Microelectrode Study of the Resting and Action Potentials of the Cockroach Giant Axon with Special Reference to the Role Played by the Nerve Sheath

1967 ◽  
Vol 47 (2) ◽  
pp. 357-373
Author(s):  
Y. PICHON ◽  
J. BOISTEL

1. The use of very fine-tipped and mechanically strong microelectrodes has allowed reliable recordings of resting and action potentials to be made in cockroach giant axons in sheathed and desheathed nerve cords. 2. When the microelectrode was withdrawn from a giant axon in an intact connective the first positive change in the potential from the resting level, was in most cases followed by a negative deflexion to the original zero level, the ‘sheath potential’. The values of this ‘sheath potential’ together with the resting potential, the action potential, the maximum rate of rise and maximum rate of fall of the action potential have been measured in three different salines. 3. In normal saline, resting potentials were lower in sheathed preparations (58·1 ± 55·4 mV.) than in desheathed ones (67·4 ± 6·2 mV.), whereas action potentials were higher in the former (103±5·9 mV.) than in the latter (85·9±4·6 mV.). 4. Elevation of K+ and Ca2+ concentrations in the saline to the haemolymph level resulted in a decrease of resting and action potentials in desheathed cords, to 57·3±5·3 mV. and 36·5±7·6 mV. respectively. No alterations in the membrane potentials were recorded in intact connectives bathed in this saline, the mean resting potential being 55·6±4·2 mV. and the mean action potential 107·9±6·0 mV. Local desheathing of the nerve cord led only to local disturbance of the resting and action potentials, thus indicating that diffusion processes along the extracellular spaces were very slow. 5. The use of a saline in which cation concentrations have been elevated to the extracellular level resulted in normal resting potentials (64·6±3·3 mV.) and action potentials (90·9±7·2 mV.) in desheathed cords, despite the relatively high potassium concentration (17·1 mM./l.). 6. Recordings of the maximum rates of rise and rates of fall showed that there was no significant modification in the shape of the action potential in these different experimental conditions. 7. The values of the ‘sheath potential’ were very variable from one impalement to another and it is suggested that this potential might be related to variations of the microelectrode tip potential bathed in different ionic solutions. 8. The low resting potentials and high action potentials of giant axons in intact nerve cords may result from an excess of inorganic cations in the extracellular fluid.

1968 ◽  
Vol 49 (1) ◽  
pp. 31-38
Author(s):  
Y. PICHON ◽  
J. BOISTEL

1. Resting and action potentials have been recorded in giant axons of the cockroach when the intact nerve cord was bathed in the insect's own haemolymph. 2. Low resting potentials (43.0±4.8 mV.) and large action potentials (105.1±6.8 mV.) were obtained in these preparations as compared with those recorded in de-sheathed nerve cords. 3. Recordings of the maximum rates of rise and fall have shown that the shape of the action potential was essentially similar in de-sheathed preparations and in intact nerve cords. 4. These results have been discussed in terms of the unequal distribution of ions between the haemolymph, the extracellular fluid and the axoplasm of the giant axons. 5. The low measured resting potential agrees with a K+ concentration in the haemolymph of about 20 mM./l., a value which is only slightly lower than the measured one (Pichon, 1963). 6.The occurrence of large action potentials in these apparently depolarized axons may be related to the stabilizing action of divalent cations such as Ca2+ which are contained in the extracellular fluid in relatively large amounts. 7. The very large recorded overshoots (62.1±7.0 mV.) may be linked with a low sodium concentration in the axoplasm and a high sodium concentration in the extracellular fluid of the giant axons of intact nerve cords, thus resulting in a high sodium equilibrium potential, ENa.


1995 ◽  
Vol 74 (2) ◽  
pp. 673-683 ◽  
Author(s):  
A. A. Oyelese ◽  
D. L. Eng ◽  
G. B. Richerson ◽  
J. D. Kocsis

1. The effects of axotomy on the electrophysiologic properties of adult rat dorsal root ganglion (DRG) neurons were studied to understand the changes in excitability induced by traumatic nerve injury. Nerve injury was induced in vivo by sciatic nerve ligation with distal nerve transection. Two to four weeks after nerve ligation, a time when a neuroma forms, lumbar (L4 and L5) DRG neurons were removed and placed in short-term tissue culture. Whole cell patch-clamp recordings were made 5–24 h after plating. 2. DRG neurons were grouped into large (43–65 microns)-, medium (34–42 microns)-, and small (20–32 microns)- sized classes. Large neurons had short duration action potentials with approximately 60% having inflections on the falling phase of their action potentials. In contrast, action potentials of medium and small neurons were longer in duration and approximately 68% had inflections. 3. Pressure microejection of gamma-aminobutyric acid (GABA, 100 microM) or muscimol (100 microM) onto voltage-clamped DRG neurons elicited a rapidly desensitizing inward current that was blocked by 200 microM bicuculline. To measure the peak conductance induced by GABA or muscimol, neurons were voltage-clamped at a holding potential of -60 mV, and pulses to -80 mV and -100 mV were applied at a rate of 2.5 or 5 Hz during drug application. Slope conductances were calculated from plots of whole cell current measured at each of these potentials. 4. GABA-induced currents and conductances of control DRG neurons increased progressively with cell diameter. The mean GABA conductance was 36 +/- 10 nS (mean +/- SE) in small neurons, 124 +/- 21 nS in medium neurons, and 527 +/- 65 nS in large neurons. 5. After axotomy, medium neurons had significantly larger GABA-induced conductances compared with medium control neurons (390 +/- 50 vs. 124 +/- 21; P < 0.001). The increase in GABA conductance of medium neurons was associated with a decrease in duration of action potentials. In contrast, small neurons had no change in GABA conductance or action potential duration after ligation. The GABA conductance of large control neurons was highly variable, and ligation resulted in an increase that was significant only for neurons > 50 microns. The mean action potential duration in large neurons was not significantly changed, but neurons with inflections on the falling phase of the action potential were less common after ligation. There was no difference in resting potential or input resistance between control and ligated groups, except that the resting potential was less negative in small cells after axotomy.(ABSTRACT TRUNCATED AT 400 WORDS)


1984 ◽  
Vol 62 (5) ◽  
pp. 596-599
Author(s):  
Julio Alvarez ◽  
Francisco Dorticós ◽  
Jesús Morlans

Experiments were performed to study the effects of hypoxia on the characteristics of premature action potentials of rabbit papillary muscles. At normal resting potential, the duration of the premature action potential at the shortest coupling intervals was always greater than that of the control response. As the coupling interval was increased beyond 150 ms, the duration of the premature action potential regained control values. In cells depolarized to −70 mV by KCl, early lengthening of the premature response was attenuated. After 60 min of hypoxia, recovery of action potential duration at normal and reduced resting potentials was accelerated. The maximum rate of depolarization and its reactivation time constant were not affected by 60 min of hypoxia. It is suggested that intracellular free Ca is important in the control of action potential duration via the outward background potassium current.


1992 ◽  
Vol 70 (9) ◽  
pp. 1236-1246 ◽  
Author(s):  
Jean Marc Renaud ◽  
Peter Light

The effects of increasing the extracellular K+ concentration on the capacity to generate action potentials and to contract were tested on unfatigued muscle fibers isolated from frog sartorius muscle. The goal of this study was to investigate further the role of K+ in muscle fatigue by testing whether an increased extracellular K+ concentration in unfatigued muscle fibers causes a decrease in force similar to the decrease observed during fatigue. Resting and action potentials were measured with conventional microelectrodes. Twitch and tetanic force was elicited by field stimulation. At pHo (extracellular pH) 7.8 and 3 mmol K+∙L−1 (control), the mean resting potential was −86.6 ± 1.7 mV (mean ± SEM) and the mean overshoot of the action potential was 5.6 ± 2.5 mV. An increased K+ concentration from 3 to 8.0 mmol∙L−1 depolarized the sarcolemma to −72.2 ± 1.4 mV, abolished the overshoot as the peak potential during an action potential was −12.0 ± 3.9 mV, potentiated the twitch force by 48.0 ± 5.7%, but did not affect the tetanic force (maximum force) and the ability to maintain a constant force during the plateau phase of a tetanus. An increase to 10 mmol K+∙L−1 depolarized the sarcolemma to −70.1 ± 1.7 mV and caused large decreases in twitch (31.6 ± 26.1%) and tetanic (74.6 ± 12.1%) force. Between 3 and 9 mmol K+∙L−1, the effects of K+ at pHo 7.2 (a pHo mimicking the change in interstitial pH during fatigue) and 6.4 (a pHo known to inhibit force recovery following fatigue) on resting and action potentials as well as on the twitch and tetanic force were similar to those at pHo 7.8. Above 9 mmol K+∙L−1 significant differences were found in the effect of K+ between pHo 7.8 and 7.2 or 6.4. In general, the decrease in peak action potential and twitch and tetanic force occurred at higher K+ concentrations as the pHo was more acidic. The results obtained in this study do not support the hypothesis that an accumulation of K+ at the surface of the sarcolemma is sufficiently large to suppress force development during fatigue. The possibility that the K+ concentration in the T tubules reaches the critical K+ concentration necessary to cause a failure of the excitation–contraction coupling mechanism is discussed.Key words: excitation–contraction coupling, fatigue, potassium, tetanus, twitch.


1956 ◽  
Vol 187 (2) ◽  
pp. 338-340 ◽  
Author(s):  
J. Walter Woodbury ◽  
Donald M. McIntyre

For the first time overshooting action potentials of pregnant guinea pig uterus have been recorded intracellularly. Flexibly mounted ultramicroelectrodes were used. The largest action potential (AP) seen was 48 mv with an associated resting potential (RP) of 38 mv. The mean of 129 measurements of RP in four guinea pigs was 32.6 mv. The mean of 86 AP's was 21.9 mv. Although overshoot was seen only occasionally, the action potentials were always of the same order of magnitude as the resting potentials. It seems probable that the excitable mechanisms of uterine muscle though labile and variable are closely similar to those of other tissues.


1977 ◽  
Vol 232 (1) ◽  
pp. 23-29 ◽  
Author(s):  
M. Westerfield ◽  
J. W. Moore ◽  
Y. S. Kim ◽  
G. M. Padilla

Partially purified toxin(s), GbTX, extracted from Gymnodinium breve red tide organisms elicits a spontaneous train of action potentials in the squid giant axon. The spikes have a shape similar to that in the normal seawater control except for an increase in the rate of recovery from the afterhyperpolarization. With this more rapid recovery, the membrane potential overshoots the resting potential and threshold, triggers another spike, and thus produces repetitive firing. Voltage-clamp studies revealed that the toxin has no effect on the normal sodium or potassium conductance changes produced by step depolarization. However, consistent with the faster recovery after an action potential, GbTX speeds recovery of the “shut-off” currents to their steady-state values after a depolarization. The most likely mechanism by which the toxin accelerates recovery after an action potential (leading to repetitive firing) is the induction of a small additional inward current which was found to be reduced by prehyperpolarization. This toxin-induced current which speeds recovery is blocked by tetrodotoxin and hence presumably flows through the sodium channel.


1956 ◽  
Vol 40 (1) ◽  
pp. 1-17 ◽  
Author(s):  
F. H. Shaw ◽  
Shirley E. Simon ◽  
B. M. Johnstone

The sartorius muscles of 320 toads have been analyzed for Na+ and K+. There is a wide variation in the Na+ content which when calculated intracellularly varied from 0 m.eq./kg. to 58 m.eq./kg. In particular it was found that the distribution of internal Na+ in the intact animal was such that only 17 per cent of the muscles should give from the Nernst equation the observed overshoot of 37 mv. In contrast to this wide variation the K+ content is comparatively constant, the range being 71 to 112 m.eq./kg. The mean observed resting potential of 87 mv. agreed well with the potential calculated from the mean intracellular K+ by the Nernst equation. Analyses of plasma show that the Na+ content is constant at 130 m.eq./liter, and the K+ is 3.0 m.eq./liter. The resting and action potentials of 77 muscles have been recorded and then the muscles have been analyzed. The results have shown that there is no correlation between the level of intracellular Na+ and the overshoot. Furthermore the apparent correlation between the average K+ content and the average resting potential has been shown to be fortuitous, when the correlation in individual muscles is considered. When a muscle is soaked in Ringer solution for several hours there is a gain of Na+ and a loss of K+. These shifts should result in changes in the respective potentials, but such changes were not found. The above findings have been discussed in the light of the present theories that the resting potential and the action potential are directly related to the ionic ratio across the membrane. Our results very definitely do not support the theory that the overshoot is related to the Na+ gradient, and this also applies with respect to the K+ gradient and the resting potential.


1980 ◽  
Vol 58 (4) ◽  
pp. 549-552 ◽  
Author(s):  
S. Donaldson ◽  
G. O. Mackie ◽  
A. Roberts

Aglantha can swim in two ways, one of which, fast swimming, is evoked by contact with predators and serves for escape. The response consists of two or three violent contractions of which the first propels the animal a distance equivalent to five body lengths. Peak velocities in the range 0.3–0.4 m s−1 were measured. Drag is reduced by contraction of the tentacles.Coordination of escape swimming and tentacle contraction is achieved by a system of giant axons. A giant axon runs down each tentacle; action potentials in these elements show a one-for-one correspondence with potentials recorded from a ring-shaped axon lying in the margin near the tentacle bases. The ring giant synapses with eight motor giants which run up the subumbrella innervating the swimming muscles.Conduction velocities in the giant axons may be as high as 4.0 m s−1 in the case of the largest (40 μm diameter) axons. A value of 1.6 ms was obtained for minimum synaptic delay between the ring and motor giant axons.


1974 ◽  
Vol 60 (3) ◽  
pp. 653-671
Author(s):  
D. B. SATTELLE

1. A mean resting potential of -53.3 (S.D. ±2.7) mV has been obtained for 23 neurones of the parietal and visceral ganglia of Limnaea stagnalis (L.). Changes in the resting potential of between 28 and 43 mV accompany tenfold changes in [K+0]. A modified constant-field equation accounts for the behaviour of most cells over the range of external potassium concentrations from 0-5 to 10.o mM/1. Mean values have been estimated for [K+1, 56.2 (S.D.± 9-0) mM/1 and PNa/PK, 0-117 (S.D.±0-028). 2. Investigations on the ionic basis of action potential generation have revealed two cell types which can be distinguished according to the behaviour of their action potentials in sodium-free Ringer. Sodium-sensitive cells are unable to support action potentials for more than 8-10 min in the absence of sodium. Sodium slopes of between 29 and 37 mV per decade change in [Na+0] have been found for these cells. Tetrodotoxin (5 x 10-5 M) usually blocks action potentials in these neurones. Calcium-free inger produces a marked reduction in the overshoot potential and calcium slopes of about 18 mV per decade change in [Ca2+o] are found. Manganous chloride only partially reduces the action potential overshoot in these cells at concentrations of 10 mM/l. 3. Sodium-insensitive neurones maintain action potentials in the absence of external sodium. Stimulation only slightly reduces the amplitude of the action potential under these conditions and such cells are readily accessible to potassium ions in the bathing medium. A calcium-slope of 29 mV per decade change in [Ca2+o] has been observed in these cells in the absence of external sodium. 4. It is concluded that both sodium and calcium ions can be involved in the generation of the action potential in neurones of Limnaea stagnate, their relative contribution varying in different cells.


2001 ◽  
Vol 86 (6) ◽  
pp. 2998-3010 ◽  
Author(s):  
Nace L. Golding ◽  
William L. Kath ◽  
Nelson Spruston

In hippocampal CA1 pyramidal neurons, action potentials are typically initiated in the axon and backpropagate into the dendrites, shaping the integration of synaptic activity and influencing the induction of synaptic plasticity. Despite previous reports describing action-potential propagation in the proximal apical dendrites, the extent to which action potentials invade the distal dendrites of CA1 pyramidal neurons remains controversial. Using paired somatic and dendritic whole cell recordings, we find that in the dendrites proximal to 280 μm from the soma, single backpropagating action potentials exhibit <50% attenuation from their amplitude in the soma. However, in dendritic recordings distal to 300 μm from the soma, action potentials in most cells backpropagated either strongly (26–42% attenuation; n = 9/20) or weakly (71–87% attenuation; n = 10/20) with only one cell exhibiting an intermediate value (45% attenuation). In experiments combining dual somatic and dendritic whole cell recordings with calcium imaging, the amount of calcium influx triggered by backpropagating action potentials was correlated with the extent of action-potential invasion of the distal dendrites. Quantitative morphometric analyses revealed that the dichotomy in action-potential backpropagation occurred in the presence of only subtle differences in either the diameter of the primary apical dendrite or branching pattern. In addition, action-potential backpropagation was not dependent on a number of electrophysiological parameters (input resistance, resting potential, voltage sensitivity of dendritic spike amplitude). There was, however, a striking correlation of the shape of the action potential at the soma with its amplitude in the dendrite; larger, faster-rising, and narrower somatic action potentials exhibited more attenuation in the distal dendrites (300–410 μm from the soma). Simple compartmental models of CA1 pyramidal neurons revealed that a dichotomy in action-potential backpropagation could be generated in response to subtle manipulations of the distribution of either sodium or potassium channels in the dendrites. Backpropagation efficacy could also be influenced by local alterations in dendritic side branches, but these effects were highly sensitive to model parameters. Based on these findings, we hypothesize that the observed dichotomy in dendritic action-potential amplitude is conferred primarily by differences in the distribution, density, or modulatory state of voltage-gated channels along the somatodendritic axis.


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