Electrical properties of the pacemaker neurons in the heart ganglion of a stomatopod, Squilla oratoria.

doi:10.1085/JGP.50.4.813

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Electrical properties of the pacemaker neurons in the heart ganglion of a stomatopod, Squilla oratoria.

Journal Article•DOI•

Electrical properties of the pacemaker neurons in the heart ganglion of a stomatopod, Squilla oratoria.

Akira Watanabe¹, Shosaku Obara¹, Toyohiro Akiyama¹, Katsuto Yumoto¹•Institutions (1)

Tokyo Medical and Dental University¹

01 Mar 1967-The Journal of General Physiology (The Rockefeller University Press)-Vol. 50, Iss: 4, pp 813-838

TL;DR: Comparison with action potentials caused by axonal stimulation and analysis of time relations indicate that with stronger currents the soma membrane is directly stimulated whereas with weaker currents the impulse first arises in the axon and then invades the Soma.

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Abstract: In the Squilla heart ganglion, the pacemaker is located in the rostral group of cells. After spontaneous firing ceased, the electrophysiological properties of these cells were examined with intracellular electrodes. Cells respond to electrical stimuli with all-or-none action potentials. Direct stimulation by strong currents decreases the size of action potentials. Comparison with action potentials caused by axonal stimulation and analysis of time relations indicate that with stronger currents the soma membrane is directly stimulated whereas with weaker currents the impulse first arises in the axon and then invades the soma. Spikes evoked in a neuron spread into all other neurons. Adjacent cells are interconnected by electrotonic connections. Histologically axons are tied with the side-junction. B spikes of adjacent cells are blocked simultaneously by hyperpolarization or by repetitive stimulation. Experiments show that under such circumstances the B spike is not directly elicited from the A spike but is evoked by invasion of an impulse or electrotonic potential from adjacent cells. On rostral stimulation a small prepotential precedes the main spike. It is interpreted as an action potential from dendrites.

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Journal Article•DOI•

Organization of the stomatogastric ganglion of the spiny lobster

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Brian Mulloney¹, Allen I. Selverston¹•Institutions (1)

University of California, San Diego¹

01 Mar 1974-Journal of Comparative Physiology A-neuroethology Sensory Neural and Behavioral Physiology

TL;DR: The Stomatogastric ganglion of Panulirus interruptus contains about 30 neurons, and controls the movements of the lobster's stomach, and a group of six neurons which drive the stomach's lateral teeth are described.

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Abstract: The Stomatogastric ganglion ofPanulirus interruptus contains about 30 neurons, and controls the movements of the lobster's stomach When experimentally isolated, the ganglion continues to generate complex rhythmic patterns of activity in its motor neurons which are similar to those seen in intact animals

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275 citations

Journal Article•DOI•

Reliable, responsive pacemaking and pattern generation with minimal cell numbers: the crustacean cardiac ganglion.

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Ian M. Cooke¹•Institutions (1)

University of Hawaii¹

01 Apr 2002-The Biological Bulletin

TL;DR: The continuing relevance of the crustacean cardiac ganglion as a relatively simple model for pacemaking and central pattern generation is confirmed by the rapidly widening documentation of intrinsic potentials such as plateau potentials in neurons of all major animal groups.

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Abstract: Investigations of the electrophysiology of crustacean cardiac ganglia over the last half-century are reviewed for their contributions to elucidating the cellular mechanisms and interactions by which a small (as few as nine cells) neuronal network accomplishes extremely reliable, rhythmical, patterned activation of muscular activity-in this case, beating of the neurogenic heart. This ganglion is thus a model for pacemaking and central pattern generation. Favorable anatomy has permitted voltage- and space-clamp analyses of voltage-dependent ionic currents that endow each neuron with the intrinsic ability to respond with rhythmical, patterned impulse activity to nonpatterned stimulation. The crustacean soma and initial axon segment do not support impulse generation but integrate input from stretch-sensitive dendrites and electrotonic and chemically mediated synapses on axonal processes in neuropils. The soma and initial axon produce a depolarization-activated, calcium-mediated, sustained potential, the "driver potential," so-called because it drives a train of impulses at the "trigger zone" of the axon. Extreme reliability results from redundancy and the electrotonic coupling and synaptic interaction among all the neurons. Complex modulation by central nervous system inputs and by neurohormones to adjust heart pumping to physiological demands has long been demonstrated, but much remains to be learned about the cellular and molecular mechanisms of action. The continuing relevance of the crustacean cardiac ganglion as a relatively simple model for pacemaking and central pattern generation is confirmed by the rapidly widening documentation of intrinsic potentials such as plateau potentials in neurons of all major animal groups. The suite of ionic currents (a slowly inactivating calcium current and various potassium currents, with variations) observed for the crustacean cardiac ganglion have been implicated in or proven to underlie a majority of the intrinsic potentials of neurons involved in pattern generation.

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131 citations

Cites background from "Electrical properties of the pacema..."

...…first discussed as an intrinsic potential by Watanabe (1958) in lobster CG, and further described in studies of the Squilla (stomatopod) CG (Watanabe et al., 1967a, b), driver potentials are relatively slow, sustained, regenerative depolarizations that may arise from a gradual pacemaker…...
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...…the DP) with attenuated sharp deflections that are synchronous with the overshooting impulses arising from a flat baseline recorded from the axon (Watanabe et al., 1967b, Squilla oratorio; Tazaki, 1970, Eriocheir japonicus; Tazaki, 1973, Panulirus japonicus; Tazaki and Cooke, 1983a, Portunus…...
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...Such appositions have also been described in CG of Panulirus (Ohsawa, 1972) and Squilla (Irisawa and Hama, 1965; Watanabe et al., 1967a)....
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...(Watanabe et al., 1967a, fig....
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...6A) (Watanabe and Bullock, 1960; Watanabe et al., 1967b, in Squilla; Tazaki, 1972, in Eriocheir; Mayeri, 1973a, b, in Homarus; Matsui et al., 1977, in Panulirus; Tazaki and Cooke, 1979a, and Benson, 1980, in Portunus)....
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Other•DOI•

Organization of Invertebrate Motor Systems

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Donald Kennedy¹, William J. Davis²•Institutions (2)

Stanford University¹, University of California, Santa Cruz²

01 Dec 1977-Comprehensive Physiology

TL;DR: The sections in this article are: Anatomic Organization, Reflex Organization, Central Organization of Motor Systems, and Complex Behavioral Phenomena.

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Abstract: The sections in this article are: 1 Properties of Muscle 11 Anatomic Organization 12 Contraction Speed 13 Strength and Extent of Contraction 14 Thresholds for Excitation-Contraction Coupling 15 Correlations with Innervation 16 Dependence of Tension on Recent History 2 Motor Neurons and the Motor Unit 21 Motor Neuron Morphology 22 Correlations Between Motor Neuron Morphology and Function 23 Neuromuscular Transmission 24 Excitation-Contraction Coupling 25 Peripheral Motor Unit Organization 26 Matching of Central and Peripheral Properties 27 Ontogeny and Regeneration 3 Reflex Organization 31 Proprioceptive Reflexes 32 Exteroreceptive Reflexes 33 Righting Reflexes 34 Optomotor Reflexes 35 Control of Reflex Excitability 4 Central Organization of Motor Systems 41 Structure of Motor Programs 42 Storage of Motor Programs 43 Release of Motor Programs by Command Elements 44 Central Versus Peripheral Control of Motor Output 45 Development of Pattern-Generating Networks 46 Complex Behavioral Phenomena 5 Conclusion

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97 citations

Journal Article•DOI•

Pacemaker potentials for the periodic burst discharge in the heart ganglion of a stomatopod, Squilla oratoria.

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Akira Watanabe¹, Shosaku Obara¹, Toyohiro Akiyama¹•Institutions (1)

Tokyo Medical and Dental University¹

01 Mar 1967-The Journal of General Physiology

TL;DR: From somata of the pacemaker neurons in the Squilla heart ganglion, pacemaker potentials for the spontaneous periodic burst discharge are recorded with intracellular electrodes, showing that it is an electrically excitable response.

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Abstract: From somata of the pacemaker neurons in the Squilla heart ganglion, pacemaker potentials for the spontaneous periodic burst discharge are recorded with intracellular electrodes. The electrical activity is composed of slow potentials and superimposed spikes, and is divided into four types, which are: (a) "mammalian heart" type, (b) "slow generator" type, (c) "slow grower" type, and (d) "slow deficient" type. Since axons which are far from the somata do not produce slow potentials, the soma and dendrites must be where the slow potentials are generated. Hyperpolarization impedes generation of the slow potential, showing that it is an electrically excitable response. Membrane impedance increases on depolarization. Brief hyperpolarizing current can abolish the plateau but brief tetanic inhibitory fiber stimulation is more effective for the abolition. A single stimulus to the axon evokes the slow potential when the stimulus is applied some time after a previous burst. Repetitive stimuli to the axon are more effective in eliciting the slow potential, but the depolarization is not maintained on continuous stimulation. Synchronization of the slow potential among neurons is achieved by: (a) the electrotonic connections, with periodic change in resistance of the soma membrane, (b) active spread of the slow potential, and (c) synchronization through spikes.

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78 citations

Cites background or result from "Electrical properties of the pacema..."

..., · ~ ceding paper (Watanabe et al., 1967)....
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...The electrotonic isolation of the parallel axons from the soma is consistent with the histological finding (Watanabe et al., 1967), which indicates that the proximal part of the axon does not form side-junctions with the parallel axons....
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...The ratio is about 1.3, which is certainly out of the range of the attenuation ratios observed in resting cells (Watanabe et al., 1967)....
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...3, which is certainly out of the range of the attenuation ratios observed in resting cells (Watanabe et al., 1967)....
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...On the other hand, it is known that the cell somata are electrotonically connected with each other across a distance of several millimeters (Watanabe et al., 1967), and the spontaneous slow potential spreads from one cell to another (Fig....
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Journal Article•DOI•

Integrative Neurophysiology of the Lobster Cardiac Ganglion

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Daniel K. Hartline

01 Feb 1979-Integrative and Comparative Biology

TL;DR: The overall view is of a two-layered neural system in which the small cells possess an endogenous oscillatory driver potential, synchronized by synaptic and electrotonic interac?

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Abstract: synopsis. The synchronized bursts of impulses produced by the nine neurons of the isolated Homarus cardiac ganglion are usually initiated by Cell 7. Activity in all other cells commences with very short latency thereafter. Impulses in most cells originate in trigger zones located 1-2 mm from the cell body, but the first several impulses in Cells 8 and 9 frequently originate in distal trigger zones some distance from the somata. Large cells fire at a high initial frequency, dropping rapidly to a low frequency plateau. Small cells exhibit a more tonic behavior and fire at intermediate rates. More anterior small cells tend to fire faster than more posterior ones. The major synaptic interactions are the impulse-mediated excitatory ones from small cells to large cells, and possibly to more anterior small cells. There are weak interactions from large cells back onto small cells, and very specific interactions from Cells 1 and 2 onto 3A, 4A, 5A, and 3B, 4B, 5B respectively. The large discrete EPSPs generated in large cells by small cell impulses appear to be the explanation for "discrete positioning" in large-cell firing patterns. In this situation, large-cell impulses only fire at discrete times during the burst, regardless of the actual large-cell pattern. The overall view is of a two-layered neural system in which the small cells possess an endogenous oscillatory driver potential, synchronized by synaptic and electrotonic interac? tions, and driving a train of impulses in each cell. This activates excitatory synapses on the large cells, which combined with a triggered driver potential in each large cell, produces synchronized trains of motor impulses which activate the heart muscle, causing the heart? beat.

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68 citations

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Journal Article•DOI•

The Spread of Excitation among Neurons in the Heart Ganglion of the Stomatopod, Squilla oratoria

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Akira Watanabe¹, Kimihisa Takeda¹•Institutions (1)

Tokyo Medical and Dental University¹

01 Mar 1963-The Journal of General Physiology

TL;DR: Neurons in the heart ganglion of the mantis shrimp (a stomatopod crustacean) are functionally tightly linked together, indicating that the excitation in one neuron spreads very rapidly to all others.

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Abstract: Neurons in the heart ganglion of the mantis shrimp (a stomatopod crustacean) are functionally tightly linked together. The extracellular action potential from the whole trunk very often shows a complex form, but the response is all-or-none to the applied stimulus, indicating that the excitation in one neuron spreads very rapidly to all others. Application of isotonic MgCl2 solution or repetitive stimulation sometimes separates the spike into its components. The resting potential of the soma membrane is 50 to 60 mv. External stimulation elicits a spike of 60 to 80 mv amplitude with a step on its rising phase. Hyperpolarization reveals one more inflection on the rising phase. These inflections divide the soma action potential into three parts, A1, A2, and B spikes in that order from the foot. The B spike disappears on increasing the hyperpolarization, but A1 and A2 remain, indicating that B originates from the soma membrane, whereas A1 and A2 originate from the two axons of the bipolar cell. Thus the impulse invades the soma from two directions, one from the stimulated side, the other from the other side via the "parallel axons" and the "side-connections;" the latter are presumed to interconnect the axons. When the parallel axons are cut, conduction takes place across the soma with a greatly reduced safety factor and a prolonged conduction time. Neuron-to-neuron transmission takes place in either direction.

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21 citations

"Electrical properties of the pacema..." refers background or methods in this paper

...way of ephapses since the transmission goes both ways, there is only small indication of fatigue (Watanabe and Takeda, 1963), and changing the extracellular divalent ion concentrations has little effect (Watanabe et al....
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...Extra impulse generation (A 2-A 4) and repetitive firing (A2 and A4) are frequently observed in this ganglion, especially in a state of refractoriness (Watanabe and Takeda, 1963)....
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...The method of dissection and mounting of the heart was similar to that described in the earlier paper (Watanabe and Takeda, 1963), but several alterations were necessary for studying the rostral cell group....
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...This is different from the effect observed in caudal cells of the ganglion, in which the spike number is not increased to more than two with a DC stimulus (Watanabe and Takeda, 1963)....
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...trast with the usual action potential, which always spreads throughout the local system (Watanabe and Takeda, 1963)....
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Journal Article•DOI•

The electrocardiogram of a stomatopod

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Hiroshi Irisawa, Aya Irisawa

01 Jun 1957-The Biological Bulletin

TL;DR: The results of transection experiments on the nerve trunk support the view that the nerve cell of the thirteenth segment has a dominant role in the pacemaker activity of the heart contraction.

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Abstract: 1. The electrocardiogram of the tubular heart of the mantis shrimp, Squilla oratoria de Haan, was studied. Structural findings are described which confirm Alexandrowicz's observation.2. The electrogram consists of rapid spike components and slow action potentials. The spikes originate from the median nervous system of this heart, and the slow potential from the muscle.3. The results of transection experiments on the nerve trunk support the view that the nerve cell of the thirteenth segment has a dominant role in the pacemaker activity of the heart contraction.

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15 citations

Journal Article•DOI•

Contact of adjacent nerve fibers in the cardiac nerve of mantis shrimp

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Aya Irisawa¹, Kiyoshi Hama²•Institutions (2)

Hiroshima University¹, Osaka University²

01 Jan 1965-Japanese Journal of Physiology

14 citations

"Electrical properties of the pacema..." refers background in this paper

...Irisawa and Hama (1965) found, with the aid of the electron microscope, that the nerve fibers in this ganglion were often tied close together, separated only by a very thin double plasma membrane (apparently a "tight junction")....
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On the pace maker mechanism of the heart of the squill,Squilla oratoria de Haan.

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T. Shibuya

01 Mar 1961

9 citations

"Electrical properties of the pacema..." refers background in this paper

...In the Squilla heart ganglion the pacemaker for the periodic burst discharge is usually located in its rostral neurons (Shibuya, 1961; Watanabe and Takeda, 1963)....
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