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Interneurones Co Ordinating the Ventilatory Movements of the Thoracic Spiracles in the Locust

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jf. exp. Biol. (1982), 97, 385-400 IJ85

fcPjV/i 11 figures rrinted in Great Britain

INTERNEURONES CO-ORDINATING THE

VENTILATORY MOVEMENTS OF THE

THORACIC SPIRACLES IN THE LOCUST

BY MALCOLM BURROWS

Department of Zoology, University of Cambridge, Downing Street, Cambridge CBz 3F7, England

{Received 30 July 1981)

SUMMARY

A pair of interneurones has been identified by intracellular recording and staining which co-ordinates the movements of the thoracic spiracles in the ventilatory rhythm.

An interneurone has its cell body on the left or on the right side of the metathoracic ganglion and an axon which ascends to the other thoracic ganglia in the contralateral connective. Each interneurone produces bursts of spikes in time with the inspiratory phase of ventilation. These spikes evoke inhibitory post-synaptic potentials (IPSPs) in thoracic spiracular closer motor neurones. Both interneurones synapse upon the closer motor neurones in each thoracic segment. These connexions, which may be direct, inhibit the spiking of the closer motor neurones during inspiration.

The interneurones do not appear to have an innate rhythmicity but instead receive a periodic synaptic input which inhibits their spikes during expira-tion. The underlying cause of the spikes is less clear. Apart from brief periods at the start and end of a burst, the spikes occur at a constant fre-quency that is independent of the ventilatory rate.

The pattern of the spiracular motor output could be altered by manipulat-ing the frequency and number of spikes in an interneurone. When the frequency of spikes in the interneurone was raised, the motor bursts had a higher initial frequency and were of briefer duration; when the frequency was lowered, the motor bursts were of lower initial frequency and of longer overall duration. Altering the spikes in one interneurone, however, could not affect the frequency of the ventilatory rhythm, or reset the rhythm.

INTRODUCTION

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muscles in abdominal and thoracic segments. The abdominal muscles contract rhythmically to provide the propulsive forces that drive air around the complex network of tracheae. Muscles also control the aperture of the paired openings, the spiracles, on each abdominal segment. They contract rhythmically in time with ventilation opening during expiration and closing during inspiration. The thoracic muscles involved in normal ventilation are those which control the spiracles, causing them to open during inspiration and to close during expiration. A one-way circulation of air in the tracheae thereby results. When ventilation is stressed other thoracic muscles may be recruited that move the head rhythmically.

The dominant pacemaker for both the abdominal and thoracic movements is within the metathoracic ganglion (Miller, i960). In this ganglion are interneurones with a putative co-ordinating function whose axons either descend to the abdominal ganglia or ascend to the other thoracic ganglia. If the metathoracic ganglion is de-stroyed, individual abdominal ganglia can sustain a ventilatory rhythm, but the thoracic ganglia cannot. Some abdominal interneurones involved in ventilation are known by extracellular recordings from the connectives that link the abdominal ganglia (Lewis, Miller & Mills, 1973), and from intracellular recordings made in the metathoracic ganglion from one of them (Pearson, 1980). The output connexions of these interneurones are not known. By contrast the output connexions of two sets of thoracic interneurones have been described in some detail from intracellular record-ings made from pairs of spiracular and flight motor neurones (Burrows, 1975 a, b,

1981). One set, probably consisting of two interneurones, causes inhibition of spiracu-lar closer motor neurones during inspiration (Burrows, 1982). A second set probably of two interneurones is active during expiration exciting closer motor neurones and some flight motor neurones, as well as inhibiting spiracular opener motor neurones (Burrows 1975 a, b). In this paper the first set of thoracic co-ordinating interneurones has been identified by intracellular recording and staining. It is shown that there are two interneurones which make inhibitory synaptic connections with thoracic spiracu-lar closer motor neurones. Manipulation of the pattern of spikes in one interneurone alters the pattern of the motor output but not the frequency of the ventilatory rhythm itself.

MATERIALS AND METHODS

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Locust ventilatory interneurones

|bte with silver in a whole ganglion (Bacon & Altman, 1977). Drawings of a stained interneurone were made with a camera lucida. Transverse wax sections 10 /«n thick were made of the ganglia containing the stained neurones. The nomenclature of the longitudinal tracts within a ganglion is taken from the scheme devised by Gregory (1974) for the cockroach. All electrical signals were stored on magnetic tape using an FM tape recorder for later photography, or analysis with a DL 4000 signal processor (Data Laboratories Ltd., London). The description of the morphology is based upon three stains of the interneurone, and the physiology upon simultaneous recordings from an interneurone and a spiracular motor neurone in five locusts.

RESULTS

An electrode probing within the metathoracic ganglion posterior to the emergence of lateral nerves 3 encounters many neurones whose patterns of spikes or synaptic potentials are linked to the ventilatory rhythm. The majority subsequently prove to be motor neurones but some are interneurones. One particular type of interneurone, encountered on both the left and the right sides of the ganglion, produces bursts of spikes in time with the ventilatory movements of the thoracic and abdominal muscles. The activity of these interneurones can be related more precisely to the particular phase of ventilation by correlating their spikes with those recorded simultaneously in a motor neurone whose activity is already well known. A suitable motor neurone is a closer of the mesothoracic spiracles which produces bursts of spikes that start abruptly at the beginning of expiration and end before the onset of the next inspiration (Fig. 1 a). This burst of spikes is therefore a convenient indicator of the duration of expiration.

The spikes in one of these interneurones straddle both the expiratory and inspira-tory phases of ventilation (Fig. 1 a, b). The spikes begin in the second half of expira-tion and continue throughout inspiraexpira-tion at a steady frequency (Fig. 1 c). At the start of the next expiration there is an abrupt repolarization so that only an occasional spike in the interneurone overlaps the next burst of spikes in the closer motor neurone (Fig.ic).

Output connexions of the interneurones

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(a) int

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(c)

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Fig. i. Patterns of spikes during ventilation in a metathoracic interneurone and a mesothoracic spiracular closer motor neurone, (a) The burst of spikes in the closer motor neurone corre-sponds to the expiratory phase of ventilation; the silent period to inspiration. Using this activity as an indicator of the ventilatory cycle it can be seen that in the interneurone the spikes begin during expiration and reach a plateau during inspiration, {b, c) The alternation between the spikes in the interneurone and motor neurone is shown more clearly on expanded times scales. The period of inhibition in the motor neurone corresponds to the period of spiking in the interneurone. Recordings were made from the somata of both the interneurone (int) and the motor neurone (mn). Calibration: voltage, motor neurone 16 mV, interneurone 8 mV; time (a) 800 ms, (6) 400 ms, (c) 200 ms.

evokes IPSPs. There must always remain some uncertainty from physiological observations alone as to whether a connexion is direct, particularly in this example where the recording sites are 2 mm apart and separated by processes whose conduc-tion velocities are not known. Nevertheless, there can be little doubt that the connex-ion is chemically mediated as the IPSPs have a reversal potential (Burrows, 1982). Further evidence that the spikes in an interneurone evoke IPSPs in the motor neurone is derived by passing pulses of current into an interneurone to increase its frequency of spikes during inspiration (Fig. 2 d, e). The result is that the frequency of IPSPs in the motor neurone is increased accordingly, and the overall level of hyper-polarization is accentuated.

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Locust ventilatory interneurones

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Fig. 2. Spikes in an interneurone evoke hyperpolarizing synaptic potentials in a mesothoracic spiracular closer motor neurone, (a) A segment of a recording taken during inspiration to show the spikes in the interneurone (lower trace) and hyperpolarizing, potentials in the motor neurone (upper trace). (6, c) Spikes in the interneurone (upper traces) are used to trigger the sweep of an oscilloscope. Superimposing many sweeps reveals that an hyperpolarizing potential in the motor neurone accompanies each spike in the interneurone. (d, e) A depolariz-ing pulse of current is applied to the interneurone which raises the frequency of its spikes and increases the hyperpolarization in the motor neurone. This is more clearly seen at higher gain and on a faster time scale in (e). The occurrence of the next burst of spikes in the motor neurone is, however, unaffected by the manipulation administered to the interneurone. Calibration: voltage, motor neurone (a, b, c and e) 4 mV, (d) 16 mV, interneurone (a) 8 mV, (b, c) 4 mV, (d, e) 16 mV; current 10 nA; time (a, e) 100 ms (6) 16 ms, (c) 8 ms, (d) 200 ms.

that this interneurone also synapses upon these motor neurones. No other thoracic motor neurones or interneurones have been sought as possible targets for the output of this interneurone. The morphology of an interneurone (Fig. 4) suggests that it would not synapse upon abdominal neurones so that no search has been made for connexions with these.

Numbers of this type of interneurone

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de-Motor neurone

16 ms

Fig. 3. Signal averaging clearly reveals the connection between an interneurone and a meso-thoracic spiracular closer motor neurone. A spike in the interneurone triggers the signal processor to average events that occur both before and after the spike. Six successive averages of the hyperpolarizing potential each associated with the occurrence of 256 spikes in the interneurone are shown. Calibration: voltage, motor neurone 2 mV, interneurone 4 mV, time 16 ms.

pending upon the extent to which the frequency of spikes has been changed (Fig. ga,b). The simplest interpretation of these results is that there is a pair of symmetrically arranged interneurones which evokes the IPSPs; one with an axon in the left and the other with an axon in the right connective of the thoracic central nervous system.

Morphology of an interneurone

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Locust ventilatory internenrones 391

Piameter and lies within the ventral cortex of cell bodies. Its co-ordinates are given by a line drawn across the ganglion level with the anterior edge of the main nerve to the hind leg (nerve 5) and an antero-posterior line from the middle of the ipsilateral anterior connective. The primary neurite runs medially and dorsally from the cell body to form a short expanded segment on the midline of the ganglion and level with the anterior edge of nerve 3 (Figs. 4, 5). The majority of neuropilar branches arise from this expanded segment. They are profuse and extend from the expanded segment to form a roughly circular area with a radius of 300 ftm, when viewed dorsally. The branches which have a narrow and even diameter extend to both the left and right sides of the ganglion.

The majority of the branches in this region are restricted to the neuropile of the first abdominal ganglion which is fused to the metathoracic ganglion (Fig. 5 a). A few extend into the neuropile of the metathoracic segment at the level of the expanded segment (Fig. 5 c, d), whilst the more anterior branches are clearly within the dorsal neuropile. Within the first abdominal segment there are branches around both the dorsal and ventral edges of the neuropile (Fig. 5 c). The axon also arises from the expanded segment approximately at the level of the section shown in Fig. 5 c. It runs diagonally to the side of the ganglion opposite to the cell body and then turns anteriorly to enter the Lateral Dorsal Tract (Fig. 5 a, b). The axon continues to run anteriorly in this tract and eventually enters the anterior connective where it occupies a position in the dorsal-lateral quadrant. Before entering the connective however, the axon gives rise to some medially and some laterally directed branches in the most dorsal region of the neuropile (Figs. 4, 5 a). These have an appearance quite distinct from the branches arising more posteriorly. They are sparsely branched and with an uneven diameter along their length which lends them a beaded appearance. There is almost no overlap between these sparse anterior branches and the more profuse posterior ones.

Within the mesothoracic ganglion the branches of an interneurone are more sparse. The majority are restricted to the same side of the ganglion as the axon, but some project across the midline particularly in the more posterior regions. Many branches project to the same regions of the neuropile as do the branches of the spiracular closer motor neurones (see Burrows, 1982). The axon enters the pro-mesothoracic connective but has, as yet, not been traced to the prothoracic ganglion.

Inputs to the interneurones

Currents of increasing intensity applied to an interneurone progressively reduce the number of spikes and reveal a persistent and rhythmical fluctuation of the mem-brane potential in time with ventilation (Fig. 6a-c). The'memmem-brane is gradually depolarized during one expiratory phase, reaches a peak when the excitatory synaptic input to a spiracular closer motor neurone stops and is usually maintained at this level during inspiration (Fig. 66, c). Throughout the depolarizing phase there are small fluctuations probably caused by synaptic potentials. However, no single sequence of synaptic potentials can be identified in these intrasomatic recordings as the cause of the overall depolarization.

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Fig. 4. A drawing of an interneurone stained with cobalt and intensified with silver. The whole mount of the metathoracic ganglion is viewed dorsally. Not all of the enormous number of fine branches are included. Lateral nerves 1, 3, 5 and 6 only are drawn. Letters (a-f) indicate the position of sections shown in Fig. 5.

time as the depolarization in a closer motor neurone (Fig. 6d, e). The inputs to the interneurone now occur in waves similar to the excitatory waves in a spiracular closer motor neurone (Fig. 6d, e). When the waves are particularly prominent in the two neurones, it appears that they are common and evoked by the same presynaptic intei neurones. When the interneurone is hyperpolarized the waves decrease in amplitude and reach an apparent reversal potential, indicating that they are inhibitory synaptic potentials.

Patterns of spikes in an interneurone

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Fig. 6. Inputs to an interneurone. (a) The interneurone (lower trace) is hyperpolarized with a steady current of o-2 nA. Most spikes are abolished but the ventilatory rhythm continues in it and in a mesothoracic spiracular closer motor neurone (upper trace). (6) The hyper-polarizing current is increased to 1-2 nA and all spikes are abolished to reveal a membrane potential that fluctuates in time with the ventilatory rhythm, (c) The shape of the underlying waveform can be more clearly seen at a slower time scale, (d, e) The motor neurone is hyper-polarized so that its depolarizing synaptic potentials can be compared with the simultaneous hyperpolarization of the interneurone. Calibration: voltage, motor neurone i6mV, inter-neurone (a, 6) 16 mV, (c-e) 8 mV; time (a, b) 200 ms, (c, d) 400 ms, (e) 100 ms.

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400 ms Fig. 9. Altering the pattern of spikes in an interneurone changes the pattern of spikes in a meso-thoracic spiracular closer motor neurone, (a) The normal pattern, with no manipulation of the membrane potential of the interneurone (lower trace). Note the ' beats' of the IPSPs during inspiration in the motor neurone (upper trace). (6) The interneurone is depolarized by the application of a steady current of 1 -o nA. The IPSPs no longer show beats, (c) The inter-neurone is hyperpolarized with a steady current of C5 nA to reduce the number and frequency

of its spikes, (d) The interneurone is further hyperpolarized with a current of i'5 nA to abolish all spikes. The recordings were made sequentially in one locust. Calibration: voltage; motor neurone 16 mV; interneurone 8 mV.

next expiration. The spikes that do not overlap with expiration occur at a steac frequency. For example, at a ventilatory rate of 1-2 Hz the spikes in one interneuroi occurred at 66 Hz (Fig. 7 a). The small amount of deviation from this basic frequent is revealed by a histogram of the intervals between 5000 spikes in approximately i< bursts (Fig. 76). The histogram is narrow with most intervals between 12 and 20 n (corresponding to instantaneous frequencies of 83 and 50 Hz) and with a peak 15 ms (66 Hz). There is a tail of longer intervals caused by the spikes at the beginnir and end of each burst.

The number of spikes in a burst is, however, variable as is the duration of tl ventilatory cycle itself. For example, in one locust examined, the number of spik ranged from 25 to 58, although the basic frequency of spikes in either the short or i the long bursts remained the same. The number of spikes is correlated (correlatic coefficient = 092) with the duration of the ventilatory cycle (Fig. 8a): the shorti the ventilatory cycle the fewer spikes in each burst of the interneurone.

Effects of an interneurone on motor output

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Locust ventilatory interneurones

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Fig. io. The structure of a burst of spikes in a mesothoracic spiracular motor neurone is altered by changing the frequency of spikes in an interneurone. The interval between success-ive spikes in one expiratory burst of the motor neurone is plotted against spike number. The interneurone is at its normal resting potential (A), depolarized by i nA (Q) and hyper-polarized by 1-5 nA (O). The arrows point to the first and last spikes of the bursts when the interneurone is depolarized or normal. The motor neurone spikes throughout inspiration when the interneurone is hyperpolarized.

interneurone and the duration of the ventilatory cycle (Fig. 86). Occasionally mani-pulation of the frequency of spikes in an interneurone is correlated with a change in the ventilatory rhythm. These occasional correlations can be attributed to unpredicted changes in the ventilatory rhythm and are therefore not causal correlations. Likewise, pulses of current injected into an interneurone have no detectable effect upon the timing of the next phase of ventilation whether they occur during expiration and increase or decrease the level of polarization, or during expiration and increase (Fig. zd) or decrease the frequency of spikes. In other words, the ventilatory rhythm is not reset by these manipulations of an interneurone.

Nevertheless an interneurone can have quite pronounced effects on the form of the motor output of the spiracular closer motor neurones. When an interneurone spikes in its normal pattern there are usually few if any motor spikes during inspiration (Fig. 9 a). The expiratory burst of spikes begins at high frequency, continues with the spikes in groups and then declines slowly in frequency (Fig. io). When the inter-neurone is depolarized, the level of hyperpolarization in a motor inter-neurone during inspiration is increased (Fig. gb) and the frequency of spikes at the start of expiration is increased (Fig. io). The duration of the burst is reduced because it is terminated earlier by the higher frequency of spikes in the interneurone (Fig. 96, 10). There is no effect upon the pattern of spikes in the middle of the expiratory burst.

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throughout inspiration at a frequency inversely related to the number of spikes in the interneurone (Figs. 9c, d; 10). The initial frequency of spikes during expiration is now lower and the burst itself is prolonged. The transition from expiration to inspira-tion is also more blurred.

DISCUSSION

The interneurones described here co-ordinate the movements of the thoracic spiracles in the ventilatory rhythm. They would appear from physiological evidence to synapse upon spiracular closer motor neurones in each segment evoking synaptic potentials that are chemically mediated and inhibitory. The result is to inhibit spikes in these motor neurones during inspiration. The spiracular closer motor neurones are unusual in that their axons divide within an unpaired median nerve to innervate muscles on both the left and the right sides of the body. Both anatomical and physiological evidence indicates that the interneurones themselves are also sym-metrically arranged in the central nervous system. The most parsimonious interpreta-tion of the common IPSPs in the two closer motor neurones of one segment is that they are evoked by just two interneurones. Thus one interneurone has its soma on the left side of the metathoracic ganglion and its axon in the right anterior connective, whilst the other interneurone has its soma on the right and its axon on the left. Further symmetry is added by the fact that the two interneurones each synapse upon the two closer motor neurones in a particular segment. The co-ordination of the ventilatory rhythm in the thoracic spiracles, particularly in the mesothorax where there are only closer motor neurones would thus appear to be quite simple. The two interneurones described here are responsible for the inhibition during inspiration and probably two, yet to be identified but inferred from the synaptic potentials they evoke (Burrows, 19756), are responsible for the excitation leading to spikes during expiration.

The interneurones which convey the ventilatory rhythm to the motor neurones would appear, in turn, to be driven by other interneurones. During expiration they receive an inhibitory synaptic input which usually abolishes their spikes. This input begins before the end of the preceding inspiratory phase and persists at the start of the next inspiratory phase. The effect is to lengthen the intervals between the spikes of an interneurone on both occasions. The inhibitory input appears to be derived from the same source as that which excites spiracular closer motor neurones and some flight motor neurones and which inhibits some inspiratory motor neurones (Burrows 1975 a, b). The underlying cause of the burst of spikes at a steady frequency during inspiration is less clear. An applied hyperpolarization fails to give clear evidence of a causal synaptic input. Thus it cannot be said whether an interneurone is actively depolarized by a synaptic input, or simply returns, following the cessation of the inhibitory input, to a membrane potential that is lower than the threshold for spike initiation. It was not possible to examine the interneurone in the absence of a ventilatory rhythm to determine whether it would then produce spikes at the frequency observed during the plateau phase of inspiration.

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Locust ventilatory interneurones

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Fig. 11. A diagram to show the sequence of activity during ventilation of some ventilatory motor neurones, and the interneurones described here and by Pearson (1980). The shaded areas indicate the frequency of spikes. In the thorax, the motor output of the prothoracic median nerve is shown. This nerve contains the motor neurones to the opener and closer muscles of the spiracles. In the abdomen, the motor output cf a lateral nerve is shown. This nerve innervates both inspiratory and expiratory muscles. Only one of each type of inter-neurone is shown.

other as judged by the IPSPs it produces in the closer motor neurones. Moreover, the IPSPs in the motor neurones show 'beats' indicating that the spikes in the two interneurones are not closely linked.

The tests so far employed do not reveal any inherent rhythmicity in the neurones. Pulses of depolarizing or hyperpolarizing current applied to an inter-neurone are without effect upon the ventilatory rhythm. This limited test also indicates that an interneurone is unable to affect directly, or by altering the motor output and hence the sensory feedback, other interneurones involved in producing the ventilatory rhythm. By contrast, pulses of current injected into an interneurone which conveys the ventilatory rhythm to the abdominal part of the nervous system, can reset this rhythm (Pearson, 1980). This abdominal interneurone can also alter the frequency of the ventilatory rhythm if it is depolarized or hyperpolarized (Pearson, 1980), but similar tests applied to a thoracic interneurone revealed no consistent effects. Nevertheless the thoracic interneurones do control the pattern of the motor output by influencing both the duration of the expiratory bursts of spikes in the closer motor neurones, and their initial frequency.

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Despite good descriptions of the pattern of activity in abdominal motor neurones^ (Lewis et al. 1973; Hustert, 1975), of thoracic spiracular motor neurones (Miller, i960; Burrows, 1978; 1981), of a presumed abdominal co-ordinating interneurone (Pearson, 1980) and here of thoracic interneurones, no speculation is worthwhile as to the mechanism by which the rhythm is itself generated. Clearly the task now at hand is to identify more interneurones and describe their interactions.

This work was supported by N I H grant 1RO1 NS16058-01.

REFERENCES

BACON, J. P. & ALTMAN, J. S. (1977). A silver intensification method for cobalt-filled neurones in wholemount preparations. Brain Res. 138, 359-363.

BURROWS, M. (1975a). Co-ordinating interneurones of the locust which convey two patterns of motor commands: their connexions with flight motoneurones. J. exp. Biol. 63, 713-733.

BURROWS, M. (19756). Co-ordinating interneurones of the locust which convey two patterns of motor commands: their connexions with ventilatory motoneurones. J'. exp. Biol. 63, 735-753.

BURROWS, M. (1978). Sources of variation in the output of locust spiracular motoneurones receiving common synaptic driving. J'. exp. Biol. 74, 175-186.

BURROWS, M. (1982). The physiology and morphology of median nerve motor neurones in the thoracic ganglia of the locust, jf. exp. Biol. 96, 325-341.

GREGORY, G. E. (1974). Neuroanatomy of the mesothoracic ganglion of the cockroach Periplaneta americana (L). I. The roots of the peripheral nerves. Phil. Trans. Roy. Soc. Lond. 267, 421-465. HOYLE, G. & BURROWS, M. (1973). Neural mechanisms underlying behavior in the locust Schistocerca

gregaria. 1. Physiology of identified motorneurons in the metathoracic ganglion. J. Neurobiol. 4,

3-41-HUSTERT, R. (1975). Neuromuscular coordination and proprioceptive control of rhythmical abdominal ventilation in intact Locusta migratoria migratorioides. J. comp. Physiol. 97, 159-179.

LEWIS, G. W., MILLER, P. L. & MILLS, P. S. (1973). Neuro-muscular mechanisms of abdominal pumping in the locust. J. exp. Biol. 59, 149-168.

MILLER, P. L. (i960). Respiration in the desert locust. I. The control of ventilation. J. exp. Biol. 37, 224-236.

PEARSON, K. G. (1980). Burst generation in coordinating interneurons of the ventilatory system of the locust, y. comp. Physiol. 137, 305—313.

Figure

Fig. 2. Spikes in an interneurone evoke hyperpolarizing synaptic potentials in a mesothoracicCurrentspiracular closer motor neurone, (a) A segment of a recording taken during inspiration to show
Fig. 8. (a) Graph to show the relationship between the number of spikes in an interneuroneand the duration of the ventilatory cycle (measured from the start of one expiratory burst of
Fig. io. The structure of a burst of spikes in a mesothoracic spiracular motor neurone isSpike numberaltered by changing the frequency of spikes in an interneurone
Fig. 11. A diagram to show the sequence of activity during ventilation of some ventilatorymotor neurones, and the interneurones described here and by Pearson (1980)

References

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