Calcium-induced Transitions between the Spontaneous Miniature Outward and the Transient Outward Currents in Retinal Amacrine Cells

Abstract

Spontaneous miniature outward currents (SMOCs) occur in a subset of retinal amacrine cells at membrane potentials between −60 and −40 mV. At more depolarized potentials, a transient outward current (Ito) appears and SMOCs disappear. Both SMOCs and the Ito are K+ currents carried by BK channels. They both arise from Ca2+ influx through high voltage–activated (HVA) Ca2+ channels, which stimulates release of internal Ca2+ from caffeine- and ryanodine-sensitive stores. An increase in Ca2+ influx resulted in an increase in SMOC frequency, but also led to a decline in SMOC mean amplitude. This reduction showed a temporal dependence: the effect being greater in the latter part of a voltage step. Thus, Ca2+ influx, although required to generate SMOCs, also produced a negative modulation of their amplitudes. Increasing Ca2+ influx also led to a decline in the first latency to SMOC occurrence. A combination of these effects resulted in the disappearance of SMOCs, along with the concomitant appearance of the Ito at high levels of Ca2+ influx. Therefore, low levels of Ca2+ influx, arising from low levels of activation of the HVA Ca2+ channels, produce randomly occurring SMOCs within the range of −60 to −40 mV. Further depolarization leads to greater activation of the HVA Ca2+ channels, larger Ca2+ influx, and the disappearance of discontinuous SMOCs, along with the appearance of the Ito. Based on their characteristics, SMOCs in retinal neurons may function as synaptic noise suppressors at quiescent glutamatergic synapses.

BK Channels in the Central Nervous System

“…In a subset of amacrine cells, BK channels mediate spontaneous miniature outward currents, which are hypothesized to serve as synaptic noise suppressors at quiescent glutamatergic synapses (Mitra & Slaughter, 2002a, 2002b). In A17 amacrine cells, BK channels also suppress activation of Ca V channels to limit GABA release onto rod bipolar cells (Grimes et al, 2009).…”

Computational Models and Emergent Properties of Respiratory Neural Networks

“…Dunin-Barkowski et al (67) proposed a model of the respiratory CPG incorporating at the neuronal level interactions between Ca +2 -dependent K + channels in respiratory neurons (191) and Ca +2 -induced Ca +2 -release from intracellular stores (123, 197, 198, 294) as a potential dynamic mechanism for rhythm generation at cellular and network levels. Addressing the debate about pacemaker versus inhibitory network mechanisms for rhythm generation, these investigators sought to define Ca 2+ -dependent mechanisms that could simultaneously underlie neuronal bursting pacemaker properties as well as support inhibitory-based network oscillations due to neuron activity adaptation arising from the modeled Ca 2+ -dependent processes.…”

Differential effects of charybdotoxin on the activity of retinal ganglion cells in the dark- and light-adapted mouse retina

“…In retina, calcium-activated potassium channels have been located in several different cell types, including photoreceptors (Baylor et al, 1984; Barnes and Hill, 1989; Maricq and Korenbrot, 1990; Rispoli et al, 1995; Moriondo et al, 2001), bipolar cells (Sakaba et al, 1997; Llobet et al, 2003; Palmer, 2006), amacrine cells (Mitra and Slaughter, 2002; Vigh et al, 2003), and ganglion cells (Lipton and Tauck, 1987; Wang et al, 1998, Rothe et al, 1999). There is also evidence that calcium-activated potassium channels play a role in retinal functions.…”