Low-Voltage-Activated Calcium Current Does Not Regulate the Firing Behavior in Paired Mechanosensory Neurons With Different Adaptation Properties

Abstract

Low-voltage-activated Ca(2+) currents (LVA-I(Ca)) are believed to perform several roles in neurons such as lowering the threshold for action potentials, promoting burst firing and oscillatory behavior, and enhancing synaptic excitation. They also may allow rapid increases in intracellular Ca(2+) concentration. We discovered LVA-I(Ca) in both members of paired mechanoreceptor neurons in a spider, where one neuron adapts rapidly (Type A) and the other slowly (Type B) in response to a step stimulus. To learn if I(Ca) contributed to the difference in adaptation behavior, we studied the kinetics of I(Ca) from isolated somata under single-electrode voltage-clamp and tested its physiological function under current clamp. LVA-I(Ca) was large enough to fire single action potentials when all other voltage-activated currents were blocked, but we found no evidence that it regulated firing behavior. LVA-I(Ca) did not lower the action potential threshold or affect firing frequency. Previous experiments have failed to find Ca(2+)-activated K(+) current (I(K(Ca))) in the somata of these neurons, so it is also unlikely that LVA-I(Ca) interacts with I(K(Ca)) to produce oscillatory behavior. We conclude that LVA-Ca(2+) channels in the somata, and possible in the dendrites, of these neurons open in response to the depolarization caused by receptor current and by the voltage-activated Na(+) current (I(Na)) that produces action potential(s). However, the role of the increased intracellular Ca(2+) concentration in neuronal function remains enigmatic.

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

“…TTX completely blocks the voltageactivated Na ϩ current in these neurons (Torkkeli et al 2001). Therefore the remaining inward current in the test potentials used here (Ϫ50 to 0 mV) was most likely the LVA Ca 2ϩ current previously described in these neurons (Sekizawa et al 2000). The sustained outward current cannot be blocked by K-channel blockers or conventional inhibitors of I K(Ca) (Sekizawa et al 1999).…”

“…This treatment was previously shown to block the LVA Ca 2ϩ current in these neurons (Sekizawa et al 2000). After the neurons were superfused by Ni 2ϩ solution for a minimum of 20 min, the depolarization amplitude increased (Fig.…”

“…The sustained outward current cannot be blocked by K-channel blockers or conventional inhibitors of I K(Ca) (Sekizawa et al 1999). However, this current was partially inhibited by Ni 2ϩ , which blocks LVA Ca channels (Sekizawa et al 2000), suggesting that it may be I K(Ca) that is not sensitive to the conventional blockers of this currents. To further test this possibility, we investigated whether mibefradil, a potent blocker of LVA Ca channels (Bezprozvanny and Tsien 1995;Catterall et al 2005), would have an effect on the sustained outward current along with the inward current.…”

“…This current produced large action potentials when all other voltage-activated Na ϩ and K ϩ currents were blocked. Blockers of Ca 2ϩ -activated K ϩ current [I K(Ca) ], such as charybdotoxin, apamin, and iberiotoxin, did not have any effect on the outward currents or firing behavior of these neurons (Sekizawa et al 2000). However, Ni 2ϩ and Cd 2ϩ inhibit the outward current that remains after voltage-gated K ϩ currents are blocked by TEA and 4-AP, suggesting that an outward current component sensitive to Ca 2ϩ is present in these neurons.…”

“…However, Յ50% of the noninactivating component was not blocked even with a high concentration of combination of these drugs or other K-channel blockers (Sekizawa et al 1999). The only Ca 2ϩ current that has been described in the VS-3 neurons is the transient low-voltage-activated (LVA) current, that can be completely blocked with Ni 2ϩ or Cd 2ϩ (Sekizawa et al 2000). This current activated at about Ϫ50 mV and inactivated rapidly within 50 -150 ms depending on the test voltage.…”