Isolated Giant Smooth Muscle Fibres in Beroe Ovata: Ionic Dependence of Action Potentials Reveals Two Distinct Types of Fibre

1988 ◽  
Vol 135 (1) ◽  
pp. 343-362 ◽  
Author(s):  
ANDRÉ BILBAUT ◽  
ROBERT W. MEECH ◽  
MARI-LUZ HERNANDEZ-NICAISE

1. The ionic dependence of action potentials evoked in giant smooth muscle fibres isolated by enzymatic digestion from the body wall of the marine invertebrate Beroe ovata (Ctenophora) has been investigated using conventional electrophysiological techniques. 2. Differences were observed in the two fibre types studied. The resting membrane potential was −60 ± 1.35 mV (N = 25) in longitudinal muscle fibres and −66 ±1.37 mV (N=32) in radial fibres. Action potentials had a short plateau in longitudinal fibres but not in radial fibres. 3. The action potential overshoot of both fibre types was decreased in Ca2+-free artificial sea water (ASW). In Na+-deficient ASW, action potentials could not be generated in radial fibres and showed a reduced overshoot in longitudinal fibres. 4. Tetrodotoxin (10−5moll−5) added to ASW or Ca2+-free ASW did not affect the action potentials of either type of fibre. 5. Action potentials of both fibres were partially blocked by Co2+ (20–50 mmoll−1) or Cd2+ (l-2mmoll−1). Action potentials of longitudinal fibres in Na+-deficient ASW were abolished by Co2+ (20mmoll−1). In Ca2+-free ASW, the ction potential overshoots of both sets of fibres were restored following the addition of Sr2+ or Ba2+. In longitudinal fibres, Sr2+ increased the duration of the action potential plateau. In both longitudinal and radial muscle fibres, Ba2+ prolonged the action potential. 6. In longitudinal fibres exposed to tetraethylammonium chloride (TEAC1) or 4-aminopyridine (4AP), the action potential was slightly prolonged. In these fibres, TEA+ or 4AP added to Ca2+-free ASW induced only a long-lasting depolarizing plateau. In radial fibres, the action potential duration was slightly increased in the presence of TEA+; it was unaffected by 4AP. In Ca2+-free ASW, TEA+ and 4AP induced an oscillating membrane response which appeared to be dependent on the intensity of the injected current pulse. 7. It is concluded that (a) there are significant differences between the action potentials of longitudinal and radial muscle fibres but that both are dependent on Na+ and Ca2+, (b) in longitudinal fibres, a Ca2+-activated K+ conductance and a TEA+-sensitive voltage-activated K+ conductance contribute to the repolarizing phase of the action potential, the former being predominant, (c) in radial fibres, the repolarizing phase of action potentials probably involves different membrane K+ conductances among which is a TEA+-sensitive K+ conductance.

1958 ◽  
Vol 196 (1) ◽  
pp. 39-43 ◽  
Author(s):  
Seymour Katsh ◽  
Jean M. Marshall

Female guinea pigs were injected with antigen (homologous sperm or ovalbumin) and 14–28 days later ileal segments and both uterine horns were removed. The ileal segments and one of the uterine horns from each animal were tested for responses to drugs, as well as to nonspecific and specific antigen; responses were recorded by means of a kymograph and muscle lever. The contralateral cornua were tested with nonspecific and with specific antigen as well as with drugs; responses were detected and recorded with intracellular electrodes and a mechanotransducer. The notable findings relative to the electronic studies were: within 1–2 minutes following exposure of the sensitized uterus to specific antigen there occurred a) a diminution in resting membrane potential; b) a sudden burst of action potential spikes; c) a contraction of the musculature which was of greater amplitude and of longer duration than those of the spontaneous contractions; d) during the sustained contracture phase, the rate of discharge of action potential spikes was higher than that accompanying spontaneous contractions. After desensitization, specific antigen was without effect. No effect of nonspecific antigen was observed in any of the preparations. After stimulating with specific antigen or with drugs, additional action potentials arose before repolarization from the previous action potential was completed.


2001 ◽  
Vol 86 (2) ◽  
pp. 629-640 ◽  
Author(s):  
Muthukrishnan Renganathan ◽  
Theodore R. Cummins ◽  
Stephen G. Waxman

C-type dorsal root ganglion (DRG) neurons can generate tetrodotoxin-resistant (TTX-R) sodium-dependent action potentials. However, multiple sodium channels are expressed in these neurons, and the molecular identity of the TTX-R sodium channels that contribute to action potential production in these neurons has not been established. In this study, we used current-clamp recordings to compare action potential electrogenesis in Nav1.8 (+/+) and (−/−) small DRG neurons maintained for 2–8 h in vitro to examine the role of sodium channel Nav1.8 (α-SNS) in action potential electrogenesis. Although there was no significant difference in resting membrane potential, input resistance, current threshold, or voltage threshold in Nav1.8 (+/+) and (−/−) DRG neurons, there were significant differences in action potential electrogenesis. Most Nav1.8 (+/+) neurons generate all-or-none action potentials, whereas most of Nav1.8 (−/−) neurons produce smaller graded responses. The peak of the response was significantly reduced in Nav1.8 (−/−) neurons [31.5 ± 2.2 (SE) mV] compared with Nav1.8 (+/+) neurons (55.0 ± 4.3 mV). The maximum rise slope was 84.7 ± 11.2 mV/ms in Nav1.8 (+/+) neurons, significantly faster than in Nav1.8 (−/−) neurons where it was 47.2 ± 1.3 mV/ms. Calculations based on the action potential overshoot in Nav1.8 (+/+) and (−/−) neurons, following blockade of Ca2+ currents, indicate that Nav1.8 contributes a substantial fraction (80–90%) of the inward membrane current that flows during the rising phase of the action potential. We found that fast TTX-sensitive Na+ channels can produce all-or-none action potentials in some Nav1.8 (−/−) neurons but, presumably as a result of steady-state inactivation of these channels, electrogenesis in Nav1.8 (−/−) neurons is more sensitive to membrane depolarization than in Nav1.8 (+/+) neurons, and, in the absence of Nav1.8, is attenuated with even modest depolarization. These observations indicate that Nav1.8 contributes substantially to action potential electrogenesis in C-type DRG neurons.


1981 ◽  
Vol 93 (1) ◽  
pp. 257-267 ◽  
Author(s):  
FRANCES M. ASHCROFT

The ionic requirements for the generation of action potentials in the ventral longitudinal muscle fibres of the stick insect, Carausius morosus, were investigated. Ca-free Ringer rapidly and reversibly abolished the action potential. In the presence of tetraethylammonium (TEA) ions (to suppress outward currents) the overshoot of the action potential changed 26 mV for a 10-fold change in [Ca]o. The maximum rate of rise of the action potential (measured in TEA Ringer) showed saturation at high [Ca]o. Cobaltous ions (20 mM) and the organic Ca antagonist D 600 (5×10−4g/ml) reversibly inhibited the action potential; the inhibitory effect of 1 mM-La3+ was irreversible. Barium and strontium, but not magnesium, were able to substitute for calcium as charge carriers. These results suggest that an inward movement of Ca2+ underlies the action potential of Carausius fibres.


1994 ◽  
Vol 267 (5) ◽  
pp. G938-G946 ◽  
Author(s):  
F. Vogalis ◽  
R. R. Bywater ◽  
G. S. Taylor

The electrical basis of propulsive contractions in the guinea pig choledochoduodenal junction (CDJ), which are triggered by distension, was investigated using intracellular microelectrode recording techniques. The isolated CDJ was placed in a continuously perfused tissue chamber at 37 degrees C. Membrane potential was recorded from smooth muscle cells in either the ampulla or in the upper CDJ (upper junction) regions, which were immobilized by pinning. Distension of the upper junction (20-30 s) by increasing intraductal hydrostatic pressure (mean elevation: 2.0 +/- 0.3 kPa, n = 13) triggered "transient depolarizations" (TDs: < 5 mV in amplitude and 2-5 s in duration) and action potentials in the circular muscle layer of the ampulla. The frequency of TDs in the ampulla was increased from 2.2 +/- 0.2 to 15.9 +/- 2.2 min-1 (n = 13) during distension. Simultaneous impalements of cells in the longitudinal and circular muscle layers in the ampulla revealed that subthreshold TDs in the circular layer were associated with an increased rate of action potential discharge in the longitudinal layer. Atropine (Atr; 1.4 x 10(-6) M) and tetrodotoxin (TTX; 3.1 x 10(-6) M blocked the distension-evoked increase in TD frequency, without affecting the frequency of ongoing TDs. The sulfated octapeptide of cholecystokinin (1-5 x 10(-8) M) increased the amplitude of TDs recorded in the circular muscle layer of the ampulla and increased action potential discharge rate. In separate recordings, radial stretch of the ampulla region increased the rate of discharge of action potentials in the smooth muscle of the upper junction.(ABSTRACT TRUNCATED AT 250 WORDS)


1964 ◽  
Vol 206 (1) ◽  
pp. 205-210 ◽  
Author(s):  
Makoto Kobayashi ◽  
Hiroshi Irisawa

Action potentials of the smooth muscle of cat ureter were studied by using ultramicroelectrodes. Among 193 penetrations, the resting potential averaged 45 mv and the amplitude of action potential 32 mv. In four instances a slight overshoot was recorded. Action potential consisted of a relatively rapid rising phase followed by a slow repolarization phase, and its duration was about 0.3 sec. Effects of sodium deficiency on action potential were studied by using three different sodium substitutes. Both the height and the rising rate of action potential decreased as the concentration of extracellular sodium was reduced, indicating that the action potential of ureter muscle can be explained on the basis of sodium theory. The duration of the action potential was prolonged when sucrose or choline chloride was used as a sodium substitute; on the other hand, it shortened when tris chloride was employed. The essential role of sodium ions in the development of the action potential in ureter muscle is discussed.


1964 ◽  
Vol 47 (4) ◽  
pp. 719-733 ◽  
Author(s):  
W. H. Herzog ◽  
R. M. Feibel ◽  
S. H. Bryant

In the giant axon of Loligo pealii, "aconitine potent" Merck added to the bath (10-7 to 1.25 x 10-6 gm/ml) (a) had no effect on resting membrane potential, membrane resistance and rectification, membrane response to subthreshold currents, critical depolarization, or action potential, but (b) on repetitive stimulation produced oscillations of membrane potential after the spike, depolarization, and decrease of membrane resistance. The effect sums with successive action potentials; it increases with concentration of aconitine, time of exposure, and frequency of stimulation. When the oscillations are large enough and the membrane potential is 51.6 ± SD 1.5 mv a burst of self-sustained activity begins; it usually lasts 20 to 70 sec. and at its end the membrane potential is 41.5 ± SD 1.9 mv. Repolarization occurs with a time constant of 2.5 to 11.1 min. Substitution of choline for external sodium after a burst hyperpolarizes the membrane to -70 mv, and return to normal external sodium depolarizes again beyond the resting membrane potential. The effect of aconitine on the membrane is attributed to an increase of sodium and potassium or chloride conductances following the action potential.


2012 ◽  
Vol 2012 ◽  
pp. 1-6 ◽  
Author(s):  
Seong-Jin Cho ◽  
Sang-Hun Lee ◽  
Wenji Zhang ◽  
Sae-Bhom Lee ◽  
Kwang-Ho Choi ◽  
...  

We studied the action potential of Primo-vessels in rats to determine the electrophysiological characteristics of these structures. We introduced a mathematical analysis method, a normalized Fourier transform that displays the sine and cosine components separately, to compare the action potentials of Primo-vessels with those for the smooth muscle. We found that Primo-vessels generated two types of action potential pulses that differed from those of smooth muscle: (1) Type I pulse had rapid depolarizing and repolarizing phases, and (2) Type II pulse had a rapid depolarizing phase and a gradually slowing repolarizing phase.


2000 ◽  
Vol 279 (3) ◽  
pp. G622-G630 ◽  
Author(s):  
Jason M. Hemming ◽  
Fay A. Guarraci ◽  
Tracy A. Firth ◽  
Lee J. Jennings ◽  
Mark T. Nelson ◽  
...  

Histamine is an inflammatory mediator present in mast cells, which are abundant in the wall of the gallbladder. We examined the electrical properties of gallbladder smooth muscle and nerve associated with histamine-induced changes in gallbladder tone. Recordings were made from gallbladder smooth muscle and neurons, and responses to histamine and receptor subtype-specific compounds were tested. Histamine application to intact smooth muscle produced a concentration-dependent membrane depolarization and increased excitability. In the presence of the H2 antagonist ranitidine, the response to histamine was potentiated. Activation of H2 receptors caused membrane hyperpolarization and elimination of spontaneous action potentials. The H2response was attenuated by the ATP-sensitive K+(KATP) channel blocker glibenclamide in intact and isolated smooth muscle. Histamine had no effect on the resting membrane potential or excitability of gallbladder neurons. Furthermore, neither histamine nor the H3 agonist R-α-methylhistamine altered the amplitude of the fast excitatory postsynaptic potential in gallbladder ganglia. The mast cell degranulator compound 48/80 caused a smooth muscle depolarization that was inhibited by the H1 antagonist mepyramine, indicating that histamine released from mast cells can activate gallbladder smooth muscle. In conclusion, histamine released from mast cells can act on gallbladder smooth muscle, but not in ganglia. The depolarization and associated contraction of gallbladder smooth muscle represent the net effect of activation of both H1 (excitatory) and H2 (inhibitory) receptors, with the H2receptor-mediated response involving the activation of KATPchannels.


1991 ◽  
Vol 158 (1) ◽  
pp. 63-95 ◽  
Author(s):  
G. P. Ferguson ◽  
P. R. Benjamin

Two muscle systems mediated the whole-body withdrawal response of Lymnaea stagnalis: the columellar muscle (CM) and the dorsal longitudinal muscle (DLM). The CM was innervated by the columellar nerves and contracted longitudinally to shorten the ventral head-foot complex and to pull the shell forward and down over the body. The DLM was innervated by the superior and inferior cervical nerves and the left and right parietal nerves. During whole-body withdrawal, the DLM contracted synchronously with the CM and shortened the dorsal head-foot longitudinally. The CM and the DLM were innervated by a network of motoneurones. The somata of these cells were located in seven ganglia of the central nervous system (CNS), but were especially concentrated in the bilaterally symmetrical A clusters of the cerebral ganglia. The CM was innervated by cells in the cerebral and pedal ganglia and the DLM by cells in the cerebral, pedal, pleural and left parietal ganglia. Individual motoneurones innervated large, but discrete, areas of muscle, which often overlapped with those innervated by other motoneurones. Motoneuronal action potentials evoked one-for-one non-facilitating excitatory junction potentials within muscle fibres. No all-or-nothing action potentials were recorded in the CM or DLM, and they did not appear to be innervated by inhibitory motoneurones. The whole network of motoneurones was electrotonically coupled, with most cells on one side of the CNS strongly coupled to each other but weakly coupled to cells on the contralateral side of the CNS. This electrotonic coupling between motoneurones is probably important in producing synchronous contraction of the CM and DLM when the animal retracts its head-foot complex during whole-body withdrawal.


1958 ◽  
Vol 36 (9) ◽  
pp. 959-975 ◽  
Author(s):  
E. E. Daniel ◽  
H. Singh

In myometrium from pregnant cat, repetitive action potentials have been recorded during contraction. Using intracellular electrodes the depolarizations averaged 35 mv. Maximum rate of depolarization was 1–2 v/sec and the action potential duration varied from 250 milliseconds to much longer periods. Membrane reversal of up to 10 mv sometimes occurred. Total resistance decreased during depolarization and recovered during repolarization. Typical biphasic potentials were also recorded with extracellular electrodes. Their amplitude (peak to peak) varied from 0.3 to several millivolts and their duration (peak to peak) from 10–40 milliseconds. Reduction of external sodium concentration to as little as one-ninth normal (choline chloride or sucrose replacement) did not reduce the amplitudes of the resting or action potentials measured intracellularly or extracellularly, but decreased the action potential frequency. Membrane reversal still occurred with intracellular electrodes and the maximum rate of depolarization was unchanged. The rate of repolarization was increased so that the total duration of the action potential was 150 to 200 milliseconds. With extracellular electrodes, the peak to peak amplitudes were increased and the durations were unchanged. Further reduction of external sodium concentration to less than 15–20 meq/liter caused a contraction without further change in action potential configuration. Gradual relaxation and slowing of the repetition rate of action potentials occurred and resulted eventually in complete mechanical and electrical inactivity.Rabbit taenia coli were also studied and their electrical properties contrasted to those of cat myometrium. The conclusions were reached that: (1) the available evidence opposes the hypotheses that an inward sodium current accounts for depolarization in smooth muscle and (2) smooth muscles differed in their electrical properties and mechanisms of ion distribution not only from striate muscles but also from one another.


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