Interneurons of the flight generator

None of the motor neurons contributes to the generation of the flight rhythm, and one good functional reason is that motor neurons, and there fore muscles, can be used independently of each other. This is important during steering, and during some movements of the legs in which muscles that also move the wings are involved. The regular waves of depolarisation that occur in motor neurons during flight must, therefore, originate in interneurons and be communicated to the motor neurons by synaptic transmission. Mel Robertson, Keir Pearson and others have characterised many different interneurons which show cycles of rhythmical activity, similar to those in motor neurons, during fictive flight. All of these inter-neurons generate spikes, and the interneurons generally produce a greater number of spikes per wing-beat cycle than the motor neurons. At the end of an experiment, stain is injected into a neuron so that its structure can be examined. In the thorax, about 85 different types of interneuron that are active during flight have been distinguished. All of the interneurons exist as bilateral pairs. Some probably belong to groups in which individual members have not been distinguished from each other, so that the total number of interneurons involved in the flight rhythm probably exceeds 100. The interneurons that form the central pattern generator for flight are distributed among several ganglia, and most of them branch extensively in both the second and third thoracic ganglia. In male crickets, which have very similar flight machinery to locusts, the forewing muscles are used for singing as well as for flying, and different interneurons are responsible for the two motor programs (Box 7.1).

There are two criteria for establishing whether an interneuron is part of the central pattern generator. First, it must be rhythmically active at the flight frequency; and, second, injection of a brief pulse of current into it should reset the flight rhythm. If an interneuron plays a role in generating the flight rhythm, a brief pulse of depolarising current injected into it will reset the rhythm by delaying or advancing the time of subsequent bursts of spikes (Fig. 7.3c), not only in the interneuron but also in flight motor neurons. Whether a pulse of depolarising current delivered to an interneuron advances or delays the time of the next wing-beat cycle depends on the phase of the cycle in which the stimulus current is delivered. Experiments of this type are called phase-resetting experiments. They reveal whether or not a particular neuron is involved in the clock mechanism that determines the timing of cycles in a rhythmically repeating activity. However, they do not reveal the exact mechanism for generating the rhythm.

One interneuron, number 301, is shown in Fig.7.4a. This neuron has its

Box 7.1. The control of singing in crickets

Male crickets sing by slightly elevating their forewings (a), and repeatedly rubbing a comb-like file on one against a hardened scraper on the other, shown by the cross-section through a cricket's thorax in (b). The pattern of activity in some wing muscles is very similar to their activity during flying. In Teleogryllus, during singing the wings move initially at 20 Hz, and later speed up to 35 Hz. Muscles that elevate the wings in flight cause wing closure and a pulse of sound during singing; and muscles that depress the wings in flight cause opening during singing. Despite this, different interneurons are involved in generating the two behaviour patterns. The pattern of intracellular activity recorded from motor neurons is different in the two behaviours and some interneurons are active during one activity but not the other (Hennig, 1990). This is illustrated by the recording in (c), which shows an interneuron producing clear rhythmical activity during singing, but not after flight was initiated by a puff of wind. This finding was surprising because it had been assumed that, because the two behaviours were similar, the same interneurons would be involved in generating the rhythms for flying and for singing. However, the evolution of singing behaviour must have involved the development of new neuronal circuitry. (b after Kutsch, 1969; c from Hennig (1990), copyright Springer-Verlag.)

Singing Flying

Figure 7.4 Interneurons of the central pattern generator for flight. (a) The anatomy of interneuron 301 in the second and third thoracic ganglia. The neuron was stained by injection of dye from an intracellular electrode. The cell body is indicated by the arrow. (b) Excitatory connection from interneuron 301 to interneuron 501, demonstrated by simultaneous intracellular recordings from the two neurons. Multiple sweeps of the oscilloscope are overlain, each triggered by a spike in 301. (c) Inhibitory connection from 501 to 301. (d) Schematic circuit representing the excitatory (+) and inhibitory (—) connections between 301 and 501. (Modified after Robertson & Pearson, 1985.)

Figure 7.4 Interneurons of the central pattern generator for flight. (a) The anatomy of interneuron 301 in the second and third thoracic ganglia. The neuron was stained by injection of dye from an intracellular electrode. The cell body is indicated by the arrow. (b) Excitatory connection from interneuron 301 to interneuron 501, demonstrated by simultaneous intracellular recordings from the two neurons. Multiple sweeps of the oscilloscope are overlain, each triggered by a spike in 301. (c) Inhibitory connection from 501 to 301. (d) Schematic circuit representing the excitatory (+) and inhibitory (—) connections between 301 and 501. (Modified after Robertson & Pearson, 1985.)

cell body in the second thoracic ganglion, and many branches both in this ganglion and the third thoracic ganglion. Another interneuron, number 501, is arranged the other way round, with its cell body in the third thoracic ganglion. Intracellular recording from 501 shows that this interneuron is excited at the same time as depressor motor neurons in each wing-beat cycle. Interneuron 301 is excited slightly before the activation of depressor motor neurons.

When intracellular recordings from interneurons 301 and 501 were examined in detail, interactions between the two interneurons were found. Consistency in these interactions is shown by overlaying several sweeps on the oscilloscope. Each sweep is triggered from a spike in one of the inter-neurons. A spike in 301 is always followed, after a delay of 6 ms, by a small depolarising potential in 501; and a spike in 501 is always followed, after 3 ms, by a brief, hyperpolarising IPSP in 301 (Fig. 7.4b, c). Allowing for time for neuronal signals to be conducted to the recording sites, the delay of only 3 ms in transmission from 501 to 301 suggests that this connection is direct, or monosynaptic. The greater delay in the connection from 301 to 501 leaves room for at least one additional neuron to be involved.

These two neurons form part of a circuit that could generate bursts of activity (Fig. 7.4d; Robertson & Pearson, 1985). Excitation of 301 leads to excitation of 501, after a short and fixed delay; and 501, in turn, inhibits 301 and terminates its burst of spikes. If 301 were excited from another source, it would become active again once 501's excitation had died away, and the circuit would reverberate on its own. There is some evidence that the circuit can work in this way because, in some experiments, steady excitation of 301 by current injection causes steady, rhythmical activity in 501 and in flight motor neurons. However, it is not feasible to perform the critical test of isolating this circuit from others in the thoracic ganglia. The circuit is just one of many that have been found in the flight pattern generator. It is unlikely that any single interneuron is indispensable for generating the flight pattern.

The mechanism by which 301 excites 501 has not been fully elucidated. An interneuron called number 511 is known to be interposed between 301 and 501 (Fig. 7.5). Neuron 301 inhibits 511, which in turn inhibits 501. This implies that the delayed excitation which 301 causes in 501 is by way of two successive inhibitions, a kind of interaction called disinhibition. However, for disinhibition to work in this circuit, it is necessary for 511 to cause continuous, tonic inhibition of 501. This would mean that its membrane potential was continually depolarised above the threshold for its synapses to release transmitter. Only in this way can a discrete inhibitory potential in 511, caused by a spike in 301, be converted into a discrete depolarising potential in 501. Physiological characteristics of the depolarising potential in 501 suggest that it is caused by a reduction in inhibition rather than by a conventional excitatory synapse. However, we do not know whether output synapses from 511 release transmitter tonically, without requiring spikes.

The circuit in Fig. 7.5 represents a small part of the central pattern generator for flight, and allows glimpses into its mode of operation. Wind on the head activates pathways that excite 206. Interneuron 206 excites elevator motor neurons through 504, and causes delayed excitation of depressor motor neurons through 301. As explained above, a feature of the flight program is that the duration of bursts of spikes in depressor motor neurons

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