Circuit reconfiguration in the stomatogastric ganglion of the lobster

In crustacea, movements of the foregut are achieved by contraction of discrete striated muscles, very similar to the muscles that move limbs during movements of the body. Quite complex, regularly repeating patterns of activity occur in these muscles. A major reason for investigating their control is that the neurons responsible for generating these movements are contained in four discrete, small ganglia and the nerves that connect them (Fig. 7.11a). The most intensively investigated is the stomatogastric ganglion which, in lobsters, contains just 30 neurons. A small nerve connects it with three other ganglia of the stomatogastric nervous system. Almost all of the neurons in the stomatogastric ganglion are motor neurons and, unlike the situation for the three examples described earlier in this chapter, the motor neurons are essential components of the central pattern generator.

The stomatogastric ganglion controls two different parts of the foregut, called the gastric mill and the pyloric region. The gastric mill contains three teeth, which cut and grind food after it has been churned in a region called

Gastric Mill Crustaceans

Figure 7.11 The foregut and stomatogastric nervous system of a spiny lobster (Panulirus). (a) The foregut with its ganglia and nerves. The stomatogastric ganglion lies in a blood vessel (not shown) on top of the stomach. The stomatogastric and oesophageal ganglia are unpaired, and there is a circumoesophageal ganglion attached to each of the large connective nerves which link the brain and suboesophageal ganglion. (b) A diagram showing some of the synaptic connections between neurons of the pyloric section of the stomatogastric ganglion. All neurons except the anterior burster (AB) are motor neurons; the two PD neurons control dilatation of the pylorus and the other motor neurons (VD, LP, IC and PY) control different phases of constriction. The stomatogastric nerve contains axons of neurons which have a variety of different effects on neurons of the stomatogastric ganglion. (b modified from Selverston & Miller, 1980.)

Figure 7.11 The foregut and stomatogastric nervous system of a spiny lobster (Panulirus). (a) The foregut with its ganglia and nerves. The stomatogastric ganglion lies in a blood vessel (not shown) on top of the stomach. The stomatogastric and oesophageal ganglia are unpaired, and there is a circumoesophageal ganglion attached to each of the large connective nerves which link the brain and suboesophageal ganglion. (b) A diagram showing some of the synaptic connections between neurons of the pyloric section of the stomatogastric ganglion. All neurons except the anterior burster (AB) are motor neurons; the two PD neurons control dilatation of the pylorus and the other motor neurons (VD, LP, IC and PY) control different phases of constriction. The stomatogastric nerve contains axons of neurons which have a variety of different effects on neurons of the stomatogastric ganglion. (b modified from Selverston & Miller, 1980.)

the cardiac sac. Muscles of the gastric mill are activated in a rhythm with a cycle period of 5-10 s. The pyloric region, into which the gastric mill empties, has a shorter cycle time, of 0.5-2 s; it squeezes and mixes food particles.

The pattern of synaptic connections within the ganglion and the array of active, membrane properties which single neurons possess are startlingly complex. The 14 neurons of the pyloric network are connected in a network that includes over 20 electrical synapses and over 60 chemical, inhibitory synapses (Fig. 7.11b). At one time it was thought that the gastric mill rhythm is primarily generated by reciprocal, inhibitory circuit interactions, whereas the pyloric rhythm is generated by intrinsic bursting in one inter-neuron. However, we now know that the generation of each rhythm involves both mechanisms. One experimental approach that was particularly useful in revealing the different mechanisms involved isolating single cell circuits of small numbers of cells from others in the ganglion by killing the cells that were presynaptic to the neurons of interest. To kill a particular neuron, a fluorescent dye was injected into it through a microelectrode and then an intense spot of blue light was shone onto the cell body (Selverston & Miller, 1980). Using this technique, it was possible to isolate a single pair of neurons that are connected by reciprocal, inhibitory synapses (Miller and Selverston, 1982). A simple two-neuron network is able to generate rhythmical activity, although the pattern differs from that produced by an intact stomatogastric ganglion.

Neurons of the stomatogastric nerve play a vital role in pattern generation by unmasking particular properties that are intrinsic to individual cells. The nerve contains 60-120 axons and rhythmic activity is not recorded from the stomatogastric ganglion if the stomatogastric nerve is cut or if its axons are silenced. However, rhythmic co-ordinated output from the ganglion can be restored either by stimulating axons within the nerve or by adding certain transmitters, particularly some amines or pep-tides, to the seawater bathing the ganglion. Because the pyloric neurons only burst in the presence of particular transmitters, they are called conditional oscillators. All of the neurons in the pyloric region are conditional oscillators but one, the anterior burster (AB in Fig. 7.11b), has the fastest rhythm and acts as the master clock, setting the pace for the whole pyloric region.

One particular bilateral pair of neurons that project into the stomatogas-tric ganglion, called the pyloric suppressors, have widespread effects on motor patterns (Meyrand et al., 1991; 1994). When the pyloric suppressor neurons are active, the separate pyloric and gastric mill rhythms stop; and the pyloric and gastric mill neurons become active in a new, co-ordinated pattern of rhythmic activity (Fig. 7.12a). An electric synapse links the two pyloric suppressor neurons, so they operate as a single functional unit. When the stomatogastric ganglion is expressing the pyloric and gastric mill patterns, the pyloric suppressor neurons are silent. However, they can be excited by applying food to chemoreceptors that are situated on the valve that separates the oesophagus from the stomach. When a pyloric suppressor neuron is excited, either through these sense organs or by injection of depolarising current, its membrane potential oscillates and it generates bursts of spikes. These bursts of spikes excite motor neurons which cause the valve to open, and intracellular recordings from pyloric and gastric mill neurons show profound changes in the activity patterns they express. Some neurons are tonically inhibited from producing spikes, but others, such as

Figure 7.12 Action of the pyloric suppressor neuron (PS) in reconfiguring the stomatogastric ganglion. (a) Intracellular recordings from a neuron of the pyloric region and a neuron of the gastric mill region of the stomatogas-tric ganglion. On the left, PS was silent and the two neurons expressed different rhythms of activity. When PS was stimulated, the two neurons became active in the same new rhythm. (b) A diagram to illustrate the effects of PS on the circuitry of the stomatogastric ganglion. When PS is silent, networks for the oesophageal, pyloric and gastric mill rhythms operate independently of each other. Activity in PS causes some neurons of these three networks to be incorporated into a new functional network, and silences others (dotted). (c) Behavioural correlates of PS activity. On the left, different foregut regions are acting independently and valves between them are closed. On the right, the lobster is swallowing. (a from Meyrand, Simmers & Moulins,1991; reprinted from Nature; copyright © 1991 Macmillan Magazines Ltd; b and c redrawn after Meyrand, Simmers & Moulins1994.)

Figure 7.12 Action of the pyloric suppressor neuron (PS) in reconfiguring the stomatogastric ganglion. (a) Intracellular recordings from a neuron of the pyloric region and a neuron of the gastric mill region of the stomatogas-tric ganglion. On the left, PS was silent and the two neurons expressed different rhythms of activity. When PS was stimulated, the two neurons became active in the same new rhythm. (b) A diagram to illustrate the effects of PS on the circuitry of the stomatogastric ganglion. When PS is silent, networks for the oesophageal, pyloric and gastric mill rhythms operate independently of each other. Activity in PS causes some neurons of these three networks to be incorporated into a new functional network, and silences others (dotted). (c) Behavioural correlates of PS activity. On the left, different foregut regions are acting independently and valves between them are closed. On the right, the lobster is swallowing. (a from Meyrand, Simmers & Moulins,1991; reprinted from Nature; copyright © 1991 Macmillan Magazines Ltd; b and c redrawn after Meyrand, Simmers & Moulins1994.)

the pyloric and gastric mill neurons, express a new pattern in which neurons from both regions are co-ordinated.

The new pattern is probably that for swallowing, and the pyloric suppressor neurons also cause the valve between the oesophagus and stomach to open. During swallowing, movements of the whole foregut must be coordinated to move food onwards (Fig. 7.12c) and the swallowing pattern has a frequency between that of the pyloric and gastric mill regions. After the pyloric suppressor neurons have stopped firing, the new pattern persists for several tens of seconds and the original two pyloric and gastric mill rhythms are slowly re-established. This observation is important because it shows that circuits within the ganglion itself are reconfigured by activity in the pyloric suppressor neurons (Fig. 7.12b). If the stomatogastric ganglion neurons were all driven by bursts of spikes in the pyloric suppressor neurons during swallowing, we would expect the pyloric and gastric mill rhythms to be re-established as soon as the pyloric suppressor neurons stopped firing. The pyloric suppressor neurons reconfigure the circuits of the stomatogastric ganglion, so that neurons which previously participated in different and unco-ordinated activities now express a new, single pattern. Many of the details of how this reconfiguration is achieved remain to be worked out.

Essentials of Human Physiology

Essentials of Human Physiology

This ebook provides an introductory explanation of the workings of the human body, with an effort to draw connections between the body systems and explain their interdependencies. A framework for the book is homeostasis and how the body maintains balance within each system. This is intended as a first introduction to physiology for a college-level course.

Get My Free Ebook


Post a comment