Intracellular measurements from a rapidly adapting sensory neuron

The femoral tactile spine of the cockroach contains a single sensory neuron with its cell body in the lumen of the spine. Step movements of the spine produce rapidly adapting bursts of action potentials that decay to 0 in 1 s. Previous work has shown that a large part of this adaptation occurs during action potential encoding. Intracellular recordings from the tactile spine neuron were obtained by lowering a microelectrode through the spine lumen and penetrating the cell body. Injection of Lucifer yellow followed by fluorescence microscopy confirmed the morphology of the soma, with a diameter of 30 μm, and showed an axon of 9 μm leaving the spine and proceeding proximally along the femur. Membrane-potential records were digitized and examined at high resolution during bursts of action potentials produced by depolarizing current pulses. No significant changes in action potential shape were detected during adaptation. However, the rate of depolarization between action potentials slowed dramatically during the burst. This slowing could be reduced and the burst substantially prolonged by chloramine-T (CT), an agent that reduces sodium channel inactivation in several preparations. A 100 Hz sinusoidal current was superimposed on depolarizing current pulses to test for changes in membrane conductance during a burst of action potentials. No such changes were detected, indicating that rapid adaptation is not due to changes in membrane permeability. Prolonged bursts of action potentials were followed by an after hyperpolarization (AHP) of a few millivolts, which decayed with a time constant of several seconds. The most likely cause of this phenomenon is an electrogenic pump. However, the relative contribution of pumping to action potential adaptation is unlikely to be large. Passive membrane impedance was estimated by injecting a subthreshold, white noise current stimulus and observing the resulting membrane potential fluctuations. Complex impedance functions could be fitted by a first-order, frequency response function having a direct current (DC) resistance of ~67 MΩ and a time constant of ~1.7 ms, in good agreement with results obtained from hyperpolarizing step pulses and earlier estimates from this neuron based on other techniques. A model for rapid adaptation that is compatible with these findings, and earlier observations on this neuron, has voltage-activated sodium channels that control the threshold of the neuron and inactivate with a time constant in the 100 ms range during prolonged depolarizations.