The nervous system of the nematode worm Ascai contains about 250 nerve cells; of these, the motoneurons consist of five segmental sets, each containing 11 cells. Morphologically, the motoneurons can be divided into seven different types. Their geometry is simple: some are unbranched, others have one branch point, and the most complex have two. There is no neuropil in the nerve cords; synapses are made by axo-axonal contact or onto short spines. These features enable us to study the anatomy and physiology of the system with a degree of completeness that would be difficult in other systems. The physiological activity of five of the motoneurons has been investigated, three being excitatory and two inhibitory. The excitatory motoneurons receive input from intersegmental interneurons. The inhibitory motoneurons do not receive input from the interneurons; instead they receive their input from the excitatory motoneurons in a circuit that can mediate reciprocal inhibition between the dorsal and the ventral musculature.One of the outstanding problems in neurobiology is to understand the capabilities of assemblies of neurons in terms of the properties of the cells of which they are composed. In vertebrate nervous systems this problem has been approached in situations in which small numbers of cell types are arranged in a repeating pattern (e.g., cerebellum, retina); by studying the smallest fundamental repeating unit in these systems, the logical principles by which information is transformed might be inferred.An alternative approach is to select an invertebrate system in which there is only a small number of neurons. A number of interesting results have already emerged from the study of small assemblies of neurons in invertebrates (1-7). However, these assemblies still contain a large number of interacting components, and the geometry of the neurons in many cases is as complex as that found in vertebrates.In this paper we will describe the motor nervous system of the large parasitic nematode Ascaris lumicdes. This system has a small number of neurons with extremely simple geometry. This allows us to study the physiology and anatomy of the system with a degree of completeness that would be difficult in other systems.The salient advantages of the Ascaris nervous system are threefold.(i) Cell number. The entire nervous system contains only about 250 neurons; the motor nervous system that we will describe here is divided into five segments, each containing 11 motoneurons, and there are six nonsegmental interneurons traversing the segments. By contrast, in truly segmented animals such as the crayfish and the leech, each segmental ganglion contains several hundred cells and there are hundreds or thousands of neurons impinging upon each ganglion from other centers.
The nematode nervous system is distinguished by the small number and morphological simplicity of its neurons. Recently, the shapes and synaptic interactions of each of the 302 neurons in the small free-living nematode, Caenorhabditis elegans, have been determined from reconstructions of serial sections by electron microscopy. Comparable anatomical studies of the large parasitic nematode Ascaris have concentrated on the dorsal and ventral nerve cords where reconstructions of motor neurons by light microscopy led to the identification of seven distinct types of motor neurons, each corresponding to a homologous cell type in C. elegans. In this study the shapes of the 13 neurons with cell bodies in the retrovesicular ganglion (RVG) of Ascaris suum were reconstructed from light micrographs of serial sections. In other preparations the morphology of RVG neurons was observed in whole mounts after the cells were impaled with microelectrodes and injected with the fluorescent dye Lucifer yellow. The intracellular electrodes also permitted electrical recordings and revealed that one type of cell, the AVF-like interneuron, expresses spontaneous repetitive plateau potentials. Comparisons of neuronal morphologies in the retrovesicular ganglia of Ascaris and C. elegans suggest that each neuron in Ascaris can be assigned a corresponding homolog in C. elegans. These data provide further evidence for a remarkable conservation of neuronal morphology in nematodes despite large differences in size and habitat.
A physiological preparation in which it is possible to record responses in muscle to stimulation of single motoneurons of the nematode Ascaris lumbricoides is described. With this preparation we have determined the physiological sign (E or I; excitatory or inhibitory) of the neuromuscular synapses of 21 identified motoneurons--12 are excitatory and 9 inhibitory. Ascaris motoneurons had previously been classified by morphological criteria into seven classes (Stretton, A. O. W., R. M. Fishpool, E. Southgate, J. E. Donmoyer, J. P. Walrond, J. E. R. Moses, and I. S. Kass (1978) Proc. Natl. Acad. Sci. U. S. A. 75: 3493-3497). Physiological studies were performed on members of five of these classes. Three classes of neurons (DE1, DE2, and DE3) are excitatory to dorsal muscle cells. Two classes (DI and VI) are inhibitory neurons which innervate the dorsal and ventral muscle cells, respectively. The motoneurons in Caenorhabditis elegans (White, J. E., E. Southgate, J. N. Thomson, and S. Brenner (1976) Philos. Trans. R. Soc. Lond. (Biol.) 275: 327-348) can be divided into seven morphological classes which are very similar to those in Ascaris. Based upon the structure-function correlation in Ascaris, we have predicted which motoneurons are excitatory and which are inhibitory in C. elegans.
Ascaris suum has a nervous system that is very simple both numerically and morphologically. It comprises only 298 neurons almost all of which are extremely simple in shape. Extensive anatomical descriptions of the morphology of neurons and of their synaptic connections, together with the study, by using intracellular recording techniques, of their physiological properties, have led to a prediction of how the motor nervous system controls behavior. Subsequent discovery of endogenous neuropeptides that have potent activity on subsets of the motor neurons suggests that the description of the motor circuitry is more complex than is apparent from its anatomy.
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