the motor pattern of locusts during visually induced rolling in long-term flight

Biol. Cybern. 56, 397-410 (1987) Biological Cybernetics �9 Springer-Verlag 1987

The Motor Pattern of Locusts During Visually Induced Rolling in Long-Term Flight

J. Schmidt and W. Zarnack

1. Zoologisches Institut der Universitfit G6ttingen, Berliner Strasse 28, D-3400 G6ttingen, Federal Republic of Germany

Abstract. Desert locusts (Schistocerca gregaria F.), mounted in a wind tunnel on a low-mechanical- impedance torque meter, flew for at least 30 min in the posture typical of long-term flight. As they flew, they were induced to rotate about their long axis (roll) by rotation of an artificial horizon. All maintained depar- tures from the horizontal attitude were brought about actively, by the animal's own efforts. In the roll maneuver, the hindlegs and abdomen were bent toward the side ipsilateral to the direction of rotation. However, these "rudderlike movements" were not adequate to initiate and maintain a constant roll angle.

During a roll, there was a change in the pattern of excitation of all the wing muscles that were monitored: the depressors M81, 97, 99, 112, 127, and 129, and the elevators M83, 84, 89, 113, 118, 119 (numbering according to Snodgrass 1929). Hence all 12 muscles probably not only provide power for the flight but also steer it. Evidently, then, for these muscles a rigid distinction between power and steering muscles is not appropriate.

The period of the contraction cycle changed in correlation with the roll angle, but was not a parameter for control of the roll maneuver, because the changes were the same in all muscles (Fig. 2).

Even with constant burst length, the phase shifts between the muscles changed. These changes were the main control parameter for rolling (Figs. 3-9).

There was a latency coupling between elevators and the following depressors (Fig. 3).

The changes in phase shift were tonic or phasic (sometimes phasic-tonic) in different muscle pairs (Fig. 4).

When a roll angle of ca. 15 ~ was adopted, the phase shifts between depressor muscles in a given fore- or hindwing (e.g., M127R vs. M129R) changed by about 5 ms, whereas the elevators changed by less than 1 ms (Fig. 6).

The phase shifts between the anterior elevators and depressors of a given wing, as well as the posterior

elevators and depressors, changed by ca. 5 ms (in some cases with different time courses) when the animal rolled to an angle of ca. 15 ~ (Fig. 7).

The changes in phase shift between muscles of the fore- and hindwing on one side of the body amounted, as a rule, to about 4 ms at ca. 15 ~ roll (Fig. 8).

Corresponding muscles on the two sides of the body change in phase with respect to one another by as much as 10 ms (Fig. 9). The phase shifts of all such contralateral muscle pairs except for the posterior basalar muscles, M127, have the same sign, such that the muscle ipsilateraI to the direction of rotation becomes active sooner.

1 Introduction

Neurophysiological studies of locust flight since Wil- son and Weis-Fogh (1962) have had one of two general goals: on one hand, to explain the central nervous and sensory mechanisms of pattern generation (Wilson 1968; Wendler 1974; Robertson and Pearson 1984; Reichert and Rowell 1985) and on the other, to clarify the role of the skeletal muscle system in producing the wing movements and, through them, the aerodynamic forces. In addition to analysis of the functional morphology of the muscles (Pfau 1977,1978,1982), attempts were made to learn about the parameters involved in the steering of flight by recording the neuromuscular excitation pattern, sometimes with simultaneous recording of wing movements. Taking the latter approach, Wilson and Weis-Fogh (1962) were at first concerned with unaccelerated straight-ahead flight. M6hl and Zarnack (1975, 1977a, b) and Zarnack and M6hl (1977a) studied the motor pattern during changes of course, by imposing yaw rotation on flying animals. Zarnack (1982) expanded the instrumentation to allow high-resolution three-dimensional recording of the wing movements, and thereby clarified controversial

398

questions of functional morphology. Baker (1979) and Th/iring (1986) caused the animals to generate torque actively by presenting visual stimuli. Dreher (1982) studied the behavior in a closed-loop situation with respect to flight speed. Elson and Pfliiger (1986) examined the function of the pleuroalar muscles in animals subjected to imposed roll.

But each of these studies on flight steering were conducted under specific restrictions. (a) The aerodynamic conditions of free flight were preserved inade- quately or not at all. (b) The control circuits were opened. (c) The aerodynamic reaction could not be measured.

Consequently, the results of these experiments do not apply without qualification to the situation during free flight. We have therefore modified the experimental setup by having locusts fly in the airstream of a wind tunnel. Within the tunnel, the animal was surrounded by an artificial horizon (as used by Wilson 1968). When tilting the horizon elicited a roll response, the animal could change its attitude about the long axis because it was mounted on the rotatable arm of a torque meter with low mechanical impedance. With this arrangement, all the restrictions listed above are avoided. We have now analyzed the excitation pattern of almost all flight muscles during roll movements visually induced in this way, and some of our results differ considerably from those recently published by Thiiring (1986). The experiments are intended as a first step in a complete analysis of the overall flight motor system that has been made possible by methodological innovations (Waldmann 1986).

2 Materials and Methods

The animals used in these experiments were 20 adult Schistoeerea gregaria (F.) from the colony in the First Zoological Institute of the University of Grttingen.

In each individual, the activities of 12 muscles (elevators and depressors, Table 1) were recorded

Table 1. Flight muscles from which recordings were taken

Forewing Hindwing Muscle name

Depressors 97 127 First basalar 98 128 Second basalar 99 129 Subalar 81 112 Dorsal longitudinal

Elevators 83 I 13 First tergosternal 84 Second tergosternal 89 118 Anterior tergocoxal 90 119 First posterior tergocoxal

extracellularly by 12 steel electrodes (30 gm diameter, insulated to the tip). The reference electrode was placed in the first abdominal segment.

The animals were fastened with wax, by the ventral surface, to a roll meter - a torque meter that permitted them to rotate actively about the long axis of the body (i.e., to roll). The field of view on both sides was divided to represent a horizon, which could be rotated. In the laminar airstream of a heated wind tunnel (28~ 18 cm nozzle diameter, wind speed ca. 2.3 m/s) the locusts flew steadily for at least 30 rain (Fig. la).

Roll Meter. Roll angle was measured by a torque meter made of 3-mm-thick brass rods set in ball bearings (Fig. la), which was adjusted so that the animal was able to roll out of the horizontal attitude by overcom- ing a restoring torque approximately proportional to roll angle (ca. 1.7 x 10 -~ N x m for 45 ~ roll). This torque was recorded electrically as a measure of the induced roll. With an animal mounted on it, the meter had an eigenfrequency of ca. 0.7 Hz and a logarithmic decrement of 0.44__+ 0.01.

It should be emphasizedthat the animals were not in a state of neutral equilibrium; any angle to the horizontal that they adopted had to be maintained actively.

Artificial Horizon. The horizon (Fig. 1 a) was simulated by a cylinder (diameter 25 cm, length 25 cm) colored black over half its inside circumference and white over the other. The animals flew on the cylinder axis. Above them, in the middle of the white half, were mounted two miniature fluorescent tubes ("Kolibri", Seitner; diameter 9.3 mm, length 104 mm) with a large spectral UV component. The cylinder rested on two rollers, one of which could be turned by a motor. By operation of the motor both the tilt angle of the horizon and the tilting velocity could be adjusted.

Data Processing. The amplified muscle-potential sig- nals (EMG), the horizon angle and the torque reading were recorded on analog magnetic tape with 14 FM channels. From this tape, the data were digitized for computer processing. By means of spike detectors (Zarnack and Mrhl 1977a, b; Waldmann 1986), three numbers were assigned to each muscle potential - the channel number, which identified the muscle, the time of occurrence of the peak (accurate to 64 gs), and the amplitude.

2.1 Definitions

The following definitions are used here. Period: The period P is the time separating the first

potential discharged by a given muscle in each of two consecutive wingbeat cycles (Fig. 2a).

399

electro - m y o g r a m [ ~ >

roiling batance

horizon E ~ b

H ,..-~_; W

amplifier

no!12

angutar 1 transducer

motor sensor

motor- control

Fig. la and k Arrangement of apparatus. A Angle transducer, B ball bearing, H horizon, L lamp, M motor, W wind. Further details in text

I ~J magnetic

Z~I tape station

f 14

muttiptexer

oscilloscope

14.. _J data acquisition " -1 processor

computer

Phase shift: In locust flight, over the times considered here, the period (and hence the frequency) is approximately the same in all the muscles that have been monitored (see Sect. 3.2.1.1). Therefore the con- cept of phase shift, defined as the difference in phase between two periodic quantities of(approximately) the same frequency [Burkhardt (1971) W6rterbuch der Neurophysiologie, ~Phasenverschiebung], can be ap- plied to the contraction cycles of two muscles. Here we express phase shift as the time (in ms) separating a given phase of the two cycles.

3 Results

3.1 General Behavioral Observations

In general, the locusts flew very calmly and persis- tently. Some of them flew steadily for as long as four hours. Only experiments with at least 30 rain of steady flight were evaluated; during such flight Schistocerca gregaria exhibits the typical flight posture previously

described for Locusta migratoria (Zarnack 1969). The femora of the forelegs are held upright, with the tibiae pressed back against them, in the groove between head and thorax. The middle pair of legs is extended backward next to the body. The jumping legs also lie close to the body, with the tibiae folded against the femora.

Almost every quietly flying animal could be induced to roll by tilting the artificial horizon. Most animals exhibited, to varying degrees, a kind of dorsal light reflex (the sensory basis of which was not pursued here). However, some individuals did not turn so that the back was toward the light, but rather turned away from it. Only a few animals had symmetrical roll behavior; most followed preferentially one of the directions of horizon tilt.

During roll, the positions of the hindlegs were altered. As a rule the femur on the side toward which the animal was rolling was held out at an angle to the body, often with extended tibia. The abdomen was also

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[ms] Fig. 2a-f. Period time series calculated for the activities of the anterior ( M 8 3 R / L ) and posterior ( M 1 1 3 R / L ) first tergosternal muscles (elevators) and the right posterior subalar muscle (M129R), during roll maneuvers induced by rotation of an artificial horizon. Each dot represents the period of one cycle of muscle contraction (i.e., one wingbeat). The angle of roll away from the horizontal, which is proportional to the torque exerted, is given in degrees�9 The rotation of the artificial horizon is the same for all experiments: 30 ~ left, centered, 30 ~ right. Muscle numbering according to Snodgrass (1929); see Table I

bent in the roll direction. When the wings are not beating, this "rudderlike" (Camhi 1970) posture of legs and abdomen does not produce a rolling movement; therefore, as Thiiring (1986) also inferred, this posture can have only a subordinate function.

Each roll maneuver was accompanied by changes in the neuromuscular pattern of excitation in the flight musculature, and hence in the wing movement�9 There- fore, in view of the ineffectiveness of leg and abdomen movements, it must be this excitation pattern that produces the roll.

The dynamic as well as the neuromuscular reaction always took place with a delay of seconds, as observed previously by Wilson (1968). During imposed rotation in the yaw mode, on the other hand, the neuromuscular reaction appears within at most two wingbeat cycles (M6hl and Zarnack 1977a).,

3.2 Changes in the Neuromuscular Excitation Pattern

Four neuromuscular parameters are known to be involved in the control of flight: (i) the wingbeat period (Gewecke 1972), (2) the phase shift (Zarnack and M6hl 1977a), (3) the burst length (Wilson 1968), and (4) the number of motor units recruited in a muscle (Wilson and Weis-Fogh 1962). As our method provides little information about the last of these, it will not be considered further here.

In our experiments rolling was always accompanied by a change in phase shift of all the muscles observed, and very often a change in period, but rarely in burst length. Hence changes in the excitation pattern are manifest primarily as altered phase relations between the various flight muscles and an altered wingbeat period, though the latter cannot be a controlling parameter in the case of roll (see below).

In the following sections, the period and the phase shifts between selected pairs of muscles are analyzed. (With 9 muscles for each wing, phase shifts can be measured for 28 x 36=1008 muscle pairs.) We are concerned with

(I) phase shifts with respect to a reference muscle, (2) phase shifts between muscles of a single wing, (3) phase shifts between muscles of the fore- and

hindwings on one side of the body, and (4) phase shifts between corresponding muscles of

the right and left wings. The changing phase shifts are first represented as

time series. Because many of the phase relations defined by phase shifts are tonic, for these we ignore the time factor and plot them as histograms.

At this point we should mention a general problem: the amount of phase shift between corresponding muscles on opposite sides of the body is almost always unequal even during horizontal flight. For the present

401

it cannot be determined whether such asymmetries are also present in a free-flying animal or whether - as is more likely - they are ascribable to the restrictions imposed by the experimental conditions.

3.2.1 The Time Series

From a flight lasting many minutes, a sequence of 50 s is evaluated (Figs. 2-4) during which the animal re- sponds to rightward rotation of the horizon, after a delay of ca. 10 s, with a rapid roll to the right. The animal follows leftward rotation of the horizon with a shorter delay. The roll velocity is probably reduced by the inertia of the roll meter.

Recordings were taken from four elevator muscles - the anterior M83R/L and posterior Ml13R/L (the first tergosternal muscles on both sides) - and two depressors, the right anterior first basalar muscle M97R and posterior subalar muscle M129R. The burst lengths are constant.

3.2.1.1 Contraction-Cycle Period. The period of a muscle-contraction cycle is calculated by the formula

P = t(mxx, n + 1) - t(mxx, n),

where Mxx identifies the muscle, and n is the cycle number. The periods in consecutive cycles were calculated for all the muscles listed above (Sect. 3.2.1); examples are shown in Fig. 2.

All muscles have the same period in any given wingbeat cycle. Therefore period is not a controlling parameter for roll maneuvers. Because it changes identically in corresponding contralateral muscles (e.g., M83R vs. M83L), the period of the contraction cycle cannot be responsible for asymmetry with respect to the median plane, either in the wing movements or in the resulting torque.

In general, as in the examples illustrated, changes in period are correlated with changes in roll angle. But these changes follow no discernible rules- for instance, with respect to the sign of the change. For this reason, again, period cannot be a controlling parameter.

In the examples of Fig. 2 there are oscillations in period that have not yet been explained. They are not due to oscillations of the meter system.

3.2.1.2 Phase Shifts with Respect to a Reference Muscle. We now turn to the phase shifts TA and TB (Fig. 3c and d) of the fore- and hindwing elevators M83R/L and M113R/L and of the right forewing depressor M97R with respect to the hindwing depressor M129R, which has a very regular contraction cycle. Here

rA=t (Mxx , n)--t(M129R, n) (Fig. 3c)

TB = t(Mxx, n + 1) -- t(M129R, n) (Fig. 3d)

in which Mxx is the muscle under study, t is the time and n is the cycle number.

The distinction between TA and TB is useful only when the relations between elevators and depressors are being considered, for in this case One does not know whether a particular cycle begins with the activity of the elevator or that of the depressor. For the relations between depressors (e.g., M97R-M129R, Fig. 3a), only TA is calculated. Positive values of TA indicate that the muscle Mxx is activated after the muscle M129R. For example, a phase shift of ca. 10ms in Fig. 3a signifies that M97R is active ca. 10ms later than M 129R.

The phase shifts in Fig. 3 were calculated from the same sequence that was evaluated for Fig. 2. It is evident that the phase shifts TA change with roll angle, in either a phasic (Fig. 3a; may be phasic-tonic, as the two cannot be clearly distinguished at present) or tonic (Fig. 3e-h left side) manner. The changes in phase shift are muscle-specific and amount to between 2ms (Fig. 3g) and 12 ms (Fig. 3a); these changes thus vary considerably more than those observed with imposed yaw (Zarnack 1982).

The phase shifts TB (i.e., between the reference muscle and the following elevators) are illustrated in Fig. 3e-h (right side). Surprisingly, these phase shifts parallel the changes in period, as can be seen by reference to the period time series for muscle M129R reproduced above (Fig. 3b). The fluctuations in phase shift are evidently phase-locked to those in period.

These observations confirm the existence of a latency coupling between elevators and following depressors (Hedwig and Pearson 1984). This coupling is not rigid, however, but is modulated in correlation with the roll movement. It follows that the phase shifts between elevators and depressors are controlling parameters for roll maneuvers.

3.2.1.3 Phase Shifts Between Selected Muscle Pairs. Zarnack (1982) showed that the changes in activity of a wing depressor have a direct physiological relevance to the movements (and hence to the aerodynamics) of flight. Furthermore, the coupling between the wings on one side of the body (traces of which are reflected in the phase shifts between anterior and posterior depressors) is very important aerodynamically.

We therefore checked whether during active roll movements phase shifts can be found resembling those in imposed yaw (Zarnack 1982). The results are first presented as sample time series, with special emphasis on relations with elevator muscles. These time series are taken from the same 50-s section of a long flight considered above.

Figure 4 illustrates phase shifts between the following muscle pairs:

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- elevators and depressors of a single wing (Fig. 4a and b), - anterior and posterior depressor (Fig. 4c), - anterior elevator and posterior depressor (Fig. 4d), - posterior elevator and anterior depressor (Fig. 4e), - posterior and anterior elevator (Fig. 4t), - corresponding contralateral anterior and posterior elevators (Fig. 4g and h).

Remarkably, the change in phase shift between an elevator and a following depressor is phasic in the forewing (Fig. 4a) but tonic in the hindwing (Fig. 4b). Thiiring (1986) found no phase-shift changes at all in such muscle pairs�9

The changes in phase shift between muscles of the fore- and hindwings on one side (Fig. 4c-f) are similar in magnitude to those between corresponding contralateral muscles (Fig. 4g and h).

It should also be mentioned that phase shifts of M97 with respect to other muscles in some cases have no phasic component (Fig. 5).

3.2.2 Behavior a t a Stabilized Roll Angle

The few (18 of ca. 1000 possible) combinations shown so far were selected to illustrate the time-dependence of the pattern changes. We shall now proceed to docu- ment all the combinations we can for which there seems to be some rationale. Because most of the phase relations are tonic, the phase shifts associated with a given roll angle after any transients have disappeared can be presented in histogram form. It should be emphasized once again that to fly at any angle other than horizontal the animals must overcome a restoring

404

a M99R - MSTR [] 3 ~ ~:i:i 7 ~

S0 40 ii::i

30 . i:i:

0 . . . . , ; i . , 0 I0 Ig

d MgOR - H89R D I 0 ~ i:i:i 1 0 ~

G0 ::~ii so 7i 40 ~

2o3~ L 0 i ' ' : - " . . . . . . t . . 1

S I0 IS

gMII2R - MI29R D 6 ~ i:~:i I0 ~

4oS~176176 i 3O

20

10

0 .... i .... i

-S 0 S

b ~99L - M97L [ ] 8 ~ i:i:i 1 G ~

40 iiii:,

20 iiiiiiil to 0 ii i! . . . , -I0 -S 0 S

C MSgL - M92L [ ] 1 3 ~ i:i:: G ~

s0

40 i:~i 30 !:i:'~ 20 i:i:!:i~

I lii::! _

-IO -S 0

e MgOR - M84R f M89R - M84R D 10 ~ i:~:Z 10 ~ [ ] I0 ~ i:i:i 10 ~

4~ 30 20

to

0 .... I'~l

0 S I0 IS

h MI27R - MI29R Z] 10 ~ 13!6 ~

40

30

20

tO

0 . . . . . . . . . : ! . , -S 0 S I0

I H127R - HI29R

H [~0]

40

30

20

10

0 . . . . I . . . . I

-S 0 S 10

LRTEHCY [ ms ]

40 30 20

I0

0 0 S I0

i Mt27L - MI29L 0 I0 ~ i : i : i 6 ~

G0

s0 iiili

30

20

I0

0 . . . . I

-S 0 S tO

S

[ ] l e f t ::iii!?: righL

k ~l18L - MI IgL D 6 ~ i:i:! I0 ~

70 iiil

GO :::: !iii

50 ::::

30 20 I0

0 . i: I -S 0 S

m MI27L - MI29L n MIISL - MIlgL 5~ 40

30

20

I0

0 ' ' ' F " ~ ' ' ' �9 I . . . . l

- 5 S 10

6O

40

30

20

I0

0 I . . . . i . . . . i

- 5 0 5

Fig. 6a-n. Steady-state (constant roll angle) phase shifts between depressors (a-e) or elevators (d-f) of a forewing and between depressors (g-i, 1 and m) or elevators (k and n) of a hindwing. Dotted histograms: roll to the right; hatched: horizontal; otherwise roll to the left. The locust symbol represents the animal as seen from behind. The data were obtained from several individuals; histograms for a given flight sequence can be identified by the identical roll angles indicated above them. The histograms in b and e were also obtained from a single individual. For each histogram ca. 200 consecutive wingbeat cycles (corresponding to 10 s of flight) were evaluated

torque. Each h is togram is based on ca. 200 wingbeats (about 10 s of flight).

3.2.2.1 Phase Shifts Between Muscles of a Single 14qng. Steering movements of a wing - by which is mean t depar tures f rom the wingbeat for unaccelerated for- ward hor izonta l flight - can be p roduced actively only by the muscles a t tached to this wing.

T h e R e l a t i o n s B e t w e e n T w o D e p r e s s o r s or T w o

Elevators. As an animal changes its roll angle, there are

indeed changes in the phase shifts between depressor muscles of a single wing - Fig. 6a -c and g- i illustrates them for the anter ior depressors M99 and M97, as well as for the poster ior depressors M112, M127, and M129 - a l though Thfiring (1986) observed no altered phase shifts of these muscles. Fur thermore , the h indwing depressors M127 and M129 exhibit the expected inverse changes in phase shift on the right and left sides (compare h and i in Fig. 6), such that M127 and M 1 2 9 on the side contralateral to the roll direction are active

405

almost synchronously. The indirect depressor M112 is active at almost the same time as M129 regardless of the animal's attitude (Fig. 6g).

There are at most slight changes in phase shift between the forewing elevators M84R, M89R, and MgOR, or between the hindwing elevators M118L and M119L (Fig. 6d, f, g, and k). It is likely, therefore, that the wing upstroke has little significance in steering movements. It is also evident that in the horizontal position M l l 9L is active sooner than M118L (Fig. 6n), whereas otherwise - in both leftward and rightward roll - it is active somewhat later.

The Elevator-Depressor Relation. Changes in phase of the upper and lower reversal points of a wingbeat that are correlated with steering movements (Waldmann 1986) should be reflected in different phase shifts between elevators and depressors, depending on whether the roll is to the right or left. Figure 7 illustrates such phase shifts for various hindwing elevator-depressor combinations (elevators Ml13, M l l 8, Ml19 versus depressors M127 and M129). The difference in phase shift can be as great as 4 ms (e.g., M118L-M127L, Fig. 7a).

With respect to the direction of the shift, contralateral pairs behave oppositely: in rightward roll the phase shift between M118L and M129L is shorter, and that between MI18R and M129R longer, than in

leftward roll. The phase shift between Ml18L and M129L is about the same (20 ms) in leftward roll as in the horizontal position; however, no similar asymmetric behavior with respect to the horizontal is observed in the corresponding muscle pair on the right side.

3.2.2.2 The Phase Shifts Between Fore- and Hindwing Muscles on the Same Side of the Body. In general, the phase shifts between fore- and hindwing muscles vary depending on the animal's attitude (Fig. 8), which reflects a variability in the coordination of the two ipsilateral wings (e. g., with respect to wingbeat phase) that is an important factor in the steering of flight (Zarnack 1982). The muscle pair M99R and M129R provide an exception to the rule (Fig. 8b), for their phase shift remains constant. The anterior depressor M97 has a different phase shift with respect to M129 than does M99, for both right and left roll (Fig. 8a, b).

On the side contralateral to the roll direction, M83 is active before Ml13 (Figs. 8d and e and 40. It is therefore doubtful whether the hindwing always leads the forewing by 5-10ms (Wilson and Weis-Fogh 1962); it may well be that the phase relation between fore- and hindwing varies depending on the roll angle. Perhaps the forewing on the side contralateral to the roll direction reaches its lower reversal point before the hindwing.

a 17118L - MI27L b MIIgL - MI29L C MIISL - MI29L d MIISR - MI29R

[ ] G ~ i:;:i 10 o @ ~ 3O 2O 10

0 . . . . I . . . . I . . . . 1

-30 -25 -20 - IS

so ~ !ij

3O 2O 10

:i:.. 0 . . . . I . . . . I . . . . I

-30 -2S L20 -15

60

50

40

SO

I0

0 . . . . I . . . . I

-25 -20 -15

6O

20

10 0 ~ : i~ . . . , -30 -25 -20 - I~

e

M

60

50

40

30

20

10

0

HIIgL - M127L

[%]

ii!i: v.w.

,....,.o v..,.o :.:.:.:.

: < , : . :

, . , y . . . r . . . . . . . . . .

: . : . : , : . . , . . . . . . .

: . : . : . : . : . : . , . ,

' ' 1 . . . . I

-2S -20 -IS

LATEHCY [ms]

f MItSR l M 129 ~ El8 ~ ~8 ~

70

60

so ::i::i

3O

0 ' :7'7~ -30 -25 -20 -15

g MIISL - MISgL

6O

40 30 20 tO

0 . . . . . . . -25 -20 -1S

h MIISR - MI2~R

G0 50 40 30 20 I0

0 . . . . F ~, . . . . , -30 -25 -20 -15

Fig. 7a-h. Steady-state phase shifts between elevators and depressors in the same hindwing. Except for Ml13R-M129R, all the data come from the same animal. Each histogram is based on ca. 200 consecutive wingbeat cycles. (For further details see Fig. 6)

406

70

60

60

40

30

20

I0

0

Rg?R - HI2gR b 03 ~ ~ 7 ~

40

30

20

i',i iii[ ,o I ' ' ' ' l . . . . . . . . I 0

0 S tO 16

H99R - Mi2SR

n 3 ~ i:!:! 7 ~

S tO 15 20

C r183R - I'I!29R [ ] 8 ~ !:!C! 8 ~

6O

" I ,o

3o

10

0 " " ' ' ' I " . . . . . . . I

-30 -.S -2o -iS

d r183R - HII3R

o 8 ~ i;~:i 8 ~

7O

S0

4o iiil 30 .<~?

iii,, to :{:i!

0 " ' ' 1

- 5 0 5 1O

e t183L - MII3L [%]

D8 ~ ~8 ~

60

50 i~ ,o! 30

20

10

0 J~" ~J!~ . . . . I

- 0 10

LRTEHCY [ms ] Fig. 8a-e . Phase shifts between musctes of different wings on one side of the body . E a c h histogram is based on ca. 200 consecutive wingbeat cycles. (For further details see Fig. 6)

3.2.2.3 The Phase Shifts Between Corresponding Con- tralateral Muscles. There are large changes in phase shift between corresponding muscles on the two sides of the body (M97, 83, 127, 129, 113, 118; Fig. 9 ) - about 8ms, for instance, in the example of Fig. 9b (M83L-M83R; see also Fig. 4g).

As a rule, in rightward roll the right muscle is active before its counterpart on the left, and the opposite is true for leftward roll. The phase shifts illustrated for M97 are not symmetrical about the zero point, but the changes associated with right and left roll tend to follow the rule. The first basalar muscle, Ml27, is a

a

60

SO

4O

30

20

tO

0

['192L - MSTR

[] 3 ~ i:i:i 7 ~

i!i~;

ii~Ji!!

0 S tO 1S

conspicuous exception, with phase-shift changes opposite to those of all the other muscle pairs. Again, these results are not consistent with those of Thfiring (1986), who found that all muscle pairs in the hindwings changed phase shift in a direction opposite to those of the forewings.

4 Discussion

The aerodynamic forces in locust flight are based on a complicated three-dimensional stroke-and-torsion oscillation of four wings. The depressors of the fore-

b M83L - M83R D 8 ~ i:i~ 8 ~

60 ::::,

4o #

0 I �9 ',:1: .1... ' I " ' " ' " " " 1 " ; ' ; ' ; ' I

- tO -6 0 S 10

C

80

70

6O

SO

40

30

20

,0

0

MI2~L - MI29R d rqlo ~ ~ o

~ 70 13

i!!i 6o

iii " 40

3O

iiii .o

iiiiii:. ,0 .-.v.-.,

' ' ' I . . . . I . . . . I 0

-5 S tO

LRTEMCY [ms]

H127L - M127R 0 tO ~ !:!:i ~~

e MII3L - MII3R

o 8 ~ ~:!::' 8 ~

f MI I8L - r1118R o5 ~ ~ io ~

0 S 10

6O

SO

40

30

20

I0

0 . . . . I . . . .

- tO - 6

6O

, . . . . . .

:i:?i:i 30

!!ili!ii 2o . . . . . . . .

#~i!ii::y V " , " , ' �9 I 0 . . . .

S -S

�9 . . , . � 9

�9 . . . . . . . . . . , . . . ,

: . : . : < . : . : + : . . . . . . . - . v . - . ,

I . . . . I . . . . I

S l0

Fig. 9a-f. Steady-state phase shifts between corresponding contralateral depressors and elevators of the forewing (above) and the hindwing (below). Each histogram is based on ca. 200 consecutive wingbeat cycles. (For further details see Fig. 6)

407

wing not only pull it forcefully downward but also, simultaneously, rotate it by varying amounts about its long axis. Thus the aerodynamic lift could be varied by at least two parameters - wingbeat amplitude and pronation.

In other words, lift and propulsion are controlled by a number of movement parameters, which in turn derive from a well-coordinated pattern of activity in a total of 40 flight muscles. Hence it remains a rare achievement to be able to infer conclusively that a particular change in the excitation and movement patterns will produce a particular change in the aerodynamic forces. In principle, therefore, we find it absolutely necessary that analysis of a particular flight mode, such as roll, be based not on the activity of a single steering muscle (e.g., a pleuroalar muscle), but on simultaneous recordings of as many as possible of the muscles involved in flying.

In the present paper we analyze the pattern of excitation in a large number of flight muscles - including the elevators, which have previously received little attention - with the aim of identifying the essential neuronal parameters of flight control during roll.

The temporal pattern of coordination of flight- muscle activity exhibits typical changes during active roll maneuvers by the locust. Burst length in general remains constant. Changes occur in the phase shifts between almost all the muscles investigated, confirm- ing their role as an extremely important steering mechanism (M6hl and Zarnack 1975, 1977a; Zarnack and M6hl 1977a). By altering the wing movements and the reciprocal coupling of the wings on one side of the body (Zarnack 1982, 1983), such changes in phase shift produce the roll.

Changes in phase shift are observed between direct depressors and between the depressors and elevators of a (fore- or hind-) wing. On the other hand, the phase shifts between elevators of a given wing are largely unaltered during roll maneuvers. Changes in phase shift between a forewing muscle and a hindwing muscle on the same side of the body are clearly discernible in the combinations depressor-depressor, elevator- elevator and depressor-elevator.

The combinations with the greatest phase-shift changes, 10 ms, involve corresponding contralateral muscles (depressors or elevators) of the fore- or hindwings. These changes have also been described previously by other authors for visually induced flight maneuvers (Wilson 1968; Baker 1979; Taylor 1981; Thfiring 1986; Schmidt and Zarnack 1986).

Thiiring (1986) in addition studied the phase shifts in the forewing muscles, in the combinations depressor-depressor and elevator-depressor, and found no changes while the animal was exerting roll-

mode torque. It is also notable that the change in phase shift between corresponding contralateral muscles that were observed in Thfiring's experiments were not only distinctly smaller than in ours- in some cases only 1/10 as large - but also had a different time course (see 4.3.3) in the hindwing musculature (except for the first basalar muscle, M127).

How can these discrepancies be explained? For one thing, the aerodynamic conditions during the experiments were completely different; our animals were flying in a wind tunnel, and Th/iring's were not. Moreover, her animals were operating under open- loop conditions with respect to rotation of the horizon, whereas in ours the control circuit was closed, for our animals could adjust their attitude with respect to the horizon by actively rolling whenever it was tilted.

The aerodynamic conditions under which flight experiments are conducted in the laboratory are of fundamental importance for application of the results to the process of free flight. When animals are flying without an airstream, the flow mechanics are entirely different than in free flight. Consequently, Thfiring's results are not in themselves sufficient for an interpretation of natural flight events, in view of the following considerations:

(a) Let us suppose that the excitation patterns are controlled only by visual inputs. In that case Thtiring would have measured the excitation pattern of free flight, but the aerodynamic moments of torque would have been different from those in free flight; the airflow past a rotating propeller is different when the airplane is waiting for takeoff than when it is in the air, and the aerodynamic forces produced in the two situations differ correspondingly. It follows that one cannot reliably deduce the effects of changes in the excitation pattern upon force production, as long as so little is known about the aeredynamics of locust flight. In this case, then, the relevance of the measured reactions to free flight is uncertain.

(b) On the other hand, if the aerodynamic as well as the visual surroundings contribute to flight control- as is suggested by studies of antennae, frontal hairs and various mechanosensors (Gewecke 1972; Heinzel 1982; Heukamp 1983) - the excitation patterns would be different from those in free flight.

The aerodynamic conditions in our experiments very closely approach those in free flight, and one result is that many animals flew for several hours. The dynamic response of the animals, turning voluntarily about the long axis of the body, is clearly elicited by the visual stimulus, although we do not know whether the crucial feature was the overall brightness distribution or the contrast at the horizon line.

408

4.1 Implications of the Results

The mechanism by which phase-shift changes between any two muscles affect flight attitude depends on whether the muscles act on the same wing, on the two wings on a side, or on contralateral wings. These aspects will now be considered separately.

4.1.1 The Muscles of a Single Wing

The aerodynamic action of a change in the movement of a single wing is the easiest to comprehend. In general, changes in pronation alter the aerodynamic angle of attack (Zarnack 1982; Waldmann 1986) and hence the force produced by the wing. For this reason, the phase relations of depressors to one another, elevators to one another, and depressors to elevators (all belonging to the same wing) are of fundamental importance to the understanding of flight control.

Thfiring (1986) examined the depressor combi- nation M98-M99 and the depressor-elevator combi- nation M97-M84 and, finding no phase-shift changes, concluded that phase changes between the muscles of a single wing are not involved in roll maneuvers. There is clearly an inconsistency between our results and those of Thfiring, for which we have no explanation. In particular, it is not certain whether in this case the abovementioned differences in aerodynamic conditions are responsible.

The Depressor Activities. In the combinations of depressors of a single wing studied here (M97 M99, M127-M129, M112-M129) we find phase changes of up to 5 ms (Fig. 6i), greater than those found for yaw by Zarnack and M6hl (1977a), who expressed the phase relations with reference to a temporal mean. Zarnack (1982), whose evaluation procedure was adopted here, also found (perhaps because the yaw rotation was imposed rather than voluntary) considerably smaller phase changes between the depressors of a single wing.

The changes in phase of the first basalar muscle, M97, with respect to other muscles are conspicuous for the following reasons:

(1) apparently there is no functionally fixed phase relation to the subalar muscle M99, for in different individuals either of the two muscles may lead on the side ipsilateral to the direction of roll. For instance, in one individual M97R preceded M99R in a roll to the right (Fig. 6a), and in another M99L led in a roll to the left (Fig. 6b). In another flight sequence, M97 was active before M99 during leftward roll, and when the same individual rolled to the fight the sequence was reversed. Similar variability was observed in the yaw experiments of Zarnack (1982), but in other experiments that also used imposed yaw (Zarnack and M6hl 1977; M6hl 1985) M97 was always active before M99.

In view of the fact that the subalar muscle M99 is a synergist of the first basalar muscle, M97, not only during the downstroke but also during pronation (Pfau 1977, 1978, 1982; Zarnack 1982)the sequence of activation of these muscles may be relatively unim- portant. That they are not completely interchangeable, however, is suggested by their insertions on different sclerites. Furthermore, for complete execution of the downstroke the first basalar muscle is essential whereas the subalar muscle has only an accessory function (Zarnack 1982).

(2) There is also remarkable variation in the time course of the change in phase shift between the M97 and any of the other elevators and depressors. For instance, the change in phase with respect to M129 was tonic in one individual (Fig. 5) and phasic (-tonic) in another (Fig. 4c). The changes in phase shift between other muscle pairs are typically tonic in all individuals. There is, however, the qualification that phasic (-tonic) behavior in the present case (Fig. 4c) cannot be distinguished with absolute certainty from tonic behavior with a marked nonlinear transfer characteristic. It should be noted that prolonged, stable flights are required for a phasic response with such a large time constant to be detected at all.

The Elevator Activities. The phase shifts between depressors and elevators (of a single wing) change considerably (Fig. 7), whereas those between the elevators of a wing change slightly if at all (Fig. 6d-f and k). Similarly, in intracellular recordings only small variations in phase between the elevators were found (Hedwig and Pearson 1984). These results fit well with the finding that the greatest changes in movement occur during the downstroke (Zarnack 1982; Wald- mann 1986).

Hedwig and Pearson (1984) also noted a strong coupling between elevators and the following depressors in a ganglion. In our experiments, an ad- ditional coupling between motoneurons of the meso- and metathoracic ganglia is indicated (Fig. 8d and e). The coupling is manifest in intracellular recordings as a constant latency, while in our experiments there is a functional relationship between the roll torque produced and the phase shift under consideration. The depressor:elevator relation additionally reflects the independent variation in period.

4.1.2 The Phase Shifts Between the Wings on One Side of the Body

During roll maneuvers (as was also found for imposed yaw: Zarnack and M6hl 1977a; Zarnack 1982) there are variable phase shifts between the anterior and posterior muscles on one side of the body (e.g., M97R-M127R, Fig. 3a). These are the basis of vari-

ation in the degree of aerodynamic coupling of the fore- and hindwings on one side during the downstroke (Zarnack 1982, 1983); their implications for movement physiology have not previously been adequately interpreted.

It should be recalled that either the anterior or the posterior elevator may lead, depending on the turn being executed (Fig. 7). It may be, then, that the hindwing does not lead in the upstroke in every flight mode (Wilson and Weis-Fogh 1962).

4.1.3 The Phase Changes Between Corresponding Contralateral Muscles

For all combinations of corresponding contralateral muscles, the changes in phase shift are the largest (10ms) observed in the entire study. At present, unfortunately, we can offer no plausible interpretation of this finding, because the degree of aerodynamic coupling between contralateral wings has not been investigated.

In our experiments the leading muscle is routinely that on the side ipsilateral to the direction of rotation. The only exception is M127. According to Thiiring (1986), both M127 and M129 on the ipsilateral side follow their contralateral counterparts. Perhaps the aerodynamic conditions are responsible for these disparate results.

It is striking, however, that in both studies the behavior of the posterior first basalar muscle is opposite to that of the anterior muscle, although the movements of the anterior and posterior central fields are very similar (Zarnack 1982, 1983; Schwenne and Zarnack 1986). Too little is known about the hindwing joint for any definitive solution of this apparent anomaly.

4.2 Concluding Remarks

It has been shown that in all the aerodynamically important components of the flight system - the individual wing, the two wings on the same side of the body, and the paired right and left wings - the excitation patterns can be extensively altered. The most important control parameters for roll, as for yaw, are changes in phase shift of the muscle-contraction cycles. These produce changes in the wing movements (Zarnack 1982; Waldmann and Zarnack, in prepara- tion). Because the excitation patterns of all 12 muscles studied were found to change, a strict categorization of locust flight muscles as power or steering muscles is not appropriate. Only the pleuroalar muscles, M85 and M114, because of their position and small size, appear to be exclusively steering muscles.

The electrophysiological findings presented here must be supplemented by combined electrophysiolog-

409

ical and kinematic studies (Waldmann and Zarnack 1986).

Acknowledgements. We are very grateful to Prof. Dr. N. Elsner for his extremely generous support of our project, and to Prof. Dr. K. G. G6tz for critical reading of the manuscript. The work was funded by the Deutsche Forschungsgemeinschaft, under the grants Za 86/2-3, E1 35/12.

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�9 behavior in flight. I. Patterns of time shift. J Comp Physiol A 118:215-233

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Received: January 26, 1987

Dr. W. Zarnack 1. Zoologisches Institut der Universit~it Berliner Strasse 28 D-3400 GSttingen Federal Republic of Germany

the motor pattern of locusts during visually induced rolling in long-term flight

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