Neural networks of the stomatogastric system of crustaceans as a model system of neuroethology

Question

The stomatogastric system of crustaceans is a superior model system of neurosciences. It is build up by the movable parts of the foregut and the stomatogastric nervous system. This consists of a manageable number of identified nerve cells which are organized in different neural networks which are autonomous responsible for the rhythmic activity patterns necessary for the complex movements of the foregut. Network analysis of the stomatogastric ganglion have profoundly influenced the understanding of universal cellular and synaptic building blocks which also can be found in vertebrates. A high plasticity of the activity of the stomatogastric nervous system is maintained by using a high number of neuromodulatory substances which acts upon the connections of single building blocks of a network but also by qualitative and quantitative changes of neuronal properties. Under the influence of a single neuromodulator, the activity of a single neuron can be switched between two different networks and even a regrouping of whole networks of the stomatogastric nervous system could be shown.

The elements of the stomatogastric system

Higher Crustaceans (lobster, spiny lobster, crabs, crayfish) possess a structured foregut which can be divided into 4 different parts: the esophageous, stomach, gastric mill with stomach teeth and the pyloric filtering machine. The crustaceans take their food roughly broken up using their claws. Then, peristaltic contractions of the esophageous direct the food to the stomach. There, the food is not only digested but also grinded between three strong teeth which are dorsally on the inner side of the stomach. Using an endoscope, the chewing movements of the teeth and the pumping movements of the cardio-pyloric groove can be viewed. In several steps, a complicated filtering press divides solid and fluid food-particles. The solid particles get into the hindgut where they are excreted. The fluid nutrients are taken up by the midgut gland which consists of a system of bags and also makes up a functional equivalent of the liver and pancreas.

The peristaltic swallowing movements, the contraction of the stomach as well as the chewing behaviour of the gastric mill and the functioning of the pyloric filters demand a complex apparatus of bones and muscles and also different neuronal networks which generate the different patterns of activity for the movements. These networks lie within the stomatogastric nervous system. It consists of the paired commissural ganglia, the esophageal ganglion, the stomatogastric ganglion and the nerves which interconnect the ganglia and the muscles. This system is connected to the brain by connectives and the inferior ventricular nerve.

The neural networks of the stomatogastric ganglion

The repertoire of movements is the obvious result of the information processing within the stomatogastric nervous system. This produces mainly 4 distinguishable rhythmic activity-patterns (using 4 neural networks). 2 networks lie in the commisural ganglia and the esophageal ganglion which generate the rhythm for movements of the esophageous and the stomach. The smaller stomatogastric ganglion contains approx. 30 nerve-cells which are connected to make up three different networks. 11 neurons make up the gastric network which controls the stomach teeth and 14 nerve-cells make up the pyloric network which controls movements of the pyloric filtering machine. These cells are individuals with a characteristic shape of the cellbody which can be seen using fluorescent dyes like Lucifer Yellow. In addition, characteristic properties are oscillations of their membrane potential. Therefore each cell can be identified and classified to belong to either network.

The plasticity of the neural networks and the effects upon activity patterns

A technical circuit diagram where transistors, resistors and capacitors are "hard-wired" can only produce a strict pattern of activity. A high plasticity of biological systems is achieved by allowing changes of the wiring as well as cellular properties in a quantitative and qualitative way. It was shown that a change in different modes of chewing (of the stomach teeth) was dependent on the DG-cell generating pacemaker potentials after supplying Proctolin and that the LG-cells suddenly show different kinds of potentials which change the mode of movement for the lateral teeth. Up to now, more than 20 different neuromodulators with influence upon the stomatogastric nervous system could be found. Each could promote a typical activity-pattern in isolated networks. Relevance of this patterns can be seen when actual movements are analyzed; e.g. the change of a nerve cell between two different rhythms. If the action potentials of the lateral gastric motoneuron LG oscillate between the rhythms of the gastric and pyloric network (Fig. A), the lateral teeth make hybrid closing movements (Fig. B). Mittlerweile wurden über 20 Neuromodulatoren im Stomatogastrischen Nervensystem nachgewiesen. Jeder konnte in isolierten Netzwerken typische Aktivitätsmuster hervorrufen. Erst die Bewegungsanalyse enthüllt die Bedeutung eines Erregungsmusters, das zum Beispiel ein Umschalten einer Nervenzelle zwischen zwei Rhythmen zeigt. Erscheinen die Aktionspotentiale des Lateralen Gastrischen Motoneurons LG abwechselnd im Takt des gastrischen und des pylorischen Netzwerkes (Abbildung A), führen die Lateralzähne hybride Schließbewegungen aus (Abbildung B). In the same way a change of the pyloric into the gastric network can occur. In normal conditions, the pyloric activity of the inferior cardia motoneurons IC elicits closing movements of the cardio-pyloric fringe. This neuron can adopt a hybrid way of working, containing additional long bursts of action potentials in phase with the gastric cycle. By this activity, not only the fringe is closed but also the lateral teeth are moved forward.