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

Abstract

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.