechanically stimulated filiform (trichobothria) leg hairs. This effect was blocked by the octopamine antagonist phentolamine. The octopamine-induced modulation was mimicked by 8-Br-cAMP, a cAMP analog, and blocked by Rp-cAMPS, a protein kinase A inhibitor, indicating that spider octopamine receptors activate adenylate cyclase and increase cAMP concentration.Frequency response analysis showed that octopamine increased the sensitivity of the trichobothria neurons over a broad frequency range. Thus, the major effect of octopamine is to increase its overall sensitivity to wind-borne signals from sources such as flying insect prey or predators.

GABAergic Excitation of Spider Mechanoreceptors Increases Information Capacity by Increasing Entropy Rather than Decreasing Jitter

“…We showed previously that information capacity in spider mechanoreceptor neurons rises as the firing rate is increased by current injection (French et al, 2001), octopamine (Widmer et al, 2005), or GABA A agonists (Pfeiffer et al, 2009). Here, we asked whether this increased information capacity is caused by decreased jitter or by other mechanisms.…”

“…Neuromodulation can increase or decrease excitability, as seen by changes in membrane potential and action potential firing rates (Matheson, 1997;Page and Blackshaw, 1999;Rudomin and Schmidt, 1999;Torkkeli and Panek, 2002;Birmingham et al, 2003;Widmer et al, 2005). It can also affect dynamic properties of neuronal responses or spontaneous firing patterns (Ramirez et al, 1993;Matheson, 1997;Birmingham et al, 2003;Pfeiffer et al, 2009).…”

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

“…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). Intracellular recordings from neurons of VS-3 lyriform slit sensilla in the spider patella ) and a simulated model based on these recordings showed that GABAergic inhibition can be achieved by shunting or inactivation of Na channels and that these two factors can combine to cause stronger inhibition.…”

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

“…A larger value of k indicates a greater sensitivity to high frequencies and more rapid adaptation. An increase in information capacity R was previously observed in spider mechanosensory neurons when the firing rate increased (French et al 2001;Widmer et al 2005). Graphical comparisons of AP rate and amplitude as well as membrane potential (E m ) before and after muscimol application are also shown in Fig.…”

“…The 50-to 300-m-long sensory dendrites are attached to the slits via a specialized cuticular structure . Peripherally located parts of these neurons are surrounded by thin efferent fibers (FabianFine et al 1999) that have been shown to contain GABA, glutamate, and octopamine (Fabian-Fine et al 1999Widmer et al 2005).…”