Triggering and maintaining escape swimming in Tritonia

Some of the first intracellular recordings from nerve cells in an animal behaving in a more-or-less normal pattern were made from Tritonia (Willows, Dorsett & Hoyle, 1973). By exposing the brain through a small incision and then fastening it to a support platform, intracellular recordings can be made from single neurons. The animal is suspended in a tank of seawater and can perform normal muscular movements. This experimental technique allowed identification of motor neurons and interneu-rons that are involved in local withdrawal reflexes as well as in the dorsal and ventral movements that occur during escape swimming (Fig. 7.9a). Ideas about the neuronal mechanisms that control escape swimming have been revised quite radically a number of times, and both the behaviour and the neuronal circuits that mediate it are more simple than those involved in locust flight.

A swimming episode lasts up to a minute, and consists of four to seven cycles of alternating bursts in dorsal and ventral flexion neurons. As in locust flight, interneurons generate the rhythm and communicate it to

Box 7.2. The neuromodulator octopamine

Octopamine, like some other amines, has a wide variety of effects on behaviour. In lobsters, injection of octopamine into the blood causes an animal to adopt submissive behavioural postures, whereas another amine, serotonin, causes a lobster to behave aggressively (Kravitz, 1988). There is considerable interest in elucidating the roles of these substances in behaviour: do they help prepare the body of an animal for certain kinds of behaviours, or do they also act as the triggers for particular behavioural acts? In locusts, octopamine has widespread effects. For example, it activates pathways that metabolise fat to provide energy during flying; it increases the responsiveness of pro-prioceptors such as the wing hinge stretch receptor; and it potentiates transmission at connections made by the stretch receptor in the central nervous system (Orchard, Ramirez & Lange, 1993). It is released from some of the dorsal unpaired midline (DUM) neurons which are thought to release octopamine from diffusely placed swellings of their axons rather than from conventional synapses. In (a), a DUM cell in the third thoracic ganglion of a locust was stained by intracellular injection. Sites of octopamine release, if any exist, are unknown in the central nervous system. One effect, which octopamine mediates directly on the contractile proteins, is to increase the rate of relaxation following a twitch. This is shown in recordings of twitches by the muscle that extends the hind tibia of a locust (b). Each twitch is caused by a spike in this muscle's slow motor neuron. Support for a role for DUM neurons in preparation for particular movements comes from the observations that some DUM neurons are active before and during flight (Ramirez & Orchard, 1990), and others are active just before a kick by the hind legs (Burrows & Pfluger, 1995). (a modified after Watson, 1984; b modified after Evans & Siegler, 1982.)

Control rw\r

Ig tension

With octopamine

0.5s

Figure 7.9 Escape swimming in the sea slug (Tritonia). (a) Swimming consists of several alternating dorsal and ventral flexion movements. These movements do little to propel the animal through the water; they lift it from the substrate, and it is carried by water currents. (b) The pattern of connectivity between interneurons involved in generating the program for swimming. In each side of the brain, receptors, including chemoreceptors, excite DRI, the dorsal ramp interneuron. The swim rhythm is generated by a network involving three dorsal swim interneurons, (DSIs), two ventral swim interneurons (VSIs), and one C2 interneuron. (c) Intracellular activity recorded simultaneously from a DSI, C2 and DRI during a swim episode, caused by electrical stimulation of a sensory nerve. At the start of the swim, the DSI is excited strongly, and its excitation declines slowly in a ramp-like manner during the swim. The source of this excitation is the DRI. (d) Modulation of the strength of a synapse from C2 to a motor neuron by activity in a DSI. A short burst of spikes in C2, elicited by intracellular stimulation, caused an EPSP in the motor neuron. When stimulation of C2 was preceded by stimulation of a DSI for several seconds, the size of the PSP caused by C2 increased dramatically. A similar increase was also produced by bathing the brain in seawater containing serotonin. (b and c modified after Frost & Katz, 1996; copyright National Academy of Sciences, USA; d from Katz etal., 1994; reprinted with permission from Nature; copyright © 1990 Macmillan Magazines Ltd.)

motor neurons. Three groups of interneurons on each side of the brain are involved in rhythm generation: three dorsal swim interneurons, two ventral swim interneurons, and one other interneuron called C2 (Fig. 7.9b). None of these interneurons has an intrinsic capacity to generate rhythmical oscillations in membrane potential, and the rhythm is generated by a circuit of linked interneurons. In an isolated brain, electrical stimulation of a nerve elicits a very similar pattern of intracellular activity to that which occurs in an intact animal that is swimming in response to starfish odour (Fig. 7.9c).

The swim neurons are strongly excited at the start of a swim. As the swim progresses, the excitation gradually diminishes and the cycle period becomes longer. A single interneuron on each side of the brain collects input from sensory neurons and conveys the excitation to the swim inter-neurons (Frost & Katz, 1996). The interneuron is called the dorsal ramp interneuron (DRI) because its excitation decays in a slow, ramp-like manner during a swim. Excitation of the DRI always precedes that of other interneurons before a swim starts. During a swim, a DRI continues to spike, with a brief interruption during each ventral flexion caused by an inhibitory synapse from the ventral swim interneurons. Stimulating a DRI with enough current to make it spike at similar frequencies to those that occur during a swim will trigger swim activity in the network. There are similarities between a DRI and some of the wind-sensitive interneurons of the locust flight system. Both respond to the same sensory stimuli that trigger a particular motor pattern, and electrical stimulation of the neurons triggers the pattern. However, the DRI is unlike any single wind-sensitive interneuron in that swimming will not start unless it is excited. If hyperpolarising current is injected into a DRI so that the DRI does not spike when a peripheral nerve that normally elicits swimming is stimulated, swimming does not begin. Also, ramp excitation of the three swim inter-neurons does not occur. If a DRI is hyperpolarised after a swim has started, the swim episode stops. The DRI, therefore, acts as a channel through which all sensory excitation must pass in order to activate the central pattern generator for swimming.

Each DRI makes excitatory connections with the three dorsal swim inter-neurons, which play a dual role in generating the program for swimming (Katz, Getting & Frost, 1994). First, the dorsal swim interneurons contribute to the pattern of each cycle of the rhythm through their synaptic connections with the ventral swim interneurons and with C2. Second, they sustain the rhythm because the neurotransmitter that they release, serotonin, has multiple effects within the network. Not only does serotonin act as the neurotransmitter at the output synapses made by a dorsal swim interneuron, it also increases the excitability of C2 and enhances the release of neurotransmitter from C2. For example, the EPSPs which C2 mediates in a motor neuron increase in amplitude when a dorsal swim interneuron is excited (Fig. 7.9d). The facilitatory action which the dorsal swim interneurons exert on the output synapses from C2 is called intrinsic neuromodulation, because the neuromodulator is released by neurons that are intrinsic to the pattern-generating network and is only released when the pattern generator is active. The neurons of the swim generator are also involved in less dramatic, local withdrawal responses. When swimming starts, the dorsal swim interneurons generate an intense burst of spikes, and it is likely that the serotonin which this releases ensures that the network is configured to generate co-ordinated, rhythmical swimming movements.

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.

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