Contributions of Voltage- and Ca<sup>2+</sup>-Activated Conductances to GABA-Induced Depolarization in Spider Mechanosensory Neurons

Panek, Izabela; Höger, Ulli; French, Andrew S.; Torkkeli, Päivi H.

doi:10.1152/jn.01267.2007

Cited by 8 publications

(20 citation statements)

References 51 publications

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“…Depolarization can increase rate without affecting sensitivity. The power-law relationship of action potential encoding in VS-3 neurons has been attributed to activation and inactivation properties of voltage-activated Na ϩ and K ϩ channels (French and Torkkeli 2008). Depolarization would shift the operating characteristics of these channels but not necessarily affect overall encoding sensitivity.…”

Section: Discussionmentioning

confidence: 99%

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

Pfeiffer

Torkkeli

French

2012

Journal of Neurophysiology

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GABA(A) receptors mediate mainly inhibitory effects, but there are also many examples of excitatory effects in both mammalian and invertebrate preparations. Here, we aimed to create a complete, quantitative picture of GABA(A)-mediated excitation in a mechanosensory neuron where this phenomenon has been well established. We used muscimol to activate GABA(A) receptors in spider VS-3 neurons and measured the dynamic behavior independently and separately at each of three stages of mechanoreception (receptor current, receptor potential, and action potentials) before and during modulation. We calculated frequency response functions between each stage, estimated information as signal entropy, and estimated information capacity from coherence. Since coherence is sensitive to both noise and nonlinearity, we measured signal-to-noise separately at each stage by averaging responses to repeated mechanical inputs. Muscimol depolarized VS-3 neurons and, after brief inhibition, increased their firing rates. During this excitation, we found significant changes at each stage. Receptor current was attenuated but became more selective to high frequencies. Membrane impedance and time constant fell, favoring higher frequency transmission from receptor current to receptor potential. Action potential firing increased and had higher total entropy. Information capacity from signal-to-noise was always much higher than from coherence, confirming that intracellular noise does not limit signal transmission in these neurons. We conclude that GABA(A) receptor activation shifts each stage of mechanotransduction to higher frequency sensitivity, while the elevated firing rate increases the amount of information that can be encoded. These results show that a single neurotransmitter can finely modulate a sensory neuron's sensitivity and ability to transmit information.

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Section: Discussionmentioning

confidence: 99%

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

Pfeiffer

Torkkeli

French

2012

Journal of Neurophysiology

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“…current (Sekizawa et al 2000), and their intracellular [Ca 2? ] rises significantly during action potential firing and also when the neurons are depolarized by agonists of GABA A (c-aminobutyric acid) receptors (Höger et al 2007;Panek et al 2008). Previous evidence suggests that intracellular Ca 2?…”

Section: Introductionmentioning

confidence: 99%

Calcium buffering and clearance in spider mechanosensory neurons

et al. 2012

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Spider VS-3 mechanoreceptor neurons have a low-voltage-activated Ca2+ current that raises intracellular calcium concentration [Ca2+] when they are depolarized by agonists of GABAA receptors or fire action potentials. The Ca2+ rise produces negative feedback by modulating the mechanoreceptor current and regulates Ca2+- and voltage-activated K+ currents. However, nothing is known about Ca2+ buffering in VS-3 neurons. Dynamic changes in VS-3 neuron intracellular [Ca2+] were measured using the fluorescent Ca2+ indicator Oregon Green BAPTA-1 (OG488) to understand Ca2+ buffering and clearance. Intracellular OG488 concentration increased slowly over more than 2 h as it diffused through a sharp intracellular microelectrode and spread through the cell. This slow increase was used to measure endogenous Ca2+ buffering and clearance by the added buffer technique, with OG488 acting as both added exogenous buffer and Ca2+ indicator. [Ca2+] was raised for brief periods by regular action potential firing, produced by pulsed electric current injection through the microelectrode. The resulting rise and fall of [Ca2+] were well fitted by the single compartment model of Ca2+ dynamics. With earlier ratiometric [Ca2+] estimates, these data gave an endogenous Ca2+ binding ratio of 684. Strong Ca2+ buffering may assist these neurons to deal with rapid changes in mechanical inputs.

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“…Further blockade experiments with random stimulation gave modest reductions in mean firing rate, but only after periods of up to 1 h, and this treatment did not affect firing rate adaptation (Höger & French, 2005). Application of the GABA A receptor agonists muscimol or GABA induced a long‐lasting increase in [Ca 2+ ] (Δ F/F = 0.2) (Panek et al. , 2008).…”

Section: Discussionmentioning

confidence: 99%

Feedback modulation of transduction by calcium in a spider mechanoreceptor

Höger

Torkkeli

French

2010

Eur J of Neuroscience

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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.

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

Abstract: Panek I, Höger U, French AS, Torkkeli PH. Contributions of voltageand Ca 2ϩ -activated conductances to GABA-induced depolarization in spider mechanosensory neurons.

Cited by 8 publications

References 51 publications

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

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

Calcium buffering and clearance in spider mechanosensory neurons

Feedback modulation of transduction by calcium in a spider mechanoreceptor

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

Abstract: Panek I, Höger U, French AS, Torkkeli PH. Contributions of voltageand Ca 2ϩ -activated conductances to GABA-induced depolarization in spider mechanosensory neurons.

Cited by 8 publications

References 51 publications

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

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

Calcium buffering and clearance in spider mechanosensory neurons

Feedback modulation of transduction by calcium in a spider mechanoreceptor

Contact Info

Product

Resources

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

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

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