Zoologisches Institut, Universität zu Köln, 50923 Cologne, Germany
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ABSTRACT |
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Fischer, Hanno, Joachim Schmidt, Roman Haas, and Ansgar Büschges. Pattern Generation for Walking and Searching Movements of a Stick Insect Leg. I. Coordination of Motor Activity. J. Neurophysiol. 85: 341-353, 2001. During walking, the six legs of a stick insect can be coordinated in different temporal sequences or gaits. Leg coordination in each gait is controlled and stabilized by coordinating mechanisms that affect the action of the segmental neuronal networks for walking pattern generation. At present, the motor program for single walking legs in the absence of movement-related coordinating intersegmental influences from the other legs is not known. This knowledge is a prerequisite for the investigation of the segmental neuronal mechanisms that control the movements of a leg and to study the effects of intersegmental coordinating input. A stick insect single middle leg walking preparation has been established that is able to actively perform walking movements on a treadband. The walking pattern showed a clear division into stance and swing phases and, in the absence of ground contact, the leg performed searching movements. We describe the activity patterns of the leg muscles and motoneurons supplying the coxa-trochanteral joint, the femur-tibial joint, and the tarsal leg joints of the middle leg during both walking and searching movements. Furthermore we describe the temporal coordination between them. During walking movements, the coupling between the leg joints was phase-constant; in contrast during searching movements, the coupling between the leg joints was dependent on cycle period. The motor pattern of the single leg generated during walking exhibits similarities with the motor pattern generated during a tripod gait in an intact animal. The generation of walking movements also drives the activity of thoraco-coxal motoneurons of the deafferented and de-efferented thoraco-coxal leg joint in a phase-locked manner, with protractor motoneurons being active during swing and retractor motoneurons being active during stance. These results show that for the single middle leg, a basic walking motor pattern is generated sharing similarities with the tripod gait and that the influence of the motor pattern generated in the distal leg joints is sufficient for driving the activity of coxal motoneurons so an overall motor pattern resembling forward walking is generated.
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INTRODUCTION |
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In legged organisms, locomotor
patterns are generated by a close interaction between central
rhythm-generating networks in the nervous system and sensory
information about actual movements of the appendages and changes in
body posture and equilibrium (e.g., Bässler 1983;
Cruse 1990
; Grillner 1981
;
MacPherson et al. 1997
; Orlovsky et al.
1999
; Pearson 1995
; Wendler
1964
). The motor pattern of each leg emerges from interactions
of sensory signals from the leg with central rhythm-generating networks
governing the action of individual leg joints (summaries in
Büschges and El Manira 1998
; Clarac
1991
; Pearson 1993
, 1995
) and from sensory signals and central commands coordinating the movements of adjacent leg
joints to produce a functional locomotor pattern (invertebrates: Bässler 1993
; Bässler and
Büschges 1998
; El Manira et al.
1991
; Hess and Büschges 1999
; vertebrates:
Orlovsky et al. 1999
). The resulting walking pattern is
cyclic and consists of a stance phase in which the leg is on the ground
and generates propulsion of the organism relative to the substrate and
a swing phase or a return stroke in which the leg returns to its
initial position to start the next stance.
The movements, joint forces and motor patterns of individual legs in
walking insects have been analyzed during walking in considerable
detail (e.g., Burns 1973; Cruse 1976
;
Dean and Wendler 1984
; Delcomyn and Usherwood
1973
; Duch and Pflüger 1995
; Godden and Graham 1984
; Graham 1972
; Graham and
Bässler 1981
; Graham and Epstein 1985
;
Hoyle 1964
; Pearson and Franklin 1984
;
Reingold and Camhi 1977
; Runion and Usherwood
1968
; Schmitz and Hassfeld 1989
;
Tryba and Ritzmann 2000a
,b
; Watson and Ritzman
1998a
,b
). In the stick insect, as in other species, two main
gaits are known for locomotion: the tripod gait and the tetrapod gait
(for summary, see Bässler 1983
; Cruse et
al. 1995
). Various approaches, such as amputation experiments
and experiments perturbing ongoing leg movements, have revealed the
mechanisms that coordinate the relative timing of leg movements (e.g.,
Cruse and Knauth 1989
; Dean and Wendler
1983
; Foth and Bässler 1985a
,b
;
Graham 1977
; Wendler 1964
). Six different
coordinating mechanisms have been identified that contribute to the
generation of stepping patterns during walking (recent summary in
Cruse et al. 1995
). For example, when the middle leg is
in swing, the front leg will not initiate a swing and when the
posterior leg starts a stance, the anterior neighbor can start a swing
(summary in Cruse 1990
). The proper execution of the
coordinating mechanisms relies on information about the actual phase of
movement of each leg and its loading in the walking cycle, provided by
sense organs on the legs (e.g., Cruse et al. 1984
;
summary in Cruse et al. 1995
).
How are signals that serve intersegmental coordination fed into the
segmental neuronal networks of an individual leg and what are the
neuronal mechanisms that affect patterning of motoneuronal activity in
a single leg? To be able to tackle these questions, we first need to
know the coordination pattern of the joints of a single walking leg in
the absence of coordinating influences from other legs. At present,
very little information is available on this issue. This is because
investigations on walking pattern generation in the stick insect and
other insect species were mostly carried out in preparations with
several legs present, i.e., when intersegmental coordinating mechanisms
were expressed, with only a few exceptions (e.g.,
Bässler 1986, 1993
; Bässler et
al. 1991
; Karg et al. 1991
).
The present study focuses on this question by using a stick insect
preparation in which the walking system is reduced to an "isolated
single middle leg." This single-leg preparation is an adaptation of a
preparation developed for the front leg of Cuniculina impigra (Bässler 1993; Karg et al.
1991
). Bässler and coworkers used the front leg
preparation for behaviorally oriented projects on movement control
(e.g., Karg et al. 1991
). We have chosen the middle leg
because the neuronal networks controlling the motoneurons of this leg
are known in greater detail than for the front leg (summaries in
Bässler and Büschges 1998
;
Büschges et al. 2000
). We describe the activity
patterns of the motoneuron pools innervating the muscles of the
coxa-trochanteral (CT), the femur-tibia (FT), and tibia-tarsal (TT)
joints during walking and searching movements. The coordination of
motor activity between the different leg joints was determined, and
differences in the relative timing of activity patterns in searching
and walking movements were analyzed. In addition, we investigated the
influence of the walking and searching movements in distal leg joints
on the motor activity generated in the restrained and deafferented most
proximal leg joint, the thoraco-coxal joint (TC joint). Further
investigations will make use of this preparation and its detailed
quantitative description to elucidate the neuronal mechanisms of
intrajoint and intersegmental coordination. The companion paper
(Schmidt et al. 2000
) describes the use of this
preparation to describe the intracellular generation of motoneuronal
activity patterns in the locomotor cycle.
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METHODS |
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Animals and preparations
All experiments were carried out on adult female stick insects, Cuniculina impigra Redthenbacher (syn. Baculum impigrum Brunner) obtained from a colony maintained at the Institute for Zoology, University of Cologne. The experiments were performed at room temperature (20-22°C) under dimmed-light conditions.
After removing all legs at the level of mid-coxa except for the left mesothoracic leg, the animal was fixed dorsal side up with insect pins or dental cement (Protemp, ESPE) on a foam platform with the coxa of the remaining leg situated exactly at the edge of the platform. The coxal stumps of the severed legs were fixed to the platform. The subcoxal (TC) joint was fixed with dental cement at an angle of approximately 90° to the thorax. Thus leg movements were only possible in the transverse plane. The distal leg joints, i.e., the CT, the FT, the tibia-tarsus joint, and the tarsal segments were all free to move. The mesothoracic scutum was opened dorsally by removing the tergum. The gut was left intact and placed outside of the cavity. Fat and connective tissue were removed, and the mesothoracic ganglion including the proximal basis of the lateral nerve roots was placed on a wax-coated ganglion holder. Connective tissue surrounding the ganglion was fixed to the platform with small cactus spines from Nopalea dejecta.
The lateral nerves of the removed contralateral leg were crushed as
were the lateral nerves nl2, nl4 and nl5 (nomenclature after
Marquardt 1940) of the left middle leg supplying coxal
muscles of the leg. For intracellular recordings, the ganglion was
treated with Pronase E (Merck Chemicals) for 30-90 s, and the thoracic cavity was washed several times and filled with Ringer solution (Weidler and Diecke 1969
) following established
procedures (Büschges 1989
).
Recording of leg movements
A treadband, similar to the one used by Bässler
(1993), was placed underneath the middle leg. Its direction of
movement was aligned with the projection of the longitudinal axis of
the femur. The adhesional friction of the treadband was low so that the
leg was able to move the band at rates similar to those observed in intact walking, ranging from 0.5 to 2 s (see also
Bässler 1993
; Karg et al. 1991
).
Sequences of walking (and searching) movements of the middle leg were
elicited by slightly touching the abdomen with a soft brush or by a
brief air puff to the antennae or the abdomen. In some initial
experiments (n = 4), the leg movements were filmed with
a video system (50 frames/s, SONY DXC101e and JVC HR-D 530E6) to
provide a basic description of the leg movements (Figs.
1A and 3A). In a
later set of experiments (n = 5), the movements of the
tibia (for walking movements) or the femur (for searching movements)
were monitored by an optical detector (e.g., Elsner
1977
; Foth and Graham 1983
) in synchrony
with the electromyographic (EMG) recordings (see following text) from
femoral and tibial muscles (Figs. 1B and 3A).
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Electrophysiology
Activity of the muscles driving the CT and FT joint was
monitored by inserting low-resistance EMG wires (50-µm copper wire, insulated except for the tip). For EMG recordings from tibial muscles,
i.e., extensor tibiae and flexor tibiae, the activity of both
antagonists was monitored by a common bipolar EMG recording (cf.
Weiland et al. 1986). In these recordings, potentials
from the antagonists could be easily distinguished either on the basis of their activity with flexion or extension movements of the tibia elicited by activating the animal or by the different reflex activation of extensor and flexor tibiae muscles to imposed movements of the tibia
at rest. In addition, intracellular recordings from motoneurons of both
muscles verified their clear antiphase activity during walking and
searching movements (see Schmidt et al. 2001
for
details). Walking muscles in stick insects consist of individual muscle
fibers that are only loosely coupled to each other by connective tissue. It is not possible to distinguish single motor units from EMG
recordings of muscles which are innervated by more than two motoneurons, such as the flexor tibiae and the levator trochanteris (Debrodt and Bässler 1989
; Hess and
Büschges 1997
; Storrer et al. 1986
). Hence
we did not distinguish individual muscle potentials of those muscles
(but see Duch and Pflüger 1995
) but rather
evaluated their summated activity. In those muscles that are innervated by two excitatory motoneurons, i.e., the depressor trochanteris and the
extensor tibiae (Bässler and Storrer 1980
;
Schmitz 1986
; Storrer et al. 1986
), the
largest muscle potentials can be clearly attributed to the activity of
the fast motoneurons, i.e., the fast extensor tibiae (FETi) and the
fast depressor trochanteris (FDTr).
The activity of the motoneurons supplying the protractor coxae and the
retractor coxae muscles of the TC joint was monitored by extracellular
hook-electrode recording (Schmitz et al. 1988) from the
lateral nerves nl2 and nl5, respectively (nerves labeled according to
Marquardt 1940
). The activity of the motoneurons innervating muscles moving the tarsal segments, i.e., the levator and
depressor tarsi and the retractor unguis, was monitored by intracellular recordings from the neuropilar regions of their motoneurons in the mesothoracic ganglion. Intracellular recordings were
made using an SEC-10 L amplifier (NPI Electronics, Tamm, Germany)
thin-walled glass microelectrodes (Since Products) filled with a tip
solution of 3 M KAc/0.05 M KCl (electrode resistance, 15-25 M
) were
used. In general, leg motoneurons were identified by eliciting
movements of the tarsus or its segments on being depolarized with
injected current pulses surpassing the action potential threshold (see
also Wolf 1992
).
Data evaluation and statistics
Intracellular recording, EMG recordings, injected current,
leg-position signals, and voice track were stored on an eight-channel digital audio tape recorder (Biologic DAT 1800 or DRA 800). For evaluation, the data were either displayed on a Yokogawa DL2300 chart
recorder or they were analyzed off-line on a Pentium II personal
computer using Spike 2 software (Cambridge Electronics). A/D conversion
was performed by a CED 1401plus interface (Cambridge Electronics).
Statistical analysis was performed with Apple KaleidaGraph for Windows,
StatView, and MS Excel after the criteria described in Sachs
(1978) and Batschelet (1981)
. In the text,
N gives the number of animals, n gives the sample size.
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RESULTS |
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Motor pattern of active walking and searching movements of the middle leg
WALKING MOTOR PATTERN OF THE MUSCLES SUPPLYING THE FT AND CT JOINT.
Usually, brief tactile stimulation with a fine paint brush or a short
wind puff on the abdomen was used to induce continuous walking
sequences of several steps, although walking movements (Fig.
1A) were occasionally generated spontaneously. A step cycle (Fig. 1, A and B) was characterized by two
phases, stance and swing. The power stroke, during which the treadband
was pulled toward the animal will be referred to as stance
(see also Bässler 1993), was generated
by a strong activation of the flexor tibiae muscle. In the subsequent
phase, the return stroke, the leg was lifted off the treadband, the FT
joint was extended by activity of the extensor tibiae muscle and the
leg returned to its distal starting position. This phase will be
referred to as swing (see also
Bässler 1993
). Because the leg only
moves in the transversal plane, the relationship between joint
extension versus flexion and swing and stance is more typical of front
legs during intact walking than it is of middle legs (see
DISCUSSION for details). In many walking episodes, a short
pause in activity was detectable at the times of transition between
extensor and flexor activity (Fig. 1B,
). The average
duration of the pause was 29.8 ± 29.60 (SD) ms for the
transition from stance to swing, and 112 ± 108 ms for the
transition from swing to stance (N = 14, n = 122). The duration of these pauses did not change
with step cycle duration (P > 0.05, data not shown).
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SEARCHING MOTOR PATTERN OF THE MUSCLES SUPPLYING THE FT AND CT
JOINT.
When the treadband was removed, the middle leg performed stereotype
sequences of movements that resembled searching movements previously
described for the single foreleg preparation by Karg et al.
(1991). Searching movement sequences were reconstructed from
video recordings and are shown in Fig.
3A. The search cycle consists
of two phases, trochanteral depression in combination with FT flexion
and trochanteral levation in combination with FT extension (Fig.
3Aii). A histogram of the cycle periods observed is given in
Fig. 3Aiii. The mean cycle period of the population investigated was 1,039.8 ± 458.9 ms (N = 12, n = 129).
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WALKING AND SEARCHING PATTERNS OF MOTONEURONS SUPPLYING TARSAL
JOINTS.
The tarsus, including the pretarsus composed of the arolium and claws,
is moved by three muscles, the levator tarsi (LevT), the depressor
tarsi (DprT), and the Retractor unguis (RetU) muscle. The latter is
tripartite and consists of one femoral and two tibial muscles
(Radnikow and Bässler 1991). The
activity of the motoneurons innervating these muscles was recorded
intracellularly from their neuropilar processes. EMG recordings from
the main part of the retractor unguis muscle in the femur are not
possible due to its position in the proximal femur close to the
extensor and flexor tibiae muscles. EMG recordings of the LevT and DprT
would have impaired the leg movements due to the long EMG wires (4-6
cm) necessary for the distal segments of the leg.
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Coupling of motor activity in the CT, FT, and TT joint during walking and searching movements as a function of cycle period
During walking, there was no significant correlation between extensor onset and cycle period, as defined from flexor onset to flexor onset (P > 0.05, Fig. 6Ai), indicating that the phase of extensor onset was independent of walking speed. Similarly, the phase of onset in activity of the muscles moving the CT joint, i.e., the LevTr and the DprTr, was constant over the range of cycle periods investigated relative to the onset of extensor tibiae activity (P > 0.05; Fig. 6Aii). This indicates a phase-constant coordination of CT and FT joint during consecutive steps in the single-leg preparation.
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In searching, the onset of activity in the extensor tibiae muscle changed in relation to cycle length (P < 0.05, Fig. 6Bi), resulting in an earlier onset of extensor activity during longer searching cycles. As expected from the preceding results, the activation of the LevTr did not change in relation to extensor onset (P > 0.05, Fig. 6Bii), and it did not change with cycle period. In contrast, activation of the DprTr depended on cycle period measured relative to the onset of tibial extensor activity, in a way that it was delayed with increasing cycle period (P < 0.05, Fig. 6Bii). In summary, in contrast to the phase-constant pattern of muscle activation in the CT joint and the FT joint during walking, interjoint coordination during searching did depend on cycle period [but showed a simultaneous onset of the tibial extensor and LevTr muscles (see also Fig. 3E)].
The phase of onset of tarsal motoneuron activity during walking is plotted in Fig. 6Aiii as a function of cycle period. The onset of activity in DprT and RetU in relation to flexor onset was observed to be independent of the cycle period (P > 0.05). In contrast, motoneurons innervating the LevT muscle exhibited a significant shift in their phase of activation with changing cycle period (P < 0.05). Thus for LevT motoneurons, there was no fixed coupling of activity onset in relation to the tibial muscle activation.
A general difference in the motor patterns generated either during walking or during searching movements concerned the duty cycle, i.e., the relative duration of the muscle activity as percentage of the cycle length, of the muscle antagonists of the CT and FT joint in the walking and searching cycle. The major difference in both patterns was the duty cycle of tibial muscles in the movement cycle, being for the extensor muscle on average about 75% in searching and 60% during walking and about 25% for the flexor muscle during searching and 40% during walking (not shown).
Activity of the motoneuron pools of the TC joint during walking and searching movements
In the isolated middle leg walking preparation, the most proximal
leg joint, the TC joint was not only immobilized but also deafferented
and de-efferented by cutting or crushing the lateral nerves nl2, nl4,
and nl5. Lateral nerve nl2 carries the axons innervating the protractor
coxae muscle (ProCx), and lateral nerve nl5 innervates the retractor
coxae muscle (RetCx) (Graham and Wendler 1981).
Extracellular recordings from the nerves nl2 and nl5 and EMG recordings
of tibial muscle activity during continuous walking sequences revealed
that the activity of the motoneurons innervating coxal muscles was
tightly coupled to the motor program generated in the distal leg joints
(Fig. 7A). The motoneurons of
both pools (ProCx and RetCx) exhibited clearly alternating activity in
the walking cycle. During stance, activity of RetCx motoneurons
occurred simultaneously with activity in the flexor tibiae muscle. A
short delay between the start of activity in the flexor tibiae and the
start of activity in retractor coxae motoneurons was frequently
observed (Fig. 7Ai, see also 7C). During swing,
i.e., activity of the tibial extensor muscle, ProCx motoneurons were
active. The activity of protractor motoneurons slightly outlasted leg swing and was terminated at the beginning of stance (Fig. 7,
A and C). This pattern of activity in coxal
motoneuron pools was observed in 93% of the step cycles
(N = 6, n = 58). Activity of ProCx
motoneurons with swing phase and activity of RetCx motoneurons coincident with stance phase (Fig. 7, Ai and C)
shares similarities with the leg motor pattern generated in
intact "forward" walking animals (e.g., Büschges et
al. 1994
; Graham and Bässler 1981
; Schmitz and Hassfeld 1989
). In the remaining 7% of the
step cycles recorded, alternating activity in TC motoneurons was
observed as well. In these step cycles RetCx motoneurons were found to be synergistically active with the extensor tibiae, and ProCx motoneurons were active together with the flexor tibiae muscle. These
steps resembled "rearward" walking (not shown). However, this
rearward walking pattern was never steadily maintained and never lasted
for more than two step cycles.
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During walking, the burst length of ProCx and RetCx activity was significantly correlated with cycle period (P < 0.05, Fig. 7Bi) as was observed for the muscles of the CT and FT joints (see Fig. 2). Furthermore the onset of activity in ProCx and RetCx muscles in relation to the onset of activity in the flexor tibiae muscle did not change with step cycle duration (P > 0.05, Fig. 7Bii). Therefore the phase difference between the activation of TC motoneuron pools did not change when cycle period was changing (P > 0.05). The resulting motor pattern is schematically shown in Fig. 7C. This finding was further confirmed by intracellular recording from neuropilar processes of coxal motoneurons. These recordings revealed (ProCx; N = 3; RetCx; N = 4) that the motor output generated during walking in coxal motoneurons was due to a strong modulation of the motoneuronal membrane potential around its resting membrane potential in the walking cycle (Fig. 7Aii).
During searching movements, the activity pattern of ProCx and RetCx
motoneuron pools was different as it was not related to the movements
cycle of the leg (Fig. 8, A
and B). In the majority of animals tested either RetCx or
ProCx motoneuron pools could exhibit tonic activity that was sustained
over consecutive search cycles, whereas little or mostly no activity
was observed in the particular antagonist (Fig. 8A). During
ongoing searching sequences, activity could sometimes switch from one
motoneuron pool to the other (Fig. 8A). Occasionally, slight
modulations in the overall activity of the coxal motoneuron pools were
observed (Fig. 8B) as also seen in front legs
performing searching movements (Bässler et al.
1991). Intracellular recordings from the coxal motoneurons revealed a tonic activation of individual motoneurons during the performance of searching movements (Fig. 8C).
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DISCUSSION |
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The present investigation provides a description of motor patterns generation in the stick insect middle leg, in a preparation in which influences from movements of the other legs were excluded. There are three main results of our experiments. 1) Without neighboring legs, the middle leg is able to generate stereotype walking and searching movements. Coordination of motor activity in adjacent leg joints during walking movements was found to be independent of cycle duration and hence phase-constant, while motor patterns during searching exhibited considerable dependence on cycle duration. 2) During walking, the duration of both stance and swing depended on step cycle duration, similar to the pattern seen in tripod gait (see below). 3) During walking and searching movements, motoneuron pools supplying the TC joint were also activated, even though this joint was deafferented and de-efferented. During walking there was a tight phase-constant coupling of coxal motoneuron activity with the movements generated in the distal leg joints.
Motor patterns for walking movements of a single walking leg
During walking movements of the single middle leg, the
activity of all leg muscles was driven in a cyclic manner generating consecutive stance and swing phases (Fig.
9A). The cycle periods averaged 1.515 ± 0.481 s and thus are in the same range (0.3-2 s) as those reported for the intact stick insect (Bässler
1983). Walking movements were characterized by a stereotyped
coordination between the motoneuron pools of the joints that were free
to move, i.e., CT, the FT, and the tarsal joints. The basic pattern of activity in the leg muscles was the following: during stance flexor tibiae motoneurons were active together with depressor tarsi and retractor unguis motoneurons and the treadband was pulled toward the
animal. Levator trochanteris motoneurons were activated late in the
stance phase. During late stance, levator muscle activity assists the
other stance phase muscles (flexor, retractor unguis) in
pulling the treadband toward the animal. The activation of levator
trochanteris motoneurons was maximal when the leg was lifted off the
treadband, i.e., at the transition from stance to swing. This
stance-to-swing transition was characterized by the offset of flexor
activity and the onset of activity in extensor tibiae and levator tarsi
motoneurons. This switch in motoneuronal activity caused lifting of the
leg off the treadband and extending the FT joint toward its initial
position prior to the former stance phase. In late swing, activation of
depressor motoneurons contributed to setting down the leg on the
treadband and the next step cycle started.
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In addition to the observed range of cycle periods, one similarity of
the single middle leg preparation to the intact walking stick insect
was the bi-phasic structure of walking movements with sequential stance
and swing modes. Differences to intact straight walking occur in the
operating range of FT-joint angle during stance and swing. Excursions
in FT joint are smaller for the middle leg in straight walking than in
the single middle leg preparation. This derives from the fact that in
straight walking of intact animals stance and swing leg excursions are
mainly due to movements of the coxa, i.e., in the horizontal plane of
the TC joint (Cruse et al. 1995), while in the single
leg preparation they are generated by flexion and extension of the FT
joint. In this respect, the coordination of leg muscles in the walking
cycle of the preparation used here is more similar to forward walking in the front leg (see Bässler 1983
, 1988
, 1993
;
Cruse 1976
). As in the single middle leg, the front leg
stance is generated predominantly by FT-joint flexion and swing by
FT-joint extension (Bässler 1993
). Furthermore a
similar coordination pattern occurs in the intact walking system e.g.,
an inner leg during curve walking (Jander 1982
;
Rixe and Dean 1995
). A similar reciprocity in activity of femoral muscles, as observed in the single middle leg preparation was also reported for walking at shorter cycle periods of the cockroach
(Krauthamer and Fourtner 1978
).
In the single middle leg preparation, the duration of both stance and
swing depended on cycle period. Such a dependence is seen in the intact
stick insect walking with a tripod gait (see also Bässler
1983; Cruse et al. 1995
; Graham
1985
). There is, however, a difference between these two
situations. The proportion of swing in the single middle leg
preparation is around 50% and thus significantly larger than in the
intact animal walking in tripod gait, in which swing covers around 20%
of the cycle (cf. Bässler 1983
; Graham
1985
). Several factors might contribute to this difference. In
the intact stick insect, the transition from swing to stance and vice
versa is under control of segmental and intersegmental sources: sensory
signals from the TC joint of the same leg (Bässler
1977
; Dean and Schmitz 1992
) affect the
transition from stance to swing and vice versa and coordinating signals
related to the movement phase or loading of neighboring legs affect
both transitions (Cruse 1990
). It is quite conceivable that coordinating influences do affect the duration of the swing phase
of the middle leg by shortening it and by lengthening stance phase in
intact walking. The marked quantitative changes occurring with respect
to the proportion of leg swing in the step cycle thus may arise from
these absent constraints. As such, the neuronal system generating
middle leg movements appears to operate in a "free-run mode" in the
single leg preparation. This offers a variety of approaches to
investigate neuronal mechanisms underlying coordination.
Two other influences have to be taken into account as well. First, load
signals from the same leg, i.e., the middle leg, and the mesothoracic
segment that are known to affect the generation of the stepping
patterns in walking may differ in the single middle leg preparation
(e.g., Bässler 1977; Schmitz et al.
1995
; Wendler 1964
). Such local load signals are
not necessarily restricted to the same leg but can also arise from the
other legs via mechanical coupling within the walking system. Such
signals are absent in the preparation and thus load information about
the status of the thorax is altered (e.g., Delcomyn
1991
; Ridgel et al. 2000
; Schmitz
1993
; Zill and Moran 1981
). Second, the TC-joint
of the middle leg is not free to move. Sensory information from the
CT-joint provides relevant information about the actual phase of the
leg in the walking cycle (e.g., Bässler 1977
;
Cruse et al. 1984
). Both aspects may also affect the
activity motor pattern of coxal motoneurons so that it differs from the
intact walking stick insect. As such Graham and Wendler
(1981)
have reported that in the middle leg the initial 30% of
the stance phase of the middle leg are generated during ongoing
co-activation of protractor and retractor coxae motoneurons. In the
single leg preparation, we did not observe such a phase of
co-activation of coxal motoneuron pools in the walking cycle. Both the
lack of specific load signals as well as the lack of proprioceptive
information from the coxa may contribute to this pattern.
Motor patterns for searching movements of a single walking leg
Searching movements of the single middle leg were composed of trochanteral depressor and tibial flexor activity in conjunction with activity in retractor unguis motoneurons (Fig. 9B). Subsequently trochanteral levator, tibial extensor and levator tarsi motoneurons activity started together and tarsal depressor motoneurons were activated throughout the full search cycle. In contrast to walking, the searching motor pattern exhibited considerable dependence on cycle period. The most prominent characteristic in searching movements was the simultaneous onset of tibial extensor and trochanteral levator activity. Finally, there was no coupling of motor activity in the thoraco-coxal joint to the searching cycle.
The searching movements generated in the middle leg and their
underlying motor patterns reported here are very similar to searching
movements generated in the stick insect front leg (cf. Bässler 1993; Karg et al. 1991
).
Recently data were presented for freely searching front legs
(Dürr 1999
) reporting that the stick insect leg
tends to change the position of its thoraco-coxal joint independent of
the ongoing searching movements of the CT and FT joints. This result is
in accordance with our finding that the coxal motoneuron pools were
mostly tonically active during searching sequences with activity
sometimes switching from one motoneuron pool to the other.
Interjoint coordination in stick insect walking legs
Recording motoneuronal activity of the CT-motoneuron pools during
walking revealed that both the protractor and the retractor coxae
motoneuron pools exhibited rhythmic activity coupled to the ongoing
motor pattern. The coordination mostly resembled the one known for
movements of the front legs during forward walking (e.g.,
Bässler 1983; Graham 1985
) where
during stance, retractor coxae motoneurons were active and during
swing, protractor coxae motoneurons were active. The occurrence of
patterned activity in TC-motoneuron pools during walking is interesting
because this joint was de-efferented and deafferented. The question
emerges as to how the activity of the motoneurons of the TC joint is
coupled to the walking motor pattern. From previous investigations, it has become clear that proprioceptive signals from one leg joint contribute to patterning of motoneuronal activity in adjacent leg
joints (Bässler 1993
; Hess and
Büschges 1999
). It thus appears quite conceivable that
sensory signals reporting movements and/or forces from distal leg
joints during walking may affect the premotor networks of the TC joint
so that their activity is coupled to the ongoing motor pattern. Similar
results have been reported for the action of proprioceptive signals in
the walking system of the crayfish (e.g., El Manira et al.
1991
). The best candidate sense organs for such signals would
be those that report ground contact of the leg, such as tarsal sense
organs, canal organs, and tactile hairs and spurs, or those that report
forces generated during stance, such as trochanteral and femoral
campaniform sensillae. This is corroborated by the observation that
retractor activity during stance is most often initiated after the leg
contact, i.e., following the onset of stance phase in the walking cycle
(Fig. 7C). Additionally, central preprogramming of
interjoint coordination might be involved. Such a possibility is based
on the results on rhythmic preparations of the isolated CNS in
invertebrate walking systems (Büschges et al.
1995
; Chrachri and Clarac 1990
; Johnston and Levine 1996
; Ryckebusch and Laurent 1993
).
At present, we cannot distinguish between the contribution of each of
these aspects to the coupling of motor activity in coxal motoneuron
pools to the walking pattern in the distal leg joints. In the companion paper, we have investigated how patterning of motoneuron activity during active leg movements is generated in the stick insect middle leg.
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ACKNOWLEDGMENTS |
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We are grateful to Drs. U. Bässler (formerly of the University of Kaiserslautern), R. A. DiCaprio, and H. Scharstein and G. Wendler (both from the University of Cologne) for valuable discussions throughout the course of the work. We thank Dr. R. A. DiCaprio for critically reading the manuscript and for improving its language.
This project was supported by the Deutsche Forschungsgemeinschaft (Bu857/2 and 857/6).
Present addresses: H. Fischer, School of Biology, Div. of Biomedical Sciences, Bute Medical Bldg., University of St. Andrews, Fife KY16 9TS, Scotland, UK; R. Haas, Neurologische Universitätsklinik, Hoppe-Seyler-Strasse 3, 72076 Tubingen, Germany.
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FOOTNOTES |
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Address for reprint requests: A. Büschges, Zoologisches Institut, Universität zu Köln, Weyertal 119, 50923 Cologne, Germany (E-mail: Ansgar.Bueschges{at}uni-koeln.de).
Received 10 July 2000; accepted in final form 28 September 2000.
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REFERENCES |
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