Potassium current kinetics in bursting secretory neurons: effects of intracellular calcium

Martínez, J. Jesús García; Onetti, Carlos G.; Garcı́a, Esperanza; Hernandez, Sofia

doi:10.1152/jn.1991.66.5.1455

Cited by 10 publications

(4 citation statements)

References 23 publications

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“…This is a biologically plausible mechanism, as there are an increasing number of reports suggesting that intracellular Ca 2ϩ and activity can regulate membrane currents (e.g., refs. [35][36][37].…”

Section: Long-term Control Of Intrinsic Conductances: the Role Of Actmentioning

confidence: 99%

Memory from the dynamics of intrinsic membrane currents

Marder

Abbott

Turrigiano

et al. 1996

Proc. Natl. Acad. Sci. U.S.A.

268

199

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Almost all theoretical and experimental studies of the mechanisms underlying learning and memory focus on synaptic efficacy and make the implicit assumption that changes in synaptic efficacy are both necessary and sufficient to account for learning and memory. However, network dynamics depends on the complex interaction between intrinsic membrane properties and synaptic strengths and time courses. Furthermore, neuronal activity itself modifies not only synaptic efficacy but also the intrinsic membrane properties of neurons. This paper presents examples demonstrating that neurons with complex temporal dynamics can provide short-term ''memory'' mechanisms that rely solely on intrinsic neuronal properties. Additionally, we discuss the potential role that activity may play in long-term modification of intrinsic neuronal properties. While not replacing synaptic plasticity as a powerful learning mechanism, these examples suggest that memory in networks results from an ongoing interplay between changes in synaptic efficacy and intrinsic membrane properties.The behavior of rhythmic networks depends on the complex interaction between the dynamics of the individual neurons (their intrinsic properties) and the strengths and time courses of the synapses among them (1-3). Years of research on networks as diverse as central pattern generators in invertebrates and vertebrates (3), the thalamus (4-6), and the cerebellum (7) have clearly shown that complex neuronal characteristics, such as oscillatory and plateau properties, play crucial roles in shaping neural network output. Recent work has expanded the brain regions that show neuronal oscillations to the cortex (8), suggesting that complex intrinsic properties are likely to shape the computational dynamics of many, if not all, brain regions.It is commonly assumed that short and long-lasting changes in synaptic efficacy are both necessary and sufficient to account for the stable changes in network dynamics that we call ''memory''. The remarkable success of early neural network models, in which only synaptic strengths were modified but memories were stored, showed that changes in network output could result solely from changes in synaptic strength (9). An attractive feature of synaptic modification is that it can be restricted to a subset of the synaptic connections made by a neuron, or made onto a neuron. And last, but not least, the experimental work on the Aplysia gill withdrawal reflex and hippocampal slices, in which long-lasting changes in synaptic strength could be produced, and the mechanisms underlying those changes studied (10, 11) provided strong impetus to look primarily at synaptic plasticity as the mechanism underlying memory in intact animals. However, in this paper, we show that intrinsic neuronal currents can also play a role in memory phenomena in at least two different ways. First, a variety of ''short-term'' memory mechanisms can result from slowly activating and inactivating membrane conductances that make the response of a cell depend on its recent...

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Section: Long-term Control Of Intrinsic Conductances: the Role Of Actmentioning

confidence: 99%

Memory from the dynamics of intrinsic membrane currents

Marder

Abbott

Turrigiano

et al. 1996

Proc. Natl. Acad. Sci. U.S.A.

268

199

View full text Add to dashboard Cite

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“…Calcium sensitivity is a very important phenomenon because the firing patterns have been associated with the ability for secretion in neurons (Stuenkel 1985). Several potassium currents contributing to modulate action potential firing patterns have been previously described in X-organ neurons: the delayed rectifier, the transient inactivating outward current (Martínez et al 1991), and the ATPsensitive K ϩ current (García et al 1993;Onetti et al 1996). Experimental evidence supports a key role of intracellular Ca 2ϩ in the modulation of these currents.…”

Section: Introductionmentioning

confidence: 99%

“…In the X-organ sinus gland (XO-SG) system, the most important neurosecretory system of the crayfish, a periodic increase in [Ca 2ϩ ] i in bursting neurons modifies membrane conductances and regulates electrophysiological activity (Martínez et al 1991;Onetti et al 1990). Calcium sensitivity is a very important phenomenon because the firing patterns have been associated with the ability for secretion in neurons (Stuenkel 1985).…”

Section: Introductionmentioning

confidence: 99%

Large-Conductance Ca²⁺-Activated Potassium Channels in Secretory Neurons

Lara

Acevedo-Fernández

Onetti

1999

Journal of Neurophysiology

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Large-conductance Ca2+-activated K+ channels (BK) are believed to underlie interburst intervals and contribute to the control of hormone release in several secretory cells. In crustacean neurosecretory cells, Ca2+ entry associated with electrical activity could act as a modulator of membrane K+ conductance. Therefore we studied the contribution of BK channels to the macroscopic outward current in the X-organ of crayfish, and their participation in electrophysiological activity, as well as their sensitivity toward intracellular Ca2+, ATP, and voltage, by using the patch-clamp technique. The BK channels had a conductance of 223 pS and rectified inwardly in symmetrical K+. These channels were highly selective to K+ ions; potassium permeability (PK) value was 2.3 x 10(-13) cm(3) s(-1). The BK channels were sensitive to internal Ca2+ concentration, voltage dependent, and activated by intracellular MgATP. Voltage sensitivity (k) was approximately 13 mV, and the half-activation membrane potentials depended on the internal Ca2+ concentration. Calcium ions (0.3-3 microM) applied to the internal membrane surface caused an enhancement of the channel activity. This activation of BK channels by internal calcium had a KD(0) of 0.22 microM and was probably due to the binding of only one or two Ca2+ ions to the channel. Addition of MgATP (0.01-3 mM) to the internal solution increased steady state-open probability. The dissociation constant for MgATP (KD) was 119 microM, and the Hill coefficient (h) was 0.6, according to the Hill analysis. Ca2+-activated K+ currents recorded from whole cells were suppressed by either adding Cd2+ (0.4 mM) or removing Ca2+ ions from the external solution. TEA (1 mM) or charybdotoxin (100 nM) blocked these currents. Our results showed that both BK and K(ATP) channels are present in the same cell. Even when BK and K(ATP) channels were voltage dependent and modulated by internal Ca2+ and ATP, the profile of sensitivity was quite different for each kind of channel. It is tempting to suggest that BK and KATP channels contribute independently to the regulation of spontaneous discharge patterns in crayfish neurosecretory cells.

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“…Two voltage-dependent K + currents were described, and their importance in determining the firing rate and the shape of action potentials was pointed out [17].…”

Section: Introductionmentioning

confidence: 99%

Adenine nucleotides and intracellular Ca2+ regulate a voltage-dependent and glucose-sensitive potassium channel in neurosecretory cells

Onetti

Lara

Garcı́a

1996

Pflugers Arch - Eur J Physiol

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Effects of membrane potential, intracellular Ca2+ and adenine nucleotides on glucose-sensitive channels from X organ (XO) neurons of the crayfish were studied in excised inside-out patches. Glucose- sensitive channels were selective to K+ ions; the unitary conductance was 112 pS in symmetrical K+, and the K+ permeability (PK) was 1.3 x 10(-13) cm x s(-1). An inward rectification was observed when intracellular K+ was reduced. Using a quasi-physiological K+ gradient, a non-linear K+ current/voltage relationship was found showing an outward rectification and a slope conductance of 51 pS. The open-state probability (Po) increased with membrane depolarization as a result of an enhancement of the mean open time and a shortening of the longer period of closures. In quasi-physio- logical K+ concentrations, the channel was activated from a threshold of about -60 mV, and the activation midpoint was -2 mV. Po decreased noticeably at 50 microM internal adenosine 5'-triphosphate (ATP), and single-channel activity was totally abolished at 1 mM ATP. Hill analysis shows that this inhibition was the result of simultaneous binding of two ATP molecules to the channel, and the half-blocking concentration of ATP was 174 microM. Internal application of 5'-adenylylimidodiphosphate (AMP-PNP) as well as glibenclamide also decreased Po. By contrast, the application of internal ADP (0.1 to 2 mM) activated this channel. An optimal range of internal free Ca2+ ions (0.1 to 10 microM) was required for the activation of this channel. The glucose--sensitive K+ channel of XO neurons could be considered as a subtype of ATP-sensitive K+ channel, contributing substantially to macroscopic outward current.

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Potassium current kinetics in bursting secretory neurons: effects of intracellular calcium

Cited by 10 publications

References 23 publications

Memory from the dynamics of intrinsic membrane currents

Memory from the dynamics of intrinsic membrane currents

Large-Conductance Ca²⁺-Activated Potassium Channels in Secretory Neurons

Adenine nucleotides and intracellular Ca2+ regulate a voltage-dependent and glucose-sensitive potassium channel in neurosecretory cells

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Potassium current kinetics in bursting secretory neurons: effects of intracellular calcium

Cited by 10 publications

References 23 publications

Memory from the dynamics of intrinsic membrane currents

Memory from the dynamics of intrinsic membrane currents

Large-Conductance Ca2+-Activated Potassium Channels in Secretory Neurons

Adenine nucleotides and intracellular Ca2+ regulate a voltage-dependent and glucose-sensitive potassium channel in neurosecretory cells

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Product

Resources

About

Large-Conductance Ca²⁺-Activated Potassium Channels in Secretory Neurons