Biophysical mechanisms contributing to inking behavior in Aplysia

Byrne, John H.; Shapiro, Eli; Dieringer, N.; Koester, John

doi:10.1152/jn.1979.42.5.1233

Cited by 52 publications

(67 citation statements)

References 42 publications

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“…Long delays to first-spike latency are consistent with the presence of a fast-inactivating K ϩ current (Byrne et al, 1979;Storm, 1988). However, a reduced first-spike latency following strong hyperpolarization suggested the interaction of an additional inward subthreshold current, which could include I T or I H .…”

Section: Resultsmentioning

confidence: 60%

“…The fast-inactivating class of K ϩ channels is known to be involved in actively generating a delay to first spike by activating in the subthreshold region after hyperpolarization (Byrne et al, 1979;Storm, 1988;Kanold and Manis, 1999). Conversely, I T has been generally implicated in generating rebound burst firing that is also promoted by a preceding hyperpolarization (Llinas and Jahnsen, 1982;Huguenard and Prince, 1992;Huguenard, 1996).…”

Section: Discussionmentioning

confidence: 99%

“…Many neurons actively generate long latencies to first spike that are sensitive to the preceding membrane voltage (Byrne et al, 1979;Storm, 1988;Kanold and Manis, 1999). Traditionally, a low threshold and fast inactivating K ϩ current (I A ) is required.…”

Section: Introductionmentioning

confidence: 99%

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A-Type and T-Type Currents Interact to Produce a Novel Spike Latency-Voltage Relationship in Cerebellar Stellate Cells

Molineux¹,

Fernandez²,

Mehaffey³

et al. 2005

J. Neurosci.

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The modification of first-spike latencies by low-threshold and inactivating K ϩ currents (I A ) have important implications in neuronal coding and synaptic integration. To date, cells in which first-spike latency characteristics have been analyzed have shown that increased hyperpolarization results in longer first-spike latencies, producing a monotonic relationship between first-spike latency and membrane voltage. Previous work has established that cerebellar stellate cells express members of the K v 4 potassium channel subfamily, which underlie I A in many central neurons. Spike timing in stellate cells could be particularly important to cerebellar output, because the discharge of even single spikes can significantly delay spike discharge in postsynaptic Purkinje cells. In the present work, we studied the first-spike latency characteristics of stellate cells. We show that first-spike latency is nonmonotonic, such that intermediate levels of prehyperpolarization produce the longest spike latencies, whereas greater hyperpolarization or depolarization reduces spike latency. Moreover, the range of first-spike latency values can be substantial in spanning 20 -128 ms with preceding membrane shifts of Ͻ10 mV. Using patch clamp and modeling, we illustrate that spike latency characteristics are the product of an interplay between I A and lowthreshold calcium current (I T ) that requires a steady-state difference in the inactivation parameters of the currents. Furthermore, we show that the unique first-spike latency characteristics of stellate cells have important implications for the integration of coincident IPSPs and EPSPs, such that inhibition can shift first-spike latency to differentially modulate the probability of firing.

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Section: Resultsmentioning

confidence: 60%

Section: Discussionmentioning

confidence: 99%

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A-Type and T-Type Currents Interact to Produce a Novel Spike Latency-Voltage Relationship in Cerebellar Stellate Cells

Molineux¹,

Fernandez²,

Mehaffey³

et al. 2005

J. Neurosci.

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“…One approach, to block individual currents pharmacologically (Byrne et al, 1979;Schwindt, 1992;Tierney and Harris-Warrick, 1992), often is limited by a lack of specific blockers. For example, in the R20 cells, no known blockers are completely selective for I Adepol or I K-V .…”

mentioning

confidence: 99%

The Role of K⁺Currents in Frequency-Dependent Spike Broadening inAplysiaR20 Neurons: A Dynamic-Clamp Analysis

Koester²

1996

J. Neurosci.

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The R20 neurons of Aplysia exhibit frequency-dependent spike broadening. Previously, we had used two-electrode voltage clamp to examine the mechanisms of this spike broadening (Ma and Koester, 1995). We identified three K ϩ currents that mediate action-potential repolarization: a transient A-type K ϩ current (I Adepol ), a delayed rectifier current (I K-V ), and a Ca 2ϩ -sensitive K ϩ current (I K-Ca ). A major constraint in that study was the lack of completely selective blockers for I Adepol and I K-V , resulting in an inability to assess directly the effects of their activation and inactivation on spike broadening. In the present study, the dynamic-clamp technique, which employs computer simulation to inject biologically realistic currents into a cell under current-clamp conditions (Sharp et al., 1993a,b), was used either to block I Adepol or I K-V or to modify their inactivation properties.The data in this paper, together with earlier results, lead to the following hypothesis for the mechanism of spike broadening in the R20 cells. As the spike train progresses, the primary responsibility for spike repolarization gradually shifts from I Adepol to I K-V to I K-Ca . This sequence can be explained on the basis of the relative rates of activation and inactivation of each current with respect to the constantly changing spike durations, the cumulative inactivation of I Adepol and I K-V , and the progressive potentiation of I K-Ca . Positive feedback interactions between spike broadening and inactivation contribute to the cumulative inactivation of both I Adepol and I K-V . The data also illustrate that when two or more currents have similar driving forces and partially overlapping activation characteristics, selectively blocking one current under current-clamp conditions can lead to a significant underestimate of its normal physiological importance.Key words: spike broadening; dynamic clamp; K ϩ current; I Adepol ; inactivation; Aplysia ; R20 Frequency-dependent spike broadening, an endogenously generated increase in spike duration that increases as a function of firing rate, has been shown in neurons from a variety of species to be correlated with enhanced transmitter release (Gillette et al., 1980;Coates and Bulloch, 1985) and to result primarily from inactivation of K ϩ currents (Aldrich et al., 1979a,b;Jackson et al., 1991;Bielefeldt et al., 1992;Crest and Gola, 1993;Quattrocki et al., 1994). Previously we had described the facilitatory synaptic effects and the mechanisms of frequency-dependent spike broadening in the two electrically coupled peptidergic R20 neurons of Aplysia (Ma and Koester, 1995). In addition, to analyze the mechanisms underlying spike broadening, several voltageactivated currents were isolated from the R20 cells by conventional voltage-clamp methods. These included a Na ϩ current (I Na ), a multi-component Ca 2ϩ current (I Ca ), and three K ϩ currents-a high-threshold transient A-type current (I Adepol ), a delayed rectifier current (I K-V ), and a two component Ca 2ϩ -sensitive K ϩ current...

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“…There are some examples, however, showing that the excitable membrane itself can be plastic in its response to excitation (1)(2)(3)(4)(5). As a prelude to genetic analysis of excitable membranes in Drosophila mlanogaster, physiological analysis of the dorsal longitudinal flight muscle (DLM) was undertaken.…”

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confidence: 99%

Facilitation of membrane electrical excitability in Drosophila.

Salkoff¹,

Wyman²

1980

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

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Prior electrical activity in the indirect flight muscles of Drosophila facilitates membrane excitability. The mechanism of facilitation involves the inactivation of an early, fast, transient outward current by prior membrane depolarization. In the facilitated state the ca cium-dependent spikelike response has a decreased current and voltage threshold. The facilitated state persists for 1.5 sec after a membrane active response. A single nerve-driven spike is sufficient to facilitate membrane excitability.Most known cases of changes in neural function with use depend on synaptic mechanisms. There are some examples, however, showing that the excitable membrane itself can be plastic in its response to excitation (1-5). As a prelude to genetic analysis of excitable membranes in Drosophila mlanogaster, physiological analysis of the dorsal longitudinal flight muscle (DLM) was undertaken. In the course of these studies we found striking changes in the excitability characteristics of the membrane, depending on prior use. For example, it was found that a single prior spike may evoke a large active membrane response to a stimulus that previously elicited no active response at all. The mechanism that is apparently responsible for these phenomena involves the inactivation of a transient inhibitory outward current similar to the "A" current first analyzed by Conner and Stevens (6) in molluscan neurons. METHODS AND MATERIALSAdult female D. melanogaster of wild-type strain Canton-S or the temperature-sensitive paralytic mutant stock shi(ts-1) were used in these experiments. Muscle membrane properties were found to be the same for these strains. In experiments requiring decreased transmitter release, the shi(ts-1) strain was used. The shi(ts-1) mutation confers a presynaptic temperature-sensitive defect that suppresses neurotransmitter release at temperatures higher than 290C (7,8). Thus, the use of this mutant together with appropriate temperature controls permits the experimental regulation of the size of the excitatory junction potentials (ejps). The techniques for evoking muscle responses via nerve stimulation are published (8).For recording and current injection, a single muscle fiber was impaled with two 3 M KCl-filled glass microelectrodes. Current was measured with a Ag-AgCl ground electrode by monitoring the voltage across a 10 kW resistor to ground. Flies were mounted so that the spiracles had access to air, and the dorsal thorax was opened and exposed to saline (128 mM NaCI/4.7 mM KCI/1.8 mM CaCI2/1.0 mM phosphate, pH 6.9). For experiments requiring low sodium and the complete removal of calcium, 1.4 mM [ethylenebis(oxyethylenenitrilo)]tetraacetic acid was added and NaCl was partially replaced with choline chloride (to 114 mM). Magnesium chloride (14 mM) was added for membrane stability. Muscle fibers had resting membrane potentials ranging from 60 to 90 mV. All fibers with resting potentials within this range showed the excitability changes described here. Within this range those with higher resting potentia...

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Biophysical mechanisms contributing to inking behavior in Aplysia

Cited by 52 publications

References 42 publications

A-Type and T-Type Currents Interact to Produce a Novel Spike Latency-Voltage Relationship in Cerebellar Stellate Cells

A-Type and T-Type Currents Interact to Produce a Novel Spike Latency-Voltage Relationship in Cerebellar Stellate Cells

The Role of K⁺Currents in Frequency-Dependent Spike Broadening inAplysiaR20 Neurons: A Dynamic-Clamp Analysis

Facilitation of membrane electrical excitability in Drosophila.

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Biophysical mechanisms contributing to inking behavior in Aplysia

Cited by 52 publications

References 42 publications

A-Type and T-Type Currents Interact to Produce a Novel Spike Latency-Voltage Relationship in Cerebellar Stellate Cells

A-Type and T-Type Currents Interact to Produce a Novel Spike Latency-Voltage Relationship in Cerebellar Stellate Cells

The Role of K+Currents in Frequency-Dependent Spike Broadening inAplysiaR20 Neurons: A Dynamic-Clamp Analysis

Facilitation of membrane electrical excitability in Drosophila.

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The Role of K⁺Currents in Frequency-Dependent Spike Broadening inAplysiaR20 Neurons: A Dynamic-Clamp Analysis