Identification of a putative mechanosensory neuron in Lymnaea: characterization of its synaptic and functional connections with the whole-body withdrawal interneuron

1996 ◽  
Vol 76 (5) ◽  
pp. 3230-3238 ◽  
Author(s):  
T. Inoue ◽  
M. Takasaki ◽  
K. Lukowiak ◽  
N. I. Syed
Keyword(s):  
Sensory Neuron ◽  
Action Potentials ◽  
Synaptic Connection ◽  
Lucifer Yellow ◽  
Whole Body ◽  
Pond Snail ◽  
Mechanosensory Neuron ◽  
Functional Connections ◽  
Freshwater Pond ◽  
Withdrawal Behavior

1. In this study, we identified a putative mechanosensory neuron in the freshwater pond snail Lymnaea stagnalis. This sensory neuron, termed right parietal dorsal 3 (RPD3), mediates part of the whole-body withdrawal behavior via the activation of a withdrawal interneuron. 2. RPD3 is located in the central ring ganglia, where its soma is situated on the dorsal surface of the right parietal ganglion. Intracellular injection of the dye Lucifer yellow revealed that RPD3 has both central and peripheral axonal projections. 3. In isolated-CNS preparations, RPD3 was quiescent. In semi-intact preparations, however, a gentle/moderate mechanical touch (by a pair of blunt forceps) to the mantle cavity or columellar musculature elicited action potentials in RPD3 in the absence of prepotential activity. Furthermore, mechanical stimulus-induced action potentials in RPD3 persisted in the presence of zero Ca2+/ high Mg2+ and high Ca2+/high Mg2+ salines. Together, these data suggest that RPD3 is most likely to be a primary sensory neuron. 4. In both isolated-CNS and semi-intact preparations, intracellular depolarization of RPD3 excited the whole-body withdrawal interneuron right pedal dorsal 11 (RPeD11). This synaptic connection persisted in the presence of high Ca2+ and high Mg2+ saline, suggesting that it is likely to be monosynaptic. Moreover, when stimulated electrically, the interneuron RPeD11 induced an hyperpolarizing response in RPD3. The possibility of this connection being monosynaptic was not tested, however, in the present study. Together, these data demonstrate that RPD3 excites RPeD11, which in turn may inhibit RPD3 activity. 5. In the semi-intact preparation, a mechanical touch to the mantle edge excited RPD3, which in turn generated action potentials in RPeD11. Zero Ca2+ saline blocked this synaptic connection between RPD3 and RPeD11, suggesting that it is chemical. 6. To demonstrate that RPD3 was sufficient to induce the withdrawal response and that the withdrawal behavior was mediated indirectly via RPeD11, we made simultaneous intracellular recordings from these two neurons while monitoring muscle contractions via a tension transducer. Intracellular depolarization of RPD3 elicited action potentials in RPeD11, followed by the contraction of the columellar muscle. Similar stimulation of RPD3 failed to excite a simultaneously hyperpolarized RPeD11 and as a result, no contraction of the columellar muscle occurred. Direct intracellular depolarization of RPeD11, however, induced the contraction of the columellar muscle. These data suggest that RPD3-induced withdrawal behavior is mediated in part via RPeD11.

DIFFERENTIAL TRACER COUPLING BETWEEN PAIRS OF IDENTIFIED NEURONES OF THE MOLLUSC LYMNAEA STAGNALIS

1994 ◽  
Vol 192 (1) ◽  
pp. 291-297
Author(s):  
N Ewadinger ◽  
N Syed ◽  
K Lukowiak ◽  
A Bulloch
Keyword(s):  
Nervous System ◽  
Normal Saline ◽  
Lymnaea Stagnalis ◽  
Lucifer Yellow ◽  
Electrical Coupling ◽  
Cell Communication ◽  
Pond Snail ◽  
Dye Coupling ◽  
Freshwater Pond ◽  
Weakly Coupled

Electrical coupling is a common means of cell-to-cell communication in both neuronal and non-neuronal tissues (Lowenstein, 1985). Within the nervous system, many electrically coupled neurones exhibit dye coupling (Bennett, 1973; Stewart, 1978; Glantz and Kirk, 1980; Spencer and Satterlie, 1980; Fraser and Heitler, 1993); however, some electrically coupled cells do not dye-couple (Audesirk et al. 1982; Murphy et al. 1983; Berdan, 1987; Robinson et al. 1993; Veenstra et al. 1993). Electrical coupling and dye coupling, often considered in parallel, are in fact two different parameters that can vary independently (e.g. Audesirk et al. 1982; Perez-Armendariz et al. 1991). The giant identified neurones of pulmonate and opisthobranch molluscs have frequently been used for studies of neuronal communication and its plasticity (Winlow and McCrohan, 1987; Bulloch, 1989). In the present study, we explored the relationship between electrical and tracer coupling in both strongly and weakly coupled pairs of molluscan neurones. Specifically, we examined electrically coupled, identified neurones in a freshwater pond snail, Lymnaea stagnalis L., and tested for tracer coupling with Lucifer Yellow CH and biocytin. The cells examined were the strongly electrically coupled neurones, visceral dorsal 1 (VD1) and right parietal dorsal 2 (RPD2) (Boer et al. 1979; Benjamin and Pilkington, 1986), and the weakly coupled neurones, left buccal 1 (LB1) and right buccal 1 (RB1) (Benjamin and Rose, 1979). The use of these particular neurones made it possible to compare electrical coupling with tracer coupling in the molluscan central nervous system (CNS). All experiments were performed on laboratory-bred Lymnaea stagnalis (Mollusca, Pulmonata), maintained as previously described (Ridgway et al. 1991). The CNS was dissected from mature animals (16­18 mm shell length) and pinned to the silicone rubber (RTV 616 GE) base of a recording dish in normal saline (51.3 mmol l-1 NaCl, 1.7 mmol l-1 KCl, 4.1 mmol l-1 CaCl2, 1.5 mmol l-1 MgCl2 and 5 mmol l-1 Hepes, pH 7.9). Following removal of the outer connective tissue sheath, a small Pronase crystal (Sigma, type XIV, P-5147), held by forceps, was carefully applied to specific ganglia; this treatment softened the inner sheath and facilitated microelectrode penetration. The CNS was then rinsed several times at 5 °C in normal saline.

Intracellular measurements from a rapidly adapting sensory neuron

1991 ◽  
Vol 65 (1) ◽  
pp. 49-56 ◽  
Author(s):  
T. A. Basarsky ◽  
A. S. French
Keyword(s):  
Action Potential ◽  
Sensory Neuron ◽  
Cell Body ◽  
Action Potentials ◽  
Lucifer Yellow ◽  
Membrane Conductance ◽  
Channel Inactivation ◽  
Current Pulses ◽  
Potential Shape ◽  
Sinusoidal Current

1. The femoral tactile spine of the cockroach contains a single sensory neuron with its cell body in the lumen of the spine. Step movements of the spine produce rapidly adapting bursts of action potentials that decay to 0 in 1 s. Previous work has shown that a large part of this adaptation occurs during action potential encoding. 2. Intracellular recordings from the tactile spine neuron were obtained by lowering a microelectrode through the spine lumen and penetrating the cell body. Injection of Lucifer yellow followed by fluorescence microscopy confirmed the morphology of the soma, with a diameter of 30 microns, and showed an axon of 9 microns leaving the spine and proceeding proximally along the femur. 3. Membrane-potential records were digitized and examined at high resolution during bursts of action potentials produced by depolarizing current pulses. No significant changes in action potential shape were detected during adaptation. However, the rate of depolarization between action potentials slowed dramatically during the burst. This slowing could be reduced and the burst substantially prolonged by chloramine-T (CT), an agent that reduces sodium channel inactivation in several preparations. 4. A 100 Hz sinusoidal current was superimposed on depolarizing current pulses to test for changes in membrane conductance during a burst of action potentials. No such changes were detected, indicating that rapid adaptation is not due to changes in membrane permeability.(ABSTRACT TRUNCATED AT 250 WORDS)

Whole body withdrawal circuit and its involvement in the behavioral hierarchy of the mollusk Clione limacina

1996 ◽  
Vol 75 (2) ◽  
pp. 529-537 ◽  
Author(s):  
T. P. Norekian ◽  
R. A. Satterlie
Keyword(s):  
Feeding Behavior ◽  
Motor Neurons ◽  
Prey Capture ◽  
The Body ◽  
Whole Body ◽  
High Threshold ◽  
Behavioral Repertoire ◽  
Withdrawal Behavior ◽  
Cerebral Neurons ◽  
Clione Limacina

1. The behavioral repertoire of the holoplanktonic pteropod mollusk Clione limacina includes a few well-defined behaviors organized in a priority sequence. Whole body withdrawal takes precedence over slow swimming behavior, whereas feeding behavior is dominant over withdrawal. In this study a group of neurons is described in the pleural ganglia, which controls whole body withdrawal behavior in Clione. Each pleural withdrawal (Pl-W) neuron has a high threshold for spike generation and is capable of inducing whole body withdrawal in a semi-intact preparation: retraction of the body-tail, wings, and head. Each Pl-W neuron projects axons into the main central nerves and innervates all major regions of the body. 2. Stimulation of Pl-W neurons produces inhibitory inputs to swim motor neurons that terminate swimming activity in the preparation. In turn, Pl-W neurons receive inhibitory inputs from the cerebral neurons involved in the control of feeding behavior in Clione, neurons underlying extrusion of specialized prey capture appendages. Thus it appears that specific inhibitory connections between motor centers can explain the dominance of withdrawal behavior over slow swimming and feeding over withdrawal in Clione.

Structure and Function of the Lateral Giant Neurone of the Primitive Crustacean Anaspides Tasmaniae

1979 ◽  
Vol 78 (1) ◽  
pp. 121-136
Author(s):  
GERALD E. SILVEY ◽  
IAN S. WILSON
Keyword(s):  
Action Potentials ◽  
Tactile Stimulation ◽  
Large Diameter ◽  
Whole Body ◽  
Giant Fibre ◽  
Single Action ◽  
Giant Neurone ◽  
And Function ◽  
Thoracic And Abdominal ◽  
Stimulation Of

The syncarid crustacean Anaspides tasmaniae rapidly flexes its free thoracic and abdominal segments in response to tactile stimulation of its body. This response decrements but recovers in slightly more than one hour. The fast flexion is evoked by single action potentials in the lateral of two large diameter fibres (40 μm) which lie on either side of the cord. The lateral giant fibre is made up of fused axons of 11 neurones, one in each of the last 5 thoracic and 6 abdominal ganglia. The soma of each neurone lies contralateral to the axon. Its neurite crosses that of its counterpart in the commissure and gives out dendrites into the neuropile of each hemiganglion. The lateral giant neurone receives input from the whole body but fires in response only to input from the fourth thoracic segment posteriorly. Both fibres respond with tactile stimulation of only one side. Since neither current nor action potentials spread from one fibre to the other, afferents must synapse with both giant neurones. The close morphological and physiological similarities of the lateral giant neurone in Anaspides to that in the crayfish (Eucarida) suggest that the lateral giant system arose in the ancestor common to syncarids and eucarids, prior to the Carboniferous.

Electrical properties and innervation of fibers in the orbital layer of rat extraocular muscles

1989 ◽  
Vol 61 (1) ◽  
pp. 116-125 ◽  
Author(s):  
J. Jacoby ◽  
D. J. Chiarandini ◽  
E. Stefani
Keyword(s):  
Electrical Properties ◽  
Nerve Stimulation ◽  
Action Potentials ◽  
Time Course ◽  
Lucifer Yellow ◽  
Extraocular Muscles ◽  
Resting Potential ◽  
Inferior Rectus ◽  
End Plate ◽  
Orbital Layer

1. The inferior rectus muscle of rat, one of the extraocular muscles, contains two populations of multiply innervated fibers (MIFs): orbital MIFs, located in the orbital layer of the muscle and global MIFs, found in the global layer. The electrical properties and the responses to nerve stimulation of orbital MIFs were studied with single intracellular electrodes and compared with those of twitch fibers of the orbital layer, MIFs of the global layer, and tonic fibers of the frog. 2. About 90% of the orbital MIFs did not produce overshooting action potentials. In these fibers the characteristics and time course of the responses to nerve stimulation varied along the length of the fibers. Within 2 mm of the end-plate band of the muscle, the responses consisted of several small end-plate potentials (EPPs) and a nonovershooting spike. Distal to 2 mm, the responses in most fibers consisted of large and small EPPs with no spiking response. Some fibers produced very small spikes surmounted on large EPPs. 3. Overshooting action potentials were observed in approximately 10% of the orbital MIFs recorded between the end-plate band and 2 mm distal. The presence or absence of action potentials was not related to the magnitude of the resting potential of the fibers. 4. The threshold of nerve stimulated responses in orbital MIFs was the same as that in orbital twitch fibers. A large number of orbital MIFs had latencies equal to those for the orbital twitch fibers recorded at the same distance from the end-plate band, but the average latency was greater in the MIFs. The latency of orbital MIFs was about one-half of that for the MIFs of the global layer. The values for the effective resistance and membrane time constant of orbital MIFs fell between those for orbital twitch fibers on the one hand, and global MIFs and frog tonic fibers on the other. 5. In order to compare electrical properties with innervation patterns, fibers identified electrophysiologically as orbital MIFs were injected with the fluorescent dye Lucifer yellow and then traced in Epon-embedded, serial transverse sections. In addition to numerous superficial endings distributed along the fibers, a single "en plaque" ending was also found in the end-plate band that resembled the end plates of the adjacent orbital twitch fibers. 6. From these results we conclude that the electrical activity of orbital MIFs varies along the length of the fibers.(ABSTRACT TRUNCATED AT 400 WORDS)

A System of Electrically Coupled Small Cells in the Buccal Ganglia of the Pond Snail Planorbis Corneus

1972 ◽  
Vol 56 (3) ◽  
pp. 621-637
Author(s):  
MICHAEL S. BERRY
Keyword(s):  
Synaptic Input ◽  
Action Potentials ◽  
Burst Activity ◽  
Small Cells ◽  
Pond Snail ◽  
Trigger System ◽  
Buccal Ganglia ◽  
Large Numbers ◽  
Planorbis Corneus

1. The buccal ganglia of Planorbis contain a population of electrically coupled small cells. This has been studied, in preparations of isolated ganglia, by recording intracellularly from the cells two at a time. 2. The population is usually silent but activity initiated in any one of its members tends to spread to the rest of the population in both ganglia. Failure of spread, or fatigue, gradually occurs on repetition. 3. The group has the properties of a trigger system, initiating prolonged patterned activity in large numbers of neurones in the buccal ganglia. This may normally initiate feeding. 4. In addition to central processes, both in the buccal ganglia and to the rest of the CNS, the system has peripheral axons in most of the buccal nerves. No synaptic input could be demonstrated. 5. Action potentials in some of the cells increase greatly in duration with repetition. The resulting electrotonic EPSP's, recorded in closely coupled trigger cells, correspondingly increase in size. The possible integrative significance of this is discussed, especially its effect in offsetting fatigue. 6. In some preparations spontaneous bursting occurred in trigger cells and this elicited burst activity in large neurones, including motoneurones. The system may have an intrinsic pacemaker.

Coordination of locomotor and cardiorespiratory networks of Lymnaea stagnalis by a pair of identified interneurones

1991 ◽  
Vol 158 (1) ◽  
pp. 37-62 ◽  
Author(s):  
N. I. Syed ◽  
W. Winlow
Keyword(s):  
Body Wall ◽  
Lymnaea Stagnalis ◽  
The Body ◽  
Whole Body ◽  
Pond Snail ◽  
Selective Ablation ◽  
The Central Nervous System ◽  
Body Wall Muscles ◽  
Bilateral Pair ◽  
Left And Right

1. The morphology and electrophysiology of a newly identified bilateral pair of interneurones in the central nervous system of the pulmonate pond snail Lymnaea stagnalis is described. 2. These interneurones, identified as left and right pedal dorsal 11 (L/RPeD11), are electrically coupled to each other as well as to a large number of foot and body wall motoneurones, forming a fast-acting neural network which coordinates the activities of foot and body wall muscles. 3. The left and right sides of the body wall of Lymnaea are innervated by left and right cerebral A cluster neurones. Although these motoneurones have only ipsilateral projections, they are indirectly electrically coupled to their contralateral homologues via their connections with L/RPeD11. Similarly, the activities of left and right pedal G cluster neurones, which are known to be involved in locomotion, are also coordinated by L/RPeD11. 4. Selective ablation of both neurones PeD11 results in the loss of coordination between the bilateral cerebral A clusters. 5. Interneurones L/RPeD11 are multifunctional. In addition to coordinating motoneuronal activity, they make chemical excitatory connections with heart motoneurones. They also synapse upon respiratory motoneurones, hyperpolarizing those involved in pneumostome opening (expiration) and depolarizing those involved in pneumostome closure (inspiration). 6. An identified respiratory interneurone involved in pneumostome closure (visceral dorsal 4) inhibits L/RPeD11 together with all their electrically coupled follower cells. 7. Both L/RPeD11 have strong excitatory effects on another pair of electrically coupled neurones, visceral dorsal 1 and right parietal dorsal 2, which have previously been shown to be sensitive to changes in the partial pressure of environmental oxygen (PO2). 8. Although L/RPeD11 participate in whole-body withdrawal responses, electrical stimulation applied directly to these neurones was not sufficient to induce this behaviour.

scholarly journals Action Potential Reflection and Failure at Axon Branch Points Cause Stepwise Changes in EPSPs in a Neuron Essential for Learning

2000 ◽  
Vol 83 (3) ◽  
pp. 1693-1700 ◽  
Author(s):  
Stephen A. Baccus ◽  
Brian D. Burrell ◽  
Christie L. Sahley ◽  
Kenneth J. Muller
Keyword(s):  
Action Potential ◽  
Action Potentials ◽  
Conduction Block ◽  
Neuronal Morphology ◽  
Whole Body ◽  
Reverse Direction ◽  
Mammalian Brain ◽  
Branch Points ◽  
Individual Branch ◽  
Axon Branch

In leech mechanosensory neurons, action potentials reverse direction, or reflect, at central branch points. This process enhances synaptic transmission from individual axon branches by rapidly activating synapses twice, thereby producing facilitation. At the same branch points action potentials may fail to propagate, which can reduce transmission. It is now shown that presynaptic action potential reflection and failure under physiological conditions influence transmission to the same postsynaptic neuron, the S cell. The S cell is an interneuron essential for a form of nonassociative learning, sensitization of the whole body shortening reflex. The P to S synapse has components that appear monosynaptic (termed “direct”) and polysynaptic, both with glutamatergic pharmacology. Reflection at P cell branch points on average doubled transmission to the S cell, whereas action potential failure, or conduction block, at the same branch points decreased it by one-half. Each of two different branch points affected transmission, indicating that the P to S connection is spatially distributed around these branch points. This was confirmed by examining the locations of individual contacts made by the P cell with the S cell and its electrically coupled partner C cells. These results show that presynaptic neuronal morphology produces a range of transmission states at a set of synapses onto a neuron necessary for a form of learning. Reflection and conduction block are activity-dependent and are basic properties of action potential propagation that have been seen in other systems, including axons and dendrites in the mammalian brain. Individual branch points and the distribution of synapses around those branch points can substantially influence neuronal transmission and plasticity.

A student apparatus for recording action potentials in cockroach legs.

1992 ◽  
Vol 262 (6) ◽  
pp. S18
Author(s):  
T M Linder ◽  
J Palka
Keyword(s):  
Sensory Neuron ◽  
Action Potentials ◽  
Sensory Adaptation ◽  
Simple Apparatus ◽  
Beginning Students

A comparatively simple apparatus allows even beginning students to observe action potentials in the cockroach leg. The recordings are made extracellularly by impaling the leg on two insect pins. Deflection of large spines on the leg, which are each innervated by one sensory neuron, initiates the action potentials. Using this technique, students observe the all-or-nothing nature of action potentials, their coding of information by frequency, and sensory adaptation.

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