Identification of excitatory and inhibitory motoneurons in the nematode Ascaris by electrophysiological techniques

Walrond, J. P.; Kass, Ira S.; Stretton, A. O. W.; Donmoyer, Judith E.

doi:10.1523/jneurosci.05-01-00001.1985

Cited by 64 publications

(40 citation statements)

References 15 publications

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“…Nematodes possess distinct excitatory and inhibitory motor neurons that release acetylcholine and GABA, respectively, at neuromuscular junctions Walrond et al, 1985). To determine on which type the HcGluCl␣ subunit is expressed, adult H. contortus were treated with both anti-HcGluCl␣ and anti-GABA antibodies.…”

Section: Immunolocalisation Of Hcglucl␣ and Hcglucl␤mentioning

confidence: 99%

Distribution of glutamate‐gated chloride channel subunits in the parasitic nematode Haemonchus contortus

Portillo

Jagannathan

Wolstenholme

2003

J of Comparative Neurology

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Glutamate-gated chloride channels (GluCl) are related to gamma-aminobutyric acid-A (GABA(A)) receptors and are the target sites for the avermectin/milbemycin (A/M) anthelmintics, drugs that cause paralysis of the somatic and pharyngeal muscles in nematodes. We have previously identified four GluCl subunits, HcGluClalpha, HcGluClbeta, HcGluClalpha3A, and HcGluClalpha3B from the sheep parasite Haemonchus contortus. We raised specific antisera against all of these subunits and used them in immunofluorescence experiments on adult parasites. All of the subunits were expressed in the motor nervous system, especially motor neuron commissures. Double-immunostaining experiments suggested that HcGluClalpha and HcGluClbeta were expressed on the same commissures; these were also stained with an anti-GABA antibody, suggesting that they may be inhibitory motor neurons. The HcGluClbeta subunit was also detected in lateral and sublateral nerve cords. The HcGluClalpha3A and -B subunits, products of an alternatively spliced gene, were expressed in different neurons. We found HcGluClalphaA in a pair of sensory, possibly amphid, neurons in the head, in addition to the motor neuron commissures. HcGluClalpha3B was detected in three cell bodies, probably of pharyngeal neurons, and to ventral and lateral cords. These results indicate that the GluCl are widely distributed in the H. contortus nervous system and suggest that they have critical roles controlling locomotion, pharyngeal function, and possibly sensory processing in parasitic nematodes. They also provide an explanation for the observed effects of the A/M anthelmintics.

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Section: Immunolocalisation Of Hcglucl␣ and Hcglucl␤mentioning

confidence: 99%

Distribution of glutamate‐gated chloride channel subunits in the parasitic nematode Haemonchus contortus

Portillo

Jagannathan

Wolstenholme

2003

J of Comparative Neurology

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“…applicability of C. elegans knowledge towards understanding other nematodes, and vice versa. For example, studies in the parasite Ascaris focused on anatomical and functional similarities to C. elegans in the ventral cord locomotory neurons (Johnson and Stretton, 1980;Stretton et al, 1978;Walrond et al, 1985), and studies in the parasite Strongyloides focused on similarities to C. elegans in the control of chemotaxis by amphid sensory neurons (Ashton et al, 1999;Forbes et al, 2004). We were interested instead in investigating nematode behaviors and their neuronal regulation explicitly for their evolutionary differences.…”

Section: Introductionmentioning

confidence: 99%

Evolution of pharyngeal behaviors and neuronal functions in free-living soil nematodes

Chiang

Steciuk

Shtonda

et al. 2006

Journal of Experimental Biology

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SUMMARY To explore the use of Caenorhabditis elegans and related nematodes for studying behavioral evolution, we conducted a comparative study of pharyngeal behaviors and neuronal regulation in free-living soil nematodes. The pharynx is divided into three parts: corpus, isthmus and terminal bulb,and pharyngeal behaviors consist of stereotyped patterns of two motions:pumping and peristalsis. Based on an outgroup species, Teratocephalus lirellus, the ancestral pattern of pharyngeal behaviors consisted of corpus pumping, isthmus peristalsis and terminal bulb pumping, each occurring independently. Whereas corpus pumping remained largely conserved, isthmus and terminal bulb behaviors evolved extensively from the ancestral pattern in the four major free-living soil nematode families. In the Rhabditidae family,which includes Caenorhabditis elegans, the anterior isthmus switched from peristalsis to pumping, and anterior isthmus and terminal bulb pumping became coupled to corpus pumping. In the Diplogasteridae family, the terminal bulb switched from pumping to peristalsis, and isthmus and terminal bulb became coupled for peristalsis. In the Cephalobidae family, isthmus peristalsis and terminal bulb pumping became coupled. And in the Panagrolaimidae family, the posterior isthmus switched from peristalsis to pumping. Along with these behavioral changes, we also found differences in the neuronal regulation of isthmus and terminal bulb behaviors. M2, a neuron that has no detectable function in C. elegans, stimulated anterior isthmus peristalsis in the Panagrolaimidae. Further, M4 was an important excitatory neuron in each family, but its exact downstream function varied between stimulation of posterior isthmus peristalsis in the Rhabditidae,isthmus/terminal bulb peristalsis in the Diplogasteridae, isthmus peristalsis and terminal bulb pumping in the Cephalobidae, and posterior isthmus/terminal bulb pumping in the Panagrolaimidae. In the Rhabditidae family, although M4 normally has no effect on the terminal bulb, we found that M4 can stimulate the terminal bulb in C. elegans if the Ca2+-activated K+ channel SLO-1 is inactivated. C. elegans slo-1 mutants have generally increased neurotransmission, and in slo-1 mutants we found novel electropharyngeogram signals and increased pumping rates that suggested activation of M4-terminal bulb synapses. Thus, we suggest that the lack of M4-terminal bulb stimulations in C. elegans and the Rhabditidae family evolved by changes in synaptic transmission. Altogether, we found behavioral and neuronal differences in the isthmus and terminal bulb of free-living soil nematodes, and we examined potential underlying mechanisms of one aspect of M4 evolution. Our results suggest the utility of Caenorhabditis elegans and related nematodes for studying behavioral evolution.

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“…One of the central goals of our laboratory is to elucidate the neural control of locomotion in Ascaris (Walrond et al 1985;Walrond and Stretton 1985a, b;Stretton et al 1985). So far, our electrophysiological experiments have focused primarily on motor neuronal processes outside the nerve cords, and the muscle cells they innervate.…”

Section: Introductionmentioning

confidence: 99%

Extracellular recordings from the motor nervous system of the nematode, Ascaris suum

Davis

Stretton

1992

J Comp Physiol A

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1. The close association of muscle and neurons in Ascaris suum makes it difficult to determine whether spikes recorded from nerve cords originate in muscle or neurons. We have developed criteria that distinguish muscle and neuronal activity. There are two categories of extracellular spikes. 2. The first category consists of spikes with a wide range of amplitudes, marked by large spikes. These spikes, which can be recorded over lateral muscle and over the dorsal and ventral nerve cords, are abolished when muscle is disrupted or removed, or when curare is applied. Large spikes are relatively infrequent, are correlated with intracellularly recorded muscle events, and respond to polarizations of motor neurons, implying that they originate in muscle. 3. The second spike category, small amplitude spikes, is exclusive to the ventral nerve cord, occurs more frequently than large spikes and displays patterned firing. Small spikes are not affected by muscle removal or by curare, and are correlated with motor neuronal post-synaptic potentials, but not with intracellularly recorded muscle events. We infer that they originate in neurons. 4. Low level activity recorded extracellularly over nerve cords may represent muscle activity due to tonic motor neuronal synaptic transmission. It responds to motor neuronal polarization and is suppressed by curare or muscle removal.

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Identification of excitatory and inhibitory motoneurons in the nematode Ascaris by electrophysiological techniques

Cited by 64 publications

References 15 publications

Distribution of glutamate‐gated chloride channel subunits in the parasitic nematode Haemonchus contortus

Distribution of glutamate‐gated chloride channel subunits in the parasitic nematode Haemonchus contortus

Evolution of pharyngeal behaviors and neuronal functions in free-living soil nematodes

Extracellular recordings from the motor nervous system of the nematode, Ascaris suum

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