The Effects of External Potassium and Long Duration Voltage Conditioning on the Amplitude of Sodium Currents in the Giant Axon of the Squid, <i>Loligo pealei </i>

Adelman, William J.; Palti, Yoram

doi:10.1085/jgp.54.5.589

Cited by 162 publications

(83 citation statements)

References 8 publications

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“…"Slow" inactivation of Na ϩ channels has been described previously in several neuronal preparations (Narahashi, 1964;Adelman and Palti, 1969;Chandler and Meves, 1970;Schauf et al, 1976;Rudy, 1978Rudy, , 1981Belluzi and Sacchi, 1986;Ogata et al, 1990;Ruben et al, 1992;Colbert and Johnston, 1996b;Fleidervish et al, 1996). In some cases the rates of both inactivation and recovery are comparably slow, whereas in other cases, as we describe here, entry into the slow inactivated state is faster than recovery from this state.…”

Section: Discussionsupporting

confidence: 73%

Prolonged Sodium Channel Inactivation Contributes to Dendritic Action Potential Attenuation in Hippocampal Pyramidal Neurons

1997

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During low-frequency firing, action potentials actively invade the dendrites of CA1 pyramidal neurons. At higher firing rates, however, activity-dependent processes result in the attenuation of back-propagating action potentials, and propagation failures occur at some dendritic branch points. We tested two major hypotheses related to this activity-dependent attenuation of back-propagating action potentials: (1) that it is mediated by a prolonged form of sodium channel inactivation and (2) that it is mediated by a persistent dendritic shunt activated by backpropagating action potentials. We found no evidence for a persistent shunt, but we did find that cumulative, prolonged inactivation of sodium channels develops during repetitive action potential firing. This inactivation is significant after a single action potential and continues to develop during several action potentials thereafter, until a steady-state sodium current is established. Recovery from this form of inactivation is much slower than its induction, but recovery can be accelerated by hyperpolarization. The similarity of these properties to the time and voltage dependence of attenuation and recovery of dendritic action potentials suggests that dendritic sodium channel inactivation contributes to the activity dependence of action potential back-propagation in CA1 neurons. Hence, the biophysical properties of dendritic sodium channels will be important determinants of action potential-mediated effects on synaptic integration and plasticity in hippocampal neurons. Key words: dendrite; action potential; sodium channels; synaptic integration; pyramidal neuron; activity dependentRecent experiments using simultaneous somatic and dendritic patch-pipette recordings have shown that action potentials are normally initiated in the axon and back-propagate into the dendrites of many types of C NS neurons (for review, see Stuart et al., 1997). These back-propagating action potentials are likely to provide an important spatial signal that influences ongoing synaptic integration and allows for postsynaptic firing in the axon to be associated with presynaptic activity. For example, the induction of activity-dependent changes in synaptic strength such as long-term potentiation (LTP) and long-term depression depend critically on the timing of pre-and postsynaptic inputs (Levy and Steward, 1983;Markram et al., 1997), and one form of LTP has been shown to be blocked by preventing action potentials from back-propagating into the dendrites of hippocampal pyramidal neurons (Magee and Johnston, 1997). These findings demonstrate the importance of understanding the factors that determine the extent and pattern of action potential back-propagation in pyramidal neuron dendrites.Action potential back-propagation in CA1 dendrites is complex. At low frequencies action potentials invade most of the dendritic tree in an active fashion, whereas at higher frequencies action potentials attenuate more and may fail to actively propagate into much of the dendritic tree (C allaway and Ross,...

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Section: Discussionsupporting

confidence: 73%

Prolonged Sodium Channel Inactivation Contributes to Dendritic Action Potential Attenuation in Hippocampal Pyramidal Neurons

1997

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“…The slow inactivation process, like the fast inactivation process, also attenuates the sodium conductance but with a much longer time constant (Adelman and Palti, 1969 ;Chandler and Meves, 1970;Schauf et al, 1976). Pronase and NBA do not remarkably alter slow inactivation after removing fast sodium inactivation (Rojas and Rudy, 1976 ;Oxford et al, 1978).…”

Section: Resultsmentioning

confidence: 96%

Removal of sodium channel inactivation in squid axon by the oxidant chloramine-T.

Wang¹,

Brodwick²,

Eaton³

1985

The Journal of General Physiology

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We have investigated the effects of a mild oxidant, chloramine-T (CT), on the sodium and potassium currents of squid axons under voltageclamp conditions. Sodium channel inactivation of squid giant axons can be completely removed by CT at neutral pH. Internal and external CT treatment are both effective. CT apparently removes inactivation in an irreversible, allor-none manner . The activation process of sodium channels is little affected, as judged from the voltage dependence of peak sodium currents, the rising phase of sodium currents, and the time course of tail currents following the repolarization . The removal of inactivation by CT is pH-dependent ; higher pH decreases the removal rate, whereas lower pH increases it. Internal metabisulfite, a strong reductant, does not protect inactivation from the action of external CT, nor does external metabisulfite protect from internal CT application. CT slightly depresses the peak potassium currents at comparable concentrations but has no apparent effects on their kinetics . Our results suggest that the neutral form of CT modifies an embedded methionine residue that is involved in sodium channel inactivation .

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“…The decline was strongest with the largest depolarization and was insignificant in the control measurements with TTX. It probably arose from a slow inactivation of the sodium channels (Adelman & Palti, 1969;Peganov, Khodorov & Shishkova, 1973). If Na channels can assume only one level of non-zero conductance, a parallel variation with time of the Na current and the variance indicates that the slow inactivation process does not affect this open-channel conductance.…”

Section: Conductance Fluctuations In Frog Nodesmentioning

confidence: 99%

Conductance fluctuations from the inactivation process of sodium channels in myelinated nerve fibres*

Conti

Neumcke

Nonner

et al. 1980

The Journal of Physiology

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SUMMARY1. Na currents and fluctuations of Na currents were studied under voltage clamp in the same myelinated nerve fibres of Rana esculenta at 13 'C. The results were used to test several kinetic models for the gating process of Na channels.2. Long voltage pulses, depolarizing the membrane by 16-48 mV from a hyperpolarizing holding level of -28 mV, were applied in 4 sec intervals. The d.c. and a.c. components of the membrane current were recorded during the last 328 msec of the 473 msec pulses. For each depolarization, ninety-six trials were made with the node in Ringer solution and, again, after adding 300 nM-tetrodotoxin (TTX) in that solution.3. The TTX-sensitive d.c. component declined during the 328 msec records by 14-51 % of its time average. The a.c. component was corrected for this trend by subtracting the first from the second of each pair of subsequent records. The TTXsensitive part of its variance declined, on the average, in parallel to the current, as if the open probability rather than the conductance of the individual Na channels was reduced by a slow process.4. Single-channel conductances, y/, were calculated on the assumption that Na channels have only one non-zero conductance and were corrected for the limited band width (5 kHz) of the a.c. records. Values of y increased slightly ( < 30 % from 16 to 40 mV), and averaged 8-85 + 0-7 pS (s.E. of mean, seventeen measurements on ten fibres). This small degree of change in y suggests that deviations from the all-ornone gating are very small. 5. Power spectral densities of the fluctuations between 3 Hz and 5 kHz were calculated from the trend-free a.c. records and corrected for the TTX-insensitive noise component. Control calculations showed that the only effect of the nonstationarity in the Na current was to enhance the low-frequency points of such spectra by less than 10 %. The spectra revealed at least two Lorentzian components with cut-off frequencies in the range expected from the activation and inactivation kinetics. The low-frequency component became dominant as depolarization was increased. F. CONTI, B. NEUMCKE, TV. NONNER AND R. STAMPFLI 6. Na currents recorded during brief (< 40 msec) depolarizations were analysed in terms of various all-or-none gating models, in which inactivation either was independent of activation (Hodgkin-Huxley (HH) model) or could occur only from the partly or fully activated states (coupled models). The transient Na currents were reproduced by all models.7. With the parameters from such fits, the fluctuation spectra expected for each model were calculated. The predictions differed in the fraction, rh, of the variance contributed by the slow (inactivation) fluctuations; rh was larger in the coupled models than in the HH model.8. The experimental spectra were divided into two spectral components to yield empirical values for rh. We used as templates the spectral curves derived for the fast and for the slow fluctuations of the HH model. The empirical rh values were one (48 mV) to four (16 mV) times larger than those e...

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The Effects of External Potassium and Long Duration Voltage Conditioning on the Amplitude of Sodium Currents in the Giant Axon of the Squid, Loligo pealei

Cited by 162 publications

References 8 publications

Prolonged Sodium Channel Inactivation Contributes to Dendritic Action Potential Attenuation in Hippocampal Pyramidal Neurons

Prolonged Sodium Channel Inactivation Contributes to Dendritic Action Potential Attenuation in Hippocampal Pyramidal Neurons

Removal of sodium channel inactivation in squid axon by the oxidant chloramine-T.

Conductance fluctuations from the inactivation process of sodium channels in myelinated nerve fibres*

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