Central circuitry in the jellyfish Aglantha digitale. III. The rootlet and pacemaker systems

2000 ◽  
Vol 203 (12) ◽  
pp. 1797-1807 ◽  
Author(s):  
G.O. Mackie ◽  
R.W. Meech
Keyword(s):  
Neuromuscular Junctions ◽  
Close Contact ◽  
Distinct Type ◽  
Giant Axon ◽  
Nerve Ring ◽  
Excitatory Postsynaptic Potential ◽  
Interconnected System ◽  
Giant Axons ◽  
Secondary Consequence ◽  
Stimulation Of

Tactile stimulation of the subumbrella of Aglantha digitale was found to evoke an escape swimming response similar to that evoked by stimulation of the outer surfaces of the margin but that does not involve the ring giant axon. Evidence is presented that conduction around the margin takes place via an interconnected system of rootlet interneurones. Confocal microscopy of carboxyfluorescein-filled axons showed that the rootlet neurones run out from the bases of the motor giant axons within the inner nerve ring and come into close contact with those of the neighbouring motor giant axons on either side. Transmission between the rootlet neurones has the properties of chemical synaptic transmission. A distinct type of fast excitatory postsynaptic potential (rootlet PSP) was recorded in motor giant axons following stimulation of nearby axons in 3–5 mmol l(−)(1) Mn(2+), which lowered the PSP below spike threshold. Immune labelling with anti-syntaxin 1 showed structures tentatively identified as synapses in the inner nerve ring, including some on the rootlet neurones. Neuromuscular junctions were not labelled. A secondary consequence of stimulating motor giant axons was the triggering of events in the pacemaker system. Triggering was blocked in 105 mmol l(−)(1) Mg(2+), indicating a synaptic link. Activity in the pacemaker system led indirectly to tentacle contractions (as described in earlier papers in this series), but the contractions were not as sudden or as violent as those seen when escape swimming was mediated by the ring giant axon. Events triggered in the pacemaker system fed back into the motor giants, producing postsynaptic potentials that appeared as humps in the spike after-potential. The conduction velocity of events propagating in the relay system was increased when the rootlet pathway was simultaneously excited (piggyback effect). With the addition of the rootlet pathway, the number of identified systems concerned with locomotion, feeding and tentacle contractions comes to fourteen, and the list is probably nearly complete.

Synaptic potentials and threshold currents underlying spike production in motor giant axons of Aglantha digitale

1995 ◽  
Vol 74 (4) ◽  
pp. 1662-1670 ◽  
Author(s):  
R. W. Meech ◽  
G. O. Mackie
Keyword(s):  
Neuromuscular Junctions ◽  
Sodium Current ◽  
Giant Axon ◽  
Nerve Ring ◽  
Synaptic Delay ◽  
Similar Distribution ◽  
Axon Membrane ◽  
Postsynaptic Potentials ◽  
Giant Axons ◽  
Inward Currents

1. Motor giant axons that excite swimming muscles in the jelly-fish Aglantha digitale interface with units of the inner and outer nerve rings in the margin at the base of the bell. External recording electrodes were used to monitor electrical activity at different sites within the nerve ring while events in the motor giant axon were recorded with intracellular micropipettes placed within 100 microns of the synaptic area. In some experiments, 4- to 6-micron-diam patch pipettes were used to record in situ from ion channel clusters at different locations along the axon. 2. Independently propagating calcium and sodium spikes in the motor giant axon were found to arise from different excitatory postsynaptic potentials (EPSPs). Two separate inputs were identified; one EPSP class represented an input from the pacemaker system in the inner nerve ring, whereas another represented an input from the giant axon in the outer nerve ring. EPSPs from the two nerve rings had significantly different time courses and amplitudes. EPSPs from the ring giant axon reached a peak in little more than 1 ms, whereas EPSPs from the pacemaker system reached a maximum in approximately 7 ms. These slower EPSPs may be compound events composed of postsynaptic potentials from multiple synapses excited in series by the passage of the pacemaker neuron signal. 3. The threshold for the production of calcium spikes by the slow EPSPs of the pacemaker system (-51 +/- 2.2 mV, mean +/- SD; n = 5) corresponded well with the voltage at which a net inward “T”-type calcium current first appeared in recordings from axon membrane patches (-55 to -50 mV); the threshold for the initiation of the sodium spike by the fast EPSPs of the ring giant system (-32 +/- 1.2 mV, mean +/- SD; n = 6) corresponded well with the voltage at which a net inward sodium current first appeared (-35 to -30 mV). 4. Inward currents were rarely observed in membrane patches formed using pipettes with tips of < 1 micron OD. Even with 4-micron pipettes, patches of membrane were sometimes obtained with a channel population consisting exclusively of potassium channels; calcium and sodium currents were found in highly discrete areas (“hot spots”). Preliminary findings on the undersurface of the axon, which makes synaptic contact with the myoepithelium, are consistent with a similar distribution. 5. The pathway by which the ring giant excites the motor giant axon is not definitely known. The synaptic delay between the peak of the ring giant action potential (monitored externally) and the initial rise of the fast EPSP (1.64 +/- 0.15 ms, mean +/- SD; n = 21) would allow for transmission at two synapses, because single synaptic delays at neuromuscular junctions in Aglantha are approximately 0.7 ms at 12 degrees C. The mean synaptic delay at the slow EPSP synapse was 0.88 +/- 0.09 (SD) ms (n = 12). 6. The delay between the impulse in the ring giant axon and the subsequent excitation of the motor giant axon may permit the animal to withdraw its tentacles and so lower the drag that would otherwise reduce the effectiveness of any escape swim and might induce tentacle autotomy.

Neuromuscular transmission in the jellyfish Aglantha digitale

1985 ◽  
Vol 116 (1) ◽  
pp. 1-25 ◽  
Author(s):  
P. A. Kerfoot ◽  
G. O. Mackie ◽  
R. W. Meech ◽  
A. Roberts ◽  
C. L. Singla
Keyword(s):  
Dimensional Space ◽  
Thin Sheet ◽  
Current Source ◽  
Giant Axon ◽  
The Body ◽  
Two Dimensional ◽  
Bathing Medium ◽  
Giant Axons ◽  
Motor Neurones ◽  
Stimulation Of

In the jellyfish Aglantha digitale escape swimming is mediated by the nearly synchronous activity of eight giant motor axons which make direct synaptic contact with contractile myoepithelial cells on the under-surface of the body wall. The delay in transmission at these synapses was 0.7 +/− 0.1 ms (+/− S.D.;N = 6) at 12 degrees C as measured from intracellular records. Transmission depended on the presence of Ca2+ in the bathing medium. It was not blocked by increasing the level of Mg2+ to 127 mmol l-1. The myoepithelium is a thin sheet of electrically coupled cells and injection of current at one point was found to depolarize the surrounding cells. The potential change declined with distance from the current source as expected for two-dimensional current spread. The two-dimensional space constant (lambda) was 770 micron for current flow in the circular direction and 177 micron for radial flow. The internal resistance of the epithelium (178–201 omega cm) and the membrane time constant (5–10 ms) were direction independent. No propagated epithelial action potentials were observed. Spontaneous miniature synaptic potentials of similar amplitude and rise-time were recorded intracellularly at distances of up to 1 mm from the motor giant axon. Ultrastructural evidence confirms that neuro-myoepithelial synapses also occur away from the giant axons. It is likely that synaptic sites are widespread in the myoepithelium, probably associated with the lateral motor neurones as well as the giant axons. Local stimulation of lateral motor neurones generally produced contraction in distinct fields. We suppose that stimulation of a single motor giant axon excites a whole population of lateral motor neurones and hence a broad area of the myoepithelium.

Osmotic stimulation of Na(+)-K(+)-Cl- cotransport in squid giant axon is [Cl-]i dependent

1990 ◽  
Vol 258 (4) ◽  
pp. C749-C753 ◽  
Author(s):  
G. E. Breitwieser ◽  
A. A. Altamirano ◽  
J. M. Russell
Keyword(s):  
Giant Axon ◽  
Dose Dependence ◽  
Squid Giant Axon ◽  
Dependent Manner ◽  
Transport Activity ◽  
Concentration Dependent Manner ◽  
Giant Axons ◽  
Stepwise Increase ◽  
Osmotic Stimulation ◽  
Stimulation Of

The effects of increasing extracellular osmolality on unidirectional Cl- fluxes through the Na(+)-K(+)-Cl- cotransporter were studied in internally dialyzed squid giant axons. Hyperosmotic seawater stimulated bumetanide-sensitive Cl-influx at 150 mM intracellular Cl- concentration ([Cl-]i), whereas Cl- efflux was unaffected under comparable ionic conditions. Stimulation of bumetanide-sensitive Cl- influx was proportional to the increase in extracellular osmolality. Bumetanide-sensitive Cl- influx began to increase after a latency of approximately 20 min after a stepwise increase of extracellular osmolality and continued to increase for at least 70 min. The increased bumetanide-sensitive Cl- influx measured after 65 min of exposure to hyperosmotic external fluid was a function of the intracellular Cl- concentration; stimulation by hyperosmotic external fluids was observed at physiological [Cl-]i levels (greater than 100 mM) but not at lower [Cl-]i levels. Under both normo- and hyperosmotic conditions, intracellular Cl- inhibited Na(+)-K(+)-Cl- cotransport influx in a concentration-dependent manner. However, in hyperosmotic seawater, the dose dependence of inhibition by intracellular Cl- was shifted to higher [Cl-]i values. Therefore, we conclude that hyperosmotic extracellular fluids stimulate influx via the Na(+)-K(+)-Cl- cotransport by resetting the relation between [Cl-]i and transport activity.

scholarly journals Central circuitry in the jellyfish Aglantha. II: The ring giant and carrier systems

1995 ◽  
Vol 198 (11) ◽  
pp. 2271-2278 ◽  
Author(s):  
G Mackie ◽  
R Meech
Keyword(s):  
Conduction Velocity ◽  
Action Potentials ◽  
Giant Axon ◽  
Nerve Ring ◽  
Carrier System ◽  
Close Collaboration ◽  
Giant Axons ◽  
Dense Fluid ◽  
Conduction Velocities ◽  
Carrier Systems

1. The ring giant axon in the outer nerve ring of the jellyfish Aglantha digitale is a multinucleate syncytium 85 % of which is occupied by an electron-dense fluid-filled vacuole apparently in a Gibbs&shy;Donnan equilibrium with the surrounding band of cytoplasmic cortex. Micropipette recordings show small (-15 to -25 mV) and large (-62 to -66 mV) resting potentials. Low values, obtained with a high proportion of the micropipette penetrations, are assumed to be from the central vacuole; high values from the cytoplasmic cortex. Background electrical activity includes rhythmic oscillations and synaptic potentials representing hair cell input caused by vibration. 2. After the ring giant axon has been cut, propagating action potentials evoked by stimulation are conducted past the cut and re-enter the axon on the far side. The system responsible (the carrier system) through-conducts at a velocity approximately 25 % of that of the ring giant axon and is probably composed of small neurones running in parallel with it. Numerous small neurones are seen by electron microscopy, some making one-way and some two-way synapses with the ring giant. 3. Despite their different conduction velocities, the two systems normally appear to fire in synchrony and at the velocity of the ring giant axon. We suggest that, once initiated, ring giant spikes propagate rapidly around the margin, firing the carrier neurones through serial synapses and giving them, in effect, the same high conduction velocity. Initiation of ring giant spikes can, however, require input from the carrier system. The spikes are frequently seen to be mounted on slow positive potentials representing summed carrier postsynaptic potentials. 4. The carrier system fires one-for-one with the giant axons of the tentacles and may mediate impulse traffic between the latter and the ring giant axon. We suggest that the carrier system may also provide the pathways from the ring giant to the motor giant axons used in escape swimming. 5. The findings show that the ring giant axon functions in close collaboration with the carrier system, increasing the latter's effective conduction velocity, and that interactions with other neuronal sub-systems are probably mediated exclusively by the carrier system.

Modulation of spike frequency by regions of special axonal geometry and by synaptic inputs

1976 ◽  
Vol 39 (4) ◽  
pp. 882-899 ◽  
Author(s):  
M. E. Spira ◽  
Y. Yarom ◽  
I. Parnas
Keyword(s):  
Conduction Block ◽  
Membrane Conductance ◽  
Giant Axon ◽  
Membrane Resistance ◽  
High Frequency Stimulation ◽  
Extracellular Potassium ◽  
Synaptic Inputs ◽  
Giant Axons ◽  
Synaptic Potentials ◽  
Stimulation Of

1. Spike propagation across the nonhomogeneous section of the giant axon in ganglion T3 of the cockroach was analyzed by intracellular microelectrodes recording at the posterior and anterior ends of T3. Ascending and descending potentials were evoked by stimulation of A5-A6 and T2-T3 connectives. 2. At high frequencies, descending and ascending impulses exhibit the following: a) consecutive reduction in the spike amplitude, b) a decrease in the afterhyperpolarization; c) gradual appearance of a prepotential together with an increase in delay of spike initiation; d) failure of full spike invasion into the recording area, showing only a decremental potential. 3. The duration of a train required to block spike propagation when the whole connective is stimulated is much shorter (about 6 times) than that required when a single giant axon is stimulated. 4. The conduction block is associated with a marked decrease in effective membrane resistance, greater than that expected from depolarization and delayed rectification. 5. Synaptic potentials could be recorded in the giant axons in the caudal base of ganglion T3 after stimulation of either the ipsilateral or contralateral connectives at both ends of the ganglion. These synaptic potentials could be blocked by d-tubocurarine (d-TC) or low Ca2+-high Mg2+. 6. Activation of these synapses produces a marked increase in membrane conductance, blocking propagation of spike trains through the ganglion. 7. After these synapses are blocked by d-TC or low Ca2+-high Mg2+, high-frequency stimulation still produces a conduction block. 8. It seems that conduction of spike during repetitive stimulation is affected both by accumulation of extracellular potassium, which depolarizes the membrane and causes sodium inactivation, and by activation of synaptic inputs to shunt the membrane in this region. 8. Each of these two mechanisms by itself can produce conduction block along the giant axons in ganglion T3.

Preliminary observations on escape swimming and giant neurons in Aglantha digitale (Hydromedusae: Trachylina)

1980 ◽  
Vol 58 (4) ◽  
pp. 549-552 ◽  
Author(s):  
S. Donaldson ◽  
G. O. Mackie ◽  
A. Roberts
Keyword(s):  
Action Potentials ◽  
Giant Axon ◽  
Synaptic Delay ◽  
Giant Axons ◽  
A Value ◽  
Giant Synapses ◽  
Run Up

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.

Proportion of muscles spindles supplied by skeletofusimotor axons (beta-axons) in peroneus brevis muscle of the cat

1975 ◽  
Vol 38 (6) ◽  
pp. 1390-1394 ◽  
Author(s):  
F. Emonet-Denand ◽  
Y. Laporte
Keyword(s):  
Neuromuscular Junctions ◽  
Muscle Fibers ◽  
Repetitive Stimulation ◽  
Motor Axon ◽  
Dynamic Sensitivity ◽  
Conduction Velocities ◽  
Peroneus Brevis ◽  
Stimulation Of

Of 32 cat peroneus brevis spindles, 23 (72%) were found to be supplied by a least 1 skeletofusimotor or beta-axon. A motor axon was identified as skeletofusimotor when repetitive stimulation of it elicited both the contraction of extrafusal muscle fibers and as acceleration of the discharge of primary ending, which persisted after selective block of the neuromuscular junctions of extrafusal muscle fibers. The block was obtained by stimulating single axons at 400-500/s for a few seconds. Of 135 axons supplying extrafusal muscle fibers, 24 (18%) were shown to be beta-axons; 22 beta-axons had conduction velocities ranging from 45 to 75 m/s. All but three beta-axons increased the dynamic sensitivity of primary endings. Beta-innervated spindles may also be supplied by dynamic gamma-axons.

scholarly journals The "late" Ca channel in squid axons.

1981 ◽  
Vol 78 (6) ◽  
pp. 683-700 ◽  
Author(s):  
L J Mullins ◽  
J Requena
Keyword(s):  
Steady State ◽  
Repetitive Stimulation ◽  
Test Solution ◽  
Ca Channel ◽  
Normal Concentration ◽  
Giant Axons ◽  
Light Production ◽  
High K ◽  
K Response ◽  
Stimulation Of

Squid giant axons were injected with aequorin and then treated with seawater containing 50 mM Ca and 100-465 mM K+. Measurements of light production suggested a phasic entry of Ca as well as an enhanced steady-state aequorin glow. After a test K+ depolarization, the aequorin-injected axon was stimulated for 30 min in Li seawater that was Ca-free, a procedure known to reduce [Na]i to about one-half the normal concentration. Reapplication of the elevated K+ test solution now showed that the Ca entry was virtually abolished by this stimulation in Li. A subsequent stimulation of the axon in Na seawater for 30 min resulted in recovery of the response to depolarization by high K+ noted in a normal fresh axon. In axons first tested for a high K+ response and then stimulated in Na seawater for 30 min (where [Na]i increases approximately 30%), there was approximately eight fold enhancement in this response to a test polarization. Axons depolarized with 465 mM K seawater in the absence of external Ca for several minutes were still capable of producing a large phasic entry of Ca when [Ca]0 was made 50 mM, which suggests that it is Ca entry itself rather than membrane depolarization that produced inactivation. Responses to stimulation at 60 pulses/s in Na seawater containing 50 mM Ca are at best only 5% of those measured with high K solutions. The response to repetitive stimulation is not measurable if [Ca]o is made 1 mM, whereas the response to steady depolarization is scarcely affected.

Organization of the Giant Axons of the Cockroach Periplaneta Americana

1969 ◽  
Vol 50 (3) ◽  
pp. 615-627
Author(s):  
M. E. SPIRA ◽  
I. PARNAS ◽  
F. BERGMANN
Keyword(s):  
Nerve Cord ◽  
Periplaneta Americana ◽  
Thoracic Ganglion ◽  
American Cockroach ◽  
Abdominal Ganglion ◽  
Common Pathway ◽  
Average Delay ◽  
Giant Axons ◽  
Stimulation Of

1. Stimulation of the connectives between the suboesophageal and prothoracic ganglia of the American cockroach induced ipsilateral descending spikes in the abdominal giant axons with an average delay of 0·6 msec, per thoracic ganglion. 2. Nicotine at 5 µg./ml. had no effect on conduction in the abdomen but blocked ascending responses sequentially at the 6th abdominal ganglion then at the levels of T1; T2, and T3. 3. Simultaneous descending and ascending impulses resulted in mutual extinction along the nerve cord with the point of collision depending on the interval between stimuli. 4. It is suggested that a common pathway subserves ascending and descending giant impulses and models for bi-directional conduction are discussed.

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