A‐type K⁺ current dominates somatic excitability of delayed firing neurons in rat substantia gelatinosa

Abstract

Substantia gelatinosa neurons display three main types of intrinsic firing behavior: tonic, adapting, and delayed onset. Here, voltage-gated currents expressed by delayed firing neurons were studied in nucleated patches obtained in spinal cord slices of 3-5 weeks-old rats. Inward Na+ current was negligible under these conditions and was usually occluded by superposition of much larger outward currents. Two kinds of outward currents were found, an A-type (K(A) ) and delayed rectifier (K(DR) ) potassium currents. K(A) activated rapidly (<1.5 ms at >-20 mV) and operated at subthreshold membrane potentials; voltages of steady-state half-maximal activation and inactivation were -38.7 and -87.2 mV, respectively. Inactivation was biexponential with a dominant fast component (~90%, time constant ∼8 ms). K(DR) activated more slowly (<8 ms at >-20 mV), half-maximal activation was -23.6 mV, and decayed mono-exponentially with a time constant 70-110 ms. Maximal amplitudes of K(A) were almost 10-times larger than those of K(DR) , their respective densities were 8.5 and 0.97 μS μm⁻². Tetraethylammonium, 5 mM, blocked K(DR) but not K(A) , whereas both currents were depressed by 5 mM 4-aminopyridine. In current-clamp recordings, 4-action potential but not tetraethylammonium abolished firing delay suggesting the causative role of K(A) . Thus, the predominance of fast K(A) over other somatic currents is a distinctive feature of delayed firing neurons among all other types of substantia gelatinosa neurons and likely explains the appearance of their typical firing delay.

Aging alters signaling properties in the mouse spinal dorsal horn

“…Rather many neurons can exhibit a range of discharge responses depending on factors such as membrane potential, neuromodulator signaling, and voltage-gated ion channel expression patterns. [31][32][33][34][35] For example, a shift to tonic firing could result if there were a reduction in A-type potassium currents either due to reduced expression of the underlying potassium channel or if channel function were modulated. 36,37 Such conditions would diminish the capacity of the A-type potassium current to delay AP discharge and produce tonic firing.…”

Are all spinal segments equal: intrinsic membrane properties of superficial dorsal horn neurons in the developing and mature mouse spinal cord

“…Values for R IN , RMP and selected AP properties do not vary along the rostrocaudal axis of the adult spinal cord (Tables 1 and 2). Moreover, the discharge categories described previously in lumbar SDH neurons in deeply anaesthetized rodents (Graham et al 2004), acute slices (Prescott & De Koninck, 2002; Ruscheweyh & Sandkuhler, 2002; Melnick, 2011) or organotypic cultures (Lu et al 2006) are represented in the three spinal cord regions we examined. These data suggest the relative constancy in the electrophysiological properties and discharge heterogeneity is fundamental to the way SDH neurons process peripheral signals, regardless of their source.…”

“…As the I Ar current is thought to suppress excitability and underlie delayed firing (Connor & Stevens, 1971; Hu et al 2007; Melnick, 2011) it is surprising that delayed firing is not the dominant discharge pattern in SDH neurons. In fact, in neonates delayed firing is rarely observed in any spinal region (Fig.…”

Contrasting Alterations to Synaptic and Intrinsic Properties in Upper-Cervical Superficial Dorsal Horn Neurons following Acute Neck Muscle Inflammation

“…Given I Ar currents are diminished in SDH neurons from carrageenan-injected animals one might expect this to impact on neurons with the delayed-and reluctant firing AP discharge pattern as the two have been associated in a number of previous studies [18,46,47]. For example, diminished I Ar would either reduce the delay before AP discharge or reduce the proportion of neurons exhibiting delayed and reluctant firing and convert them to more excitable forms of discharge such as tonic firing or initial bursting.…”