Feedback modulation of transduction by calcium in a spider mechanoreceptor

Abstract

Calcium ions play important roles in the adaptation of auditory hair cells, and there is evidence that they are involved in modifying the sensitivity and adaptation of a variety of vertebrate and invertebrate mechanoreceptors. However, there is little direct evidence concerning the concentration changes, signaling pathways or ultimate effects of these proposed modulatory mechanisms. We measured receptor potential, receptor current and action potentials intracellularly during mechanotransduction in a group of sensory neurons of the spider Cupiennius salei, which possesses low-voltage-activated calcium channels. Simultaneously, we elevated intracellular [Ca(2+) ] by UV light release from cage molecules, and observed increases in [Ca(2+) ] as changes in calcium-sensitive dye fluorescence. Increases of 10-15% in [Ca(2+) ] caused reductions of approximately 40% in receptor potential and approximately 20% in receptor current. Mechanically evoked action potential firing caused much larger increases in [Ca(2+) ], and the firing rate fell as [Ca(2+) ] rose during mechanical stimulation. Release of caged calcium just before mechanical stimulation significantly reduced peak firing. Dose-response measurements suggested that the binding of one or two intracellular calcium ions per channel reduces the probability of the mechanotransduction channel being open. Our data indicate that calcium regulates sensitivity in these mechanoreceptor neurons by negative feedback from action potentials onto transduction channels.

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

“…While our methods allowed separate examination of each stage, it is not possible to simply cascade the separate functions into an overall quantitative model because of possible feedback between stages. For example, action potentials are known to raise free intracellular Ca 2ϩ concentration ([Ca 2ϩ ]) and so increased firing would probably increase the effect on receptor current observed here under voltage clamp (Höger et al 2010).…”

“…Voltage jump experiments found a significant transient component of receptor potential (Gingl and French 2003) that is compatible with power-law behavior but does not explain it. Muscimol elevated [Ca 2ϩ ] in VS-3 neurons ) and increased intracellular [Ca 2ϩ ] attenuated responses to mechanical stimulation (Höger et al 2010), but this required opening of voltage-activated Ca 2ϩ channels by action potentials , which were blocked by TTX here. Finally, the distal sensory dendrite might have partially escaped the voltage clamp in the soma.…”

“…For example, the GABA A receptor agonist muscimol has been shown to raise Ca 2ϩ concentration in VS-3 neurons and Ca 2ϩ increase is also linked to the octopamine induced excitatory effect on these neurons (Torkkeli et al 2011). Since Ca 2ϩ has also been shown to modulate the receptor current (Höger et al 2010), it is possible that the earliest stages of sensory transmission are affected by GABA.To measure the contributions of GABAergic modulation to the three stages of mechanoreception, we investigated the responses of VS-3 neurons to muscimol for 15 min of pseudorandom mechanical stimulation during the excitatory period. We calculated frequency response functions between each stage, estimated signal entropy at each stage by data compression, and estimated information capacity between stages from the linear coherence function.…”

Calcium buffering and clearance in spider mechanosensory neurons

“…Ca 2? has been shown to provide feedback control of mechanically activated current (Höger et al 2010) and it regulates Ca 2? -and voltageactivated K ?…”

“…provides negative feedback by modulating the mechanotransduction channels themselves, and probably also modulating action potential encoding via Ca 2? -and voltageactivated ion channels in the cell membrane (Höger et al 2005;Höger et al 2010;Torkkeli et al 2011).…”