Slow adaptation in spider mechanoreceptor neurons

Abstract

Slow adaptation of action potential firing is a common but poorly understood property of sensory neurons. We quantified slow adaptation in a cuticular mechanoreceptor organ of the spider, Cupiennius salei, by stimulating with continuous pseudorandom mechanical displacements while recording action potentials intracellularly from the cell bodies. Firing rate declined over a period of several minutes before reaching a steady level at about half the initial rate. This slow adaptation was fitted by an exponential decay with mean time constant of 18.5 s. Recovery from slow adaptation was also fitted by an exponential process, but with a longer time constant of 167 s. The receptor potential produced by the same stimulation protocol did not change its amplitude or dynamics, showing that slow adaptation occurs during action potential encoding from the receptor potential. Experiments with chemical blockers of calcium entry or the known potassium currents failed to reduce the slow adaptation. The Na+/K+ pump blocker Ouabain decreased the time constant of slow adaptation, suggesting that ion accumulation is involved. In some experiments, a second class of small action potentials were observed, which were tentatively attributed to failed conduction from the sensory dendrite through the soma to the axon.

Locust wing stretch receptor adaptation and recovery from adaptation

“…The biphasic recovery from adaptation of the locust wing stretch receptor favours this hypothesis: if the adaptation exceeds a certain duration, the intracellular concentration of Na + may increase, and the Na + -K + pump will start generating a net outward current causing membrane hyperpolarization. However, the contribution of the electrogenic activity of the Na + -K + pump to adaptation was not proven in spider mechanoreceptor neurons [23] and hypoglossal motoneurons [7]. The results we have obtained do not allow excluding some other mechanism contributing to adaptation in the locust wing stretch receptor.…”

“…Therefore, adaptation and recovery from adaptation are tightly coupled. The recovery from adaptation can be used to describe adaptation [2,3,[21][22][23].…”

Slow and Persistent Postinhibitory Rebound Acts as an Intrinsic Short-Term Memory Mechanism

“…Spike frequency adaptation (SFA) has been extensively documented in numerous sensory systems, and it occurs on both short and long time scales (Nelken, 2004; Gardner et al, 2005; Hoger and French, 2005; Gabbiani and Krapp, 2006). Just as there is a slow form of SFA, the phenomenon documented here is a slow form of PIR.…”

Incorporating spike-rate adaptation into a rate code in mathematical and biological neurons

“…Spike-rate adaptation can occur on characteristic timescales ranging from tens of milliseconds (Madison and Nicoll 1984;Stocker et al 1999) to many seconds (Höger and French 2005), even within the same neuron (La Camera et al 2006). Adaptation is usually attributed to the M-type K ϩ current (I M ), which is activated below the voltage threshold and is largely spike independent, or to the spike-dependent, calcium-activated K ϩ current I AHP ("afterhyperpolarization") (Brown and Adams 1980;Huguenard et al 1985; Madison and Nicoll 1984;Prescott and Sejnowski 2008;Schwindt et al 1988;Storm 1990).…”

“…Adaptation is usually attributed to the M-type K ϩ current (I M ), which is activated below the voltage threshold and is largely spike independent, or to the spike-dependent, calcium-activated K ϩ current I AHP ("afterhyperpolarization") (Brown and Adams 1980;Huguenard et al 1985; Madison and Nicoll 1984;Prescott and Sejnowski 2008;Schwindt et al 1988;Storm 1990). Other mechanisms implicated include slow inactivation of Na ϩ channels (Fleidervish et al 1996), a sodiumactivated K ϩ current (Schwindt et al 1989), actions on ion pumps (French 1989;Sokolove and Cooke 1971), extracellular ion accumulation (Höger and French 2005), and, in the case of mechanosensory neurons, viscoelastic properties (Brown and Stein 1966;Nakajima and Onodera 1969).…”