Executive functions of the lateral giant neuron

A lateral giant not only initiates a tail flip, but also extensively co-ordinates the sequence of events involved. This executive function is achieved by a massive and widely distributed array of inhibitory effects that follow a spike in the giant axon. Pathways lead away from the lateral giant to exert inhibition at almost every point in the neuronal circuit generating a tail flip. The IPSPs produced at these points in the circuit differ from one another, in the delay to their onset and in duration, in such a way as to ensure that each part of the response begins and ends at the right time.

The extensor motor system is the first place where inhibition is seen following a spike in a lateral giant axon. This inhibition is accomplished by parallel actions at three points in the motor pathway to the extensor muscles: the muscle receptor organs, the motor neurons, and the extensor muscle fibres themselves. The muscle receptor organ is inhibited by a special accessory cell associated with its sensory neuron; and the fast extensor muscles are inhibited by a motor neuron that causes IPSPs in the muscle fibres, called the extensor inhibitor motor neuron. The lateral giant excites these two kinds of inhibitory neuron, and also inhibits the excitatory motor neurons of the extensor muscles (Fig. 3.5a). These inhibitory actions begin within a few milliseconds of a lateral giant spike; in fact, the delay to the onset of the IPSPs in the extensor motor neurons is as short as that of the EPSPs in the fast flexor motor neurons (Fig. 3.5b). The duration of the IPSPs produced at all three points in the extensor pathway is relatively short, having an average value of 30 ms.

These arrangements clearly function to ensure the accurate timing of the reflex extension following giant-mediated flexion. The early onset of this inhibition prevents premature activation of the extensor reflex from interfering with the initial flexion. Inhibiting the extensor pathway at three separate locations makes quite certain that extension cannot occur while the inhibition lasts. The average duration of the IPSPs at the three locations is about the same as the average duration of the giant-mediated flexion, and so the extensor system is released from inhibition just as flexion is completed. The inhibitory action of the lateral giant thus co-ordinates flexion and re-extension effectively, even though the extensor system does not receive any additional excitation from the lateral giant.

Co-ordination of the response is continued by inhibition of the flexor motor system while re-extension takes place. Two inhibitory neurons have been identified that are important in shutting down the flexor system: the inhibitory motor neuron which innervates every fast flexor muscle fibre; and the motor giant inhibitor, an interneuron which prevents the motor

Figure 3.5 Inhibition of the abdominal extensor muscles by the lateral giant. (a) Neuronal circuit generating inhibition of the extensors, showing representative neurons: the lateral giant (LG); fast extensor motor neuron (FE); extensor inhibitor (EI); the muscle receptor organ (MRO); and its accessory cell (AC). Inhibitory neurons are shown in solid black; excitatory (—and inhibitory (—•) connections are shown, but electrical and chemical synapses are not distinguished. (b) Typical recording used to build up the interpretation given in (a). The upper trace is an extracellular record from the motor nerve to the flexors, showing the lateral giant spike and subsequent compound spike from flexor motor neurons. The middle and lower traces are intracellular records showing, respectively, an EPSP in the extensor inhibitor and an IPSP in the fast extensor motor neuron. Note the short delay of the postsynaptic potentials after the lateral giant spike. (b from Wine, 1977; copyright Springer-Verlag.)

Figure 3.5 Inhibition of the abdominal extensor muscles by the lateral giant. (a) Neuronal circuit generating inhibition of the extensors, showing representative neurons: the lateral giant (LG); fast extensor motor neuron (FE); extensor inhibitor (EI); the muscle receptor organ (MRO); and its accessory cell (AC). Inhibitory neurons are shown in solid black; excitatory (—and inhibitory (—•) connections are shown, but electrical and chemical synapses are not distinguished. (b) Typical recording used to build up the interpretation given in (a). The upper trace is an extracellular record from the motor nerve to the flexors, showing the lateral giant spike and subsequent compound spike from flexor motor neurons. The middle and lower traces are intracellular records showing, respectively, an EPSP in the extensor inhibitor and an IPSP in the fast extensor motor neuron. Note the short delay of the postsynaptic potentials after the lateral giant spike. (b from Wine, 1977; copyright Springer-Verlag.)

giant from firing. Both of these inhibitory neurons are excited indirectly by the lateral giant (Fig. 3.6a). The motor giant inhibitor is strongly excited by the fast flexor motor neurons and so brings about inhibition of the motor giant very soon after the latter has fired. The flexor inhibitor is weakly excited by a variety of sources, including the fast flexor motor neurons and the corollary discharge interneurons, a class of interneurons which are excited by the segmental giants and with axons that run between segments. These sources of input bring about early depolarisation of the flexor inhibitor, but the threshold for spiking is reached only after the corollary discharge interneurons in other ganglia are recruited to provide additional input.

This roundabout pathway increases the delay, and consequently a spike is not triggered until about 15 ms after the spike in the lateral giant (Fig. 3.6b), by which time the motor giant is already inhibited. The actual flexion movement has only just begun at this time; but it must be remembered that it takes a few milliseconds for the muscles to develop tension and for the

Figure 3.6 Delayed inhibition of the fast flexor muscles by the lateral giant. (a) Neuronal circuit generating inhibition of the flexors, showing representative neurons as in Fig. 3.4 plus: the motor giant inhibitor (MoGI); corollary discharge interneuron (CDI); and flexor inhibitor (FI). Symbols have the same meaning as in Fig. 3.5, and chemical and electrical synapses are not distinguished. (b) Recording demonstrating the delayed activation of the flexor inhibitor. The upper trace is an extracellular record showing the delay between the spike in the lateral giant and the spike in the flexor inhibitor; the lower trace is a simultaneous intracellular record from the flexor inhibitor showing the compound EPSP gradually rising to threshold. (b from Wine & Mistick, 1977; reprinted by permission of Wiley-Liss, Inc., a subsidiary of John Wiley & Sons Inc.)

Figure 3.6 Delayed inhibition of the fast flexor muscles by the lateral giant. (a) Neuronal circuit generating inhibition of the flexors, showing representative neurons as in Fig. 3.4 plus: the motor giant inhibitor (MoGI); corollary discharge interneuron (CDI); and flexor inhibitor (FI). Symbols have the same meaning as in Fig. 3.5, and chemical and electrical synapses are not distinguished. (b) Recording demonstrating the delayed activation of the flexor inhibitor. The upper trace is an extracellular record showing the delay between the spike in the lateral giant and the spike in the flexor inhibitor; the lower trace is a simultaneous intracellular record from the flexor inhibitor showing the compound EPSP gradually rising to threshold. (b from Wine & Mistick, 1977; reprinted by permission of Wiley-Liss, Inc., a subsidiary of John Wiley & Sons Inc.)

tension to overcome inertia in the skeleton, so that by the time actual movement begins the electrical events that triggered the movement have already been completed. Hence, the delayed inhibition from the lateral giant prevents any additional flexor activity and prepares the way for reextension. In addition, the flexor inhibitor receives an excitatory, monosyn-aptic connection from the muscle receptor organ and this input becomes active as soon as the muscle receptor organ is released from inhibition. This input sums with that from the lateral giant, thereby prolonging activity of the flexor inhibitor for the duration of re-extension.

A further important place where inhibition acts is on the input side of the circuit, at the synapse between the hair receptors and the sensory interneu-rons. This inhibition acts both postsynaptic ally, on the dendrites of the interneurons, and also presynaptically, on the axon terminals of the receptor neurons. Presynaptic inhibition of this type is common in mechano-sensory systems, and its action is to reduce or prevent the release of neurotransmitter. Both postsynaptic and presynaptic inhibition are delayed to about 15 ms after the lateral giant spike due to the indirect pathway that mediates them, including the corollary discharge and other interneurons. This inhibition has a long duration of about 50 ms. However, not all the hair receptors are inhibited in this way; those that provide input to the extensor motor neurons are not inhibited and they contribute to the re-extension reflex.

The presynaptic inhibition of the first input synapse plays an important part in co-ordinating the startle reflex because abdominal flexion is a dramatic movement that stimulates the same receptors that trigger the reflex. If this input were not inhibited, it could cause a perpetual cycle of repeated tail flips by positive feedback. As it is, the onset of inhibition coincides with the onset of movement of the abdomen and so prevents this feedback effect. The long duration of the inhibition makes sure that a second tail flip is not triggered before the first one is completed. The occurrence of presyn-aptic inhibition at the first synapse is well correlated with the fact that this synapse is the site of habituation of the response. If postsynaptic inhibition alone were present, then synaptic transmission could still habituate during the repetitive stimulation caused by abdominal flexions, and this could render the whole system unresponsive for several hours. This habituation does not occur because presynaptic inhibition prevents the presynaptic terminals from being fully activated.

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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