Mechanisms of postinhibitory rebound and its modulation by serotonin in excitatory swim motor neurons of the medicinal leech

Abstract

Postinhibitory rebound (PIR) is defined as membrane depolarization occurring at the offset of a hyperpolarizing stimulus and is one of several intrinsic properties that may promote rhythmic electrical activity. PIR can be produced by several mechanisms including hyperpolarization-activated cation current (I(h)) or de-inactivation of depolarization-activated inward currents. Excitatory swim motor neurons in the leech exhibit PIR in response to injected current pulses or inhibitory synaptic input. Serotonin, a potent modulator of leech swimming behavior, increases the peak amplitude of PIR and decreases its duration, effects consistent with supporting rhythmic activity. In this study, we performed current clamp experiments on dorsal excitatory cell 3 (DE-3) and ventral excitatory cell 4 (VE-4). We found a significant difference in the shape of PIR responses expressed by these two cell types in normal saline, with DE-3 exhibiting a larger prolonged component. Exposing motor neurons to serotonin eliminated this difference. Cs+ had no effect on PIR, suggesting that I(h) plays no role. PIR was suppressed completely when low Na+ solution was combined with Ca2+-channel blockers. Our data support the hypothesis that PIR in swim motor neurons is produced by a combination of low-threshold Na+ and Ca2+ currents that begin to activate near -60 mV.

Convergent Rhythm Generation from Divergent Cellular Mechanisms

“…PIR bursts often involve the complementary influence of multiple voltage-dependent inward currents, as during CabPK modulation of the LG neuron (McCormick and Bal, 1997;Sekirnjak and du Lac, 2002;Angstadt et al, 2005;Sangrey and Jaeger, 2010;Wang et al, 2011;Engbers et al, 2011;Felix et al, 2011;Zheng and Raman, 2011). One inward current that often contributes to the initial PIR depolarization is I h (McCormick and Bal, 1997;Sekirnjak and du Lac, 2002;Robinson and Siegelbaum, 2003;Pirtle et al, 2010;Sangrey and Jaeger, 2010;Engbers et al, 2011;Felix et al, 2011).…”

“…These latter currents often have time-and voltagedependent properties similar to those of CabPK-activated I Trans-LTS . In many neurons, the additional PIR-generating current is some type of I Ca (McCormick and Bal, 1997;Angstadt et al, 2005;Sangrey and Jaeger, 2010;Wang et al, 2011;Engbers et al, 2011;Felix et al, 2011). The role of I h in PIR bursts is similar to that of CabPK-activated I MI in LG, which depolarizes the LG neuron after a period of inhibition and enables sufficient I Trans-LTS MCN1 and CabPK activation of the gastric mill rhythm generator involves both divergent actions of the same ionic current (I MI ) and a conserved function mediated by distinct ionic currents (I MI , I Trans-LTS ; Fig.…”

Mechanisms contributing to the dopamine induction of crawl-like bursting in leech motoneurons

“…Recently, blocking persistent sodium currents with riluzole has been shown to reduce the late component of the PIR and block bursting in cell DE-3 (Angstadt et al, 2011), unlike DA, which attenuates the PIR and promotes bursting. Furthermore, although reduced sodium salines decrease PIR in DE-3, the PIR is eliminated only when sodium is reduced and Ca 2+ is replaced with nickel (Angstadt et al, 2005) or in solutions containing high concentrations (10mmoll -1 ) of nickel (Angstadt et al, 2011). These observations suggest that a portion of the PIR is Ca 2+ -dependent and that the PIR is mediated by both persistent sodium and nonspecific cation currents.…”

Oxytocin-Induced Postinhibitory Rebound Firing Facilitates Bursting Activity in Oxytocin Neurons

“…4 B4 ). Such process is reminiscent of PIR, as described in other structures (Bertrand and Cazalets, 1998;Angstadt et al, 2005;Sohal et al, 2006). PIR is defined as the depolarization that occurs at the offset of a hyperpolarizing period.…”