Role of Proprioceptive Signals From an Insect Femur-Tibia Joint in
Patterning Motoneuronal Activity of an Adjacent Leg Joint
DIETMAR HESS AND ANSGAR BÜSCHGES
Department of Animal Physiology, Faculty of Biology, University of Kaiserslautern, 67653 Kaiserslautern, Germany
INTRODUCTION
During walking, the motor pattern driving the leg muscle
system is the result of interactions between central neural
networks, feedback signals from sense organs as well as coordinating pathways between the legs. For a variety of vertebrate
and invertebrate walking systems, interactions between central
and peripheral signals have been described in considerable
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detail on the operational level (reviews in Bässler and Büschges 1998; Clarac 1991; Grillner 1975, 1985; Pearson 1993;
Prochazka 1996; Rossignol et al. 1988). Changes in load,
information from position-sensitive sense organs of leg joints,
and information on the actual step phase of adjacent legs
strongly influence the motor pattern of each individual leg
(e.g., Bässler 1977, 1993; Cruse 1985; Foth and Bässler 1985;
Pearson and Iles 1973; Wendler 1964). Intrajoint proprioceptive information is used for sculpturing the motor output of the
leg muscle system controlling this joint. These sensory signals
can entrain motor activity produced by rhythm-generating networks (e.g., Anderson and Grillner 1983; Conway et al. 1987;
Sillar et al. 1986), and they can induce phase- or state-dependent reflex reversals in motor control networks (e.g., Bässler
1976; DiCaprio and Clarac 1981; Pearson and Collins 1993;
Skorupski and Sillar 1986; recent summary in Büschges and El
Manira 1998). Furthermore generation of the functional walking motor pattern in the multijointed limb also relies on coordination between movements of adjacent leg joints. The
knowledge, however, as yet mostly concerns the operational
level in understanding interjoint coordination. Evidence exists
for both central and peripheral influences on coordination
between adjacent joints (e.g., Angel et al. 1996; Bässler 1993;
Graham and Bässler 1981; Grillner and Zangger 1979; Robertson et al. 1985). Investigations of the neuronal mechanisms
underlying interjoint coordination only recently have been
initiated (El Manira et al. 1991). The question arises, particularly in walking systems in which individual joint oscillators
have been shown (stick insect: Büschges et al. 1995; mudpuppy: Cheng et al. 1998), how activities between adjacent leg
joints are coordinated and to what extent sensory signals play
a role in interjoint coordination.
We set out to investigate what role sensory signals from one
leg joint play in patterning motoneuronal activity of the adjacent leg joint in an insect walking system. We chose to investigate this question for sensory signals provided by the fCO in
the stick insect middle leg muscle control system for the
following reasons: the fCO can be stimulated very easily with
various defined stimulus protocols that allow a separation
between the influence of position and movement signals
(Bässler 1983). In addition, the behavioral state of the animal
can be controlled by monitoring the motor response that sensory signals from the fCO induce in intrajoint control networks
of tibial motoneuron pools.
A previous investigation described interjoint reflex action
between the fCO and trochanteral motoneurons in the stick
insect middle leg in the inactive, i.e., resting animal (Hess and
Büschges 1997). Elongation of the fCO, i.e., flexion of the FT
0022-3077/99 $5.00 Copyright © 1999 The American Physiological Society
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Hess, Dietmar and Ansgar Büschges. Role of proprioceptive signals from an insect femur-tibia joint in patterning motoneuronal
activity of an adjacent leg joint. J. Neurophysiol. 81: 1856 –1865,
1999. Interjoint reflex function of the insect leg contributes to postural
control at rest or to movement control during locomotor movements.
In the stick insect (Carausius morosus), we investigated the role that
sensory signals from the femoral chordotonal organ (fCO), the transducer of the femur-tibia (FT) joint, play in patterning motoneuronal
activity in the adjacent coxa-trochanteral (CT) joint when the joint
control networks are in the movement control mode of the active
behavioral state. In the active behavioral state, sensory signals from
the fCO induced transitions of activity between antagonistic motoneuron pools, i.e., the levator trochanteris and the depressor trochanteris
motoneurons. As such, elongation of the fCO, signaling flexion of the
FT joint, terminated depressor motoneuron activity and initiated activity in levator motoneurons. Relaxation of the fCO, signaling extension of the FT joint, induced the opposite transition by initiating
depressor motoneuron activity and terminating levator motoneuron
activity. This interjoint influence of sensory signals from the fCO was
independent of the generation of the intrajoint reflex reversal in the FT
joint, i.e., the ‘‘active reaction,’’ which is released by elongation
signals from the fCO. The generation of these transitions in activity of
trochanteral motoneurons barely depended on position or velocity
signals from the fCO. This contrasts with the situation in the resting
behavioral state when interjoint reflex action markedly depends on
actual fCO stimulus parameters, i.e., position and velocity signals. In
the active behavioral state, movement signals from the fCO obviously
trigger or release centrally generated transitions in motoneuron activity, e.g., by affecting central rhythm generating networks driving
trochanteral motoneuron pools. This conclusion was tested by stimulating the fCO in ‘‘fictive rhythmic’’ preparations, activated by the
muscarinic agonist pilocarpine in the otherwise isolated and deafferented mesothoracic ganglion. In this situation, sensory signals from
the fCO did in fact reset and entrain rhythmic activity in trochanteral
motoneurons. The results indicate for the first time that when the stick
insect locomotor system is active, sensory signals from the proprioceptor of one leg joint, i.e., the fCO, pattern motor activity in an
adjacent leg joint, i.e., the CT joint, by affecting the central rhythm
generating network driving the motoneurons of the adjacent joint.
ROLE OF SENSORY SIGNALS IN INTERJOINT COORDINATION
METHODS
Experiments were performed on adult female stick insects of the
species Carausius morosus raised in the animal facilities of the
University of Kaiserslautern under daylight conditions and at room
temperature (20 –22°C).
The animals were mounted dorsal side up on foam platform with
the forelegs and hindlegs being fixed aside the longitudinal axis of the
body (for details, see Hess and Büschges 1997). The proximal leg
segments of the left middle leg, i.e., coxa, trochanter, and femur (in
the stick insect, trochanter and femur are fused to one segment) were
fixed with dental cement (Protemp, ESPE) onto a foam rim pointing
slightly upward at an angle of ;30°. The tibia was extending over the
distal margin of the rim and the platform. The FT joint then was fixed
with dental cement at an angle of ;150°.
The thorax of the animal was opened by a sagittal cut along the
dorsal midline of the meso- and metathorax. The thoracic cavity was
filled with stick insect saline (Bässler 1977; Weidler and Diecke
1969). The mesothoracic ganglion was placed on a wax coated platform and fixed with cactus spines. The activities of motoneurons were
recorded extracellularly from the lateral nerves that carry the axons of
motoneurons innervating the muscles of the three proximal leg joints
with monopolar hook electrodes (Schmitz et al. 1988). The following
motor nerves were recorded: C1, carrying the motoneurons of the
levator trochanteris; C2, carrying the motoneurons of the depressor
trochanteris. Extensor tibiae motoneuron activity was recorded for
monitoring the behavioral state of the animal by either an extracellular
recording from the extensor nerve F2 in the femur (for details, see
Hess and Büschges 1997) or by a recording from nerve nl3, in which
the extensor motoneurons leave the ganglion. In recordings from
nerve nl3 the extensor motoneurons have the largest spikes (see also
Büschges et al. 1995).
Animals were activated by touching their abdomen or head with a
small paintbrush. During and after tactile stimulation, the experimental animal moved its unrestrained tarsi, its abdomen, and antennae.
Furthermore fast motoneurons recorded in the leg nerves were activated in a burst-like fashion (see also Bässler 1983, 1988)
Preparation for stimulation of the fCO during
pharmacologically induced rhythmic motor activity in the
otherwise isolated mesothoracic ganglion
In these experiments, the influence of sensory signals arising from
the fCO on centrally generated rhythmic motor activity in the trochanteral motoneuron pools was investigated. In this preparation,
except for the fCO all other afferent input to the isolated mesothoracic
ganglion was removed. Before the experiment, the trochanteral campaniform sensillae of the left middle leg were destroyed by drilling a
sharpened tip of an insect needle through the cuticle at their location
(Hofmann and Bässler 1982). Experimental animals were fixed to the
foam platform (Hess and Büschges 1997). The mesothoracic ganglion
was isolated from the thoracic nerve cord by cutting its anterior and
posterior connectives. Partial deafferentation of the ganglion was
achieved by cutting the following lateral nerves (labeled according to
Marquardt 1940) close to the ganglion: nervus anterior (na); nervus
posterior (np), nervus unparis [(nup); this nerve leaves the ganglion on
the dorsal surface] and the nervi laterali 2–5 (nl2–5). After positioning
an extracellular hook electrode on coxal nerves C1 and C2, action
potential propagation in these nerves toward the muscles was terminated by squeezing these motor nerves with fine forceps distal to the
recording site. The apodeme of the fCO was exposed according to the
described procedures and fixed in the clamp of the stimulus device.
Finally, the main leg nerve nervus cruris (ncr) was cut at its entrance
to the femur. Stick insect saline was applied by drops into the body
cavity.
Stock solutions of 1022 M pilocarpine (Sigma Chemicals) in saline
were prepared in advance and were diluted with saline to their final
concentrations prior to application. Application of the drugs was
performed by removing the saline from the thorax of the experimental
animal and replacing it by the drug solution under investigation with
final concentrations in the range of 1 3 1024 M to 1 3 1023 M
(Büschges et al. 1995).
Extracellular and intracellular recordings from motoneurons
Preparations of the mesothoracic ganglion for intracellular recordings were performed according to the established procedures (Büschges 1990). Intracellular recordings were performed in the ipsilateral
neuropil region of the mesothoracic ganglion that is known to contain
the arborizations of fCO afferents (Schmitz et al. 1991) as well as the
arborizations of leg motoneurons (Storrer et al. 1986). Recordings
were made using thin-walled glass microelectrodes (wpi), filled with
a solution of 2 M KAc/0.05 M KCl (electrode resistance 15–20 MV).
Mechanical stimulation of the fCO
For mechanical stimulation of fCO afferents, the femur of the left
middle leg was prepared. The receptor apodeme was exposed and
fixed in the clamp of a stimulus device; it then was cut distally and
was moved over a range of positions corresponding to femur tibiaangles between 30 and 150°. Ramp-and-hold stimuli with different
stimulus velocities and holding times were tested. Flexion movements
of the tibia were mimicked by elongation of the fCO in most cases
from a starting position of ;120° with an amplitude of 300 mm
(corresponding to a joint movement of 60°) (Weiland and Koch 1987).
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joint, activates trochanteral levator motoneurons and inhibits
trochanteral depressor motoneurons. Relaxation of the fCO,
i.e., extension of the FT joint, induces activation of depressor
motoneurons and in part coactivation of levator motoneurons.
This interjoint reflex action contributes to posture control of the
resting, i.e., standing animal. When the stick insect turns active
(active behavioral state), the joint control networks switch
from the posture-control mode to the movement-control mode
acting during locomotor movements (Bässler 1976, 1988; summary in Bässler and Büschges 1998). When the locomotor
system is active, proprioceptive signals from the FT joint are
used for controlling tibial movements by reinforcement of
movement over a broad range of movement velocities. Such
reinforcement of movement becomes obvious from the exhibition of a state-dependent reflex reversal in the FT-joint control network toward joint flexion (Bässler 1988). The question
arises what role interjoint influences of proprioceptive signals
play in the active behavioral state. Initial evidence presented
showed that in the active behavioral state elongation signals
from the fCO still induce activation of levator motoneurons,
however, in a burst-like fashion (Hess and Büschges 1997).
The present investigation addresses in more detail the role of
position and movement signals from the fCO in sculpturing
motoneuronal activity of the adjacent CT joint in the active
behavioral state of the stick insect. We will show that sensory
signals from the fCO can take part in patterning motor activity
in trochanteral motoneurons by releasing transitions of activity
between trochanteral motoneuron pools. The induction of these
transitions did not depend on the actual stimulus parameters.
The induction rather depended on the direction of movement
signaled by fCO afferents. For the first time, we will provide
evidence that proprioceptive signals from an insect leg joint
affect central rhythm generating networks driving an adjacent
leg joint.
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D. HESS AND A. BÜSCHGES
Stimulus velocities were in the range of 20 –1,200°/s. Movement
velocities in this range have been reported to be generated by the stick
insect leg muscle system (Bartling 1993; Bässler 1983). Acceleration
values of the stimuli were not controlled independently.
Data storage and statistics
RESULTS
Sensory signals the fCO induce transitions of activity
between motoneuron pools of the coxa-trochanteral joint
In the active behavioral state of the stick insect, the fast and
semifast levator and fast depressor motoneuron of the CT joint
were mostly active in clear antiphase to each other in a burstlike fashion (Fig. 1; for definition of the ‘‘active’’ behavioral
state, see also INTRODUCTION and METHODS). Only slow motoneurons of both motoneuron pools sometimes were coactivated
(see Fig. 1A). Sensory signals from the fCO influence the
activity of trochanteral motoneuron pools in the active behavioral state (Hess and Büschges 1997, their Fig. 9). Elongation
of the fCO resulted as a rule in a strong, i.e., burst-like
activation of the levator motoneurons. The spike frequency of
spontaneous active slow levator motoneurons increased rapidly, and strong activity in semifast and fast motoneurons could
be elicited. Simultaneously, activity of slow and fast trochanteral depressor motoneurons was terminated (Fig. 1, A and B)
(also Hess and Büschges 1997). In contrast, in the resting,
inactive animal elongation of the fCO are known to induce
only subtle excitation in levator motoneurons with slow and
semifast levator motoneurons being activated suprathresholdly.
In the active behavioral state, burst-like activation of trochanteral levator motoneurons, and simultaneous inactivation of depressor motoneurons (termed ‘‘transition’’), could be elicited almost routinely by fCO elongation stimuli when semifast and fast
levator motoneurons were not active before stimulus onset. This
was true despite the well-known variability in rhythmic leg motoneuron activity of the active stick insect (Fig. 1A) (see also
Bässler and Wegner 1983). In case of levator motoneurons being
active at the time of fCO elongation stimulus onset, levator
activity was enhanced. A quantitative evaluation of 25 experiments (ramp-and-hold stimuli applied to the fCO from 120 to 60°;
stimulus velocity 120°/s) showed that on average ;67.8% of the
elongation stimuli, in which the levator motoneurons were not
active before stimulus onset (n 5 977), induced a burst-like
activation of levator motoneurons. Depressor motoneuron activity
was terminated when present (Fig. 1). The remaining stimuli, in
FIG. 1. Influence of sensory signals from the femoral chordotonal organ
(fCO) on the activity of trochanteral motoneurons. A: comparison of the
influence of sensory signals from the fCO (Pos) on the levator trochanteris
(Lev) and the depressor trochanteris motoneurons (Dep) in the inactive and
active animal (S, slow; sF, semifast; F, fast levator trochanteris motoneurons;
SDTr, slow depressor; FDTr, fast depressor trochanteris motoneuron). Please
note that sF and F levator and FDTr are mostly active in antiphase. Despite the
overall variability of alternating motoneuronal activity, fCO elongation is
associated mostly with a transition from depressor to levator activity (),
whereas the reverse transition is initiated by relaxation signals from the fCO
(ƒ). B: expanded presentation of one transition occurring with fCO elongation
(i) and fCO relaxation (ii). C: average peristimulus time (PST) histograms of
levator motoneuron activity for 1 preparation. Compared is the mean levator
activity when a Dep/Lev-transition was elicited (n 5 13) and when no
Dep/Lev-transition is initiated (n 5 24). D: in some experiments, trochanteral
motor activity could be almost completely patterned by continual ramp-andhold stimulation of the fCO.
which semifast and fast levator motoneurons were not active
before stimulus onset did not induce a specific motor response
(32.2%). This is shown in Fig. 1C by PST histograms of levator
activity in one preparation.
The reverse motor response was elicited by relaxation of the
fCO when levator motoneurons were active during onset of a
relaxation stimulus. In 71.1% of the presentations (N 5 25,
n 5 863), elongation stimuli terminated levator motoneuron
activity and activated depressor motoneuron activity (Fig. 1, A
and D). The aforementioned influence of fCO signals on the
activity of trochanteral motoneurons in the active behavioral
state persisted after deafferentation of the proximal leg joints
(except from the fCO; N 5 5; not shown).
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All data were stored on an eight-channel DAT-recorder (Biologic
DTR-1802, sample rate 12 kHz) and analyzed off-line either on a
personal computer or displayed on a printer for further evaluation
(Yokogawa OR-2100). Peristimulus time (PST) histograms were generated by using the evaluation software Spike2 (Cambridge Electronics, Science Products, ver. 3.14).
Results are given either as single values for individual experiments
or as mean values 6 SD of the pooled data of the experiments.
Maximal frequency of motoneuron activity was evaluated by counting
the spikes elicited in the motor nerve classes (BINs of 200 ms width)
by using a window discriminator. The resulting value was then transformed to spikes/s. Means were compared using a t-test (depending on
the sample size) (Dixon and Massey 1969; Sachs 1997). Means were
regarded as significantly different at P , 0.05. N 5 number of
experiments; n 5 sample size.
ROLE OF SENSORY SIGNALS IN INTERJOINT COORDINATION
FIG. 2. Comparison of the latency for suprathreshold levator motoneuron
activation in the inactive and active animal. Data from 19 experiments are
given. Each point represents the latency of levator motoneuron activation
during fCO elongation (n from 6 to 72). E, occurrence of the 1st action
potential in the inactive animal; F, occurrence of the first action potential in the
active animal.
FIG. 3. Frequency plot of the occurrence of transitions in activity between
trochanteral motoneurons in the active animal during continual stimulation of
the fCO. Each ramp-and-hold cycle was divided in 8 classes (BINs) of constant
length (500 ms). Insets: exemplification of the actual transition evaluated
(taken from the same experiment). A: frequency of transitions from depressor
to levator motoneuron activity (■, N 5 20, n 5 820) and frequency of
transition from levator to depressor motoneuron activity (h N 5 20, n 5 761).
B: frequency histogram for transitions from levator to depressor activity. In this
histogram, only those transitions are counted for which ongoing levator activity has been elicited by a previous elongation stimulus at the fCO (1st filled
BIN in A).
pressor motoneuron activity was 25.1 6 18.09 ms (N 5 3, n 5
111) and not significantly different.
The interjoint influence of sensory signals from the fCO was
even more obvious when evaluating the general occurrence of
transitions between activity in levator and depressor motoneuron pools in the active animal during ongoing ramp-and-hold
stimulation of the fCO. For evaluation (Fig. 3A), similar rampand-hold cycles from each experiment were divided in eight
BINs of constant length (500 ms), and the transitions in motoneuron activity were counted. In N 5 20 animals, n 5 820
transitions from depressor to levator motoneuron activity were
evaluated during continual ramp-and-hold stimulation of the
fCO. Transitions occurred mostly (48.2%) during fCO elongation stimuli, i.e., within the first BIN (Fig. 3A) compared with
a low level of occurrence in the BINs of the remaining stimulus
cycle (5–10.6%). In the same animals, occurrence of the reverse motor response, i.e., a transition from levator to depressor motoneuron activity, was evaluated as well (N 5 20, n 5
761). This transition showed maximal occurrence during relaxation of the fCO (45.2%; 5th BIN). When evaluating specifically the termination of those levator bursts that had been
initiated by fCO elongation (N 5 20; n 5 395), i.e., the end of
only those bursts that were counted in the first BIN of Fig. 3A,
it became obvious that in the majority these bursts (44.1%, Fig.
3B) were terminated by the next relaxation stimulus at the fCO.
Intracellular recordings from trochanteral motoneurons re-
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In 45% of the experiments, i.e., in 9 of 20, ramp-and-holdstimulation of the fCO could completely pattern the activity in
trochanteral motoneurons for longer sequences of the stimulus
protocol. Elongation stimuli elicited levator motoneuron activity and terminated depressor motoneuron activity. Relaxation
stimuli had the reverse influence (Fig. 1D). This phenomenon
strongly resembled the ‘‘entrainment’’ of rhythm-generating
network by proprioceptive signals that was shown previously
in a variety of locomotor systems (e.g., Andersson and Grillner
1983; Grillner and Wallén 1977; Reye and Pearson 1988; Sillar
et al. 1986).
The latency after which levator and depressor activity was
affected in the active animal by elongation and relaxation of
the fCO did exhibit considerable variability. Neither initiation
of levator motoneuron activity by fCO elongation (Fig. 2) nor
activation of depressor activity by fCO relaxation occurred at
a fixed latency after the onset of the stimulus. Both transitions
could take place sometime throughout the ramp movement of
the fCO. As such, the latency for activation of levator motoneurons by fCO elongation was generally much longer and
more variable than the latency of the response in the inactive
behavioral state. For one preparation the mean latency of
activation in levator motoneurons in the inactive state was
12.0 6 7.9 ms (n 5 9), whereas the mean latency was 436.0 6
119.0 ms (n 5 32) in the same animal when being active.
As shown earlier (Fig. 1), movement signals from the fCO
did induce specific transitions in activity in trochanteral motoneurons. A common feature of these transitions was that
there was no overlap between the activity of semifast and fast
motoneurons of levator and depressor motoneurons. Termination of activity in one motoneuron pool was complete before
the antagonist turned active. The mean time for the switch in
activity between depressor and levator motoneurons induced
by fCO elongation was 32.8 6 21.53 ms (N 5 3, n 5 122). The
mean latency for the reverse switch between levator and de-
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FIG. 5. Relation between the generation of the reflex reversal on fCO
elongation in tibial motoneurons (‘‘active reaction’’) and the occurrence of the
transition in activity between depressor and levator motoneurons of the coxatrochanteral (CT) joint in the active animal. A: frequency of occurrence of
transition in trochanteral motoneuron activity when an active reaction in tibial
motoneurons is generated (N 5 16, n 5 353). B: frequency of occurrence of
an active reaction in tibial motoneurons when an activity transition in trochanteral motoneurons is generated (N 5 16, n 5 344). Please note that both events
can occur independently from each other with similar probability (for details,
see text).
Correlation between intrajoint (FT joint) and interjoint
(CT joint) influences of sensory signals from the fCO
in the active animal
FIG. 4. Intracellular recordings from levator and depressor trochanteris
motoneurons in the active animal during transition of motoneuronal activity (2
examples, top) and in the inactive animal (1 example, 2nd trace from bottom).
A: semifast levator motoneuron (Lev MN). B: slow depressor trochanteris
motoneuron (SDTr). Please note the marked depolarization occurring in the
active animal for the levator motoneuron with fCO elongation, and for SDTr
with fCO relaxation. - - -, resting potential before stimulus onset. Action
potentials are clipped.
From these observations, it is clear that in the active behavioral state signals from the fCO induce activity transitions the
trochanteral motoneurons. The question arose as to whether the
observed motoneuronal response to fCO stimulation was
linked to the motoneuronal activity of the FT joint. FT motoneurons are affected strongly by sensory signals from the
fCO in the inactive and active behavioral state. In the active
state, movement signals from the fCO induce a specific intrajoint motoneuronal response in tibial motoneurons, i.e., a reflex
reversal (‘‘active reaction’’) (Bässler 1976, 1988). Initial data
(Hess and Büschges 1997) did not suggest a coupling between
the generation of the reflex reversal in the FT joint and the
transition in motoneuronal activity induced in the motoneuron
pools of the CT joint. This conclusion was supported further by
additional experiments that focused on the occurrence of both
types of motoneuronal responses in the active state (Fig. 5).
Both responses can occur either together or independently from
each other. It thus is clear that in the active behavioral state the
influence of sensory signals from the fCO on trochanteral
motoneurons is not causally linked to the generation of a reflex
reversal in the FT-joint leg muscle control system.
Role of position signals from the fCO
In the following, we investigated what role position and/or
velocity signals from the fCO play for the induction of transitions in activity between trochanteral motoneuron pools. We
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vealed that in the active state, there was a marked enhancement of
synaptic inputs induced by sensory signals from the fCO compared with the inactive state (Fig. 4). Elongation of fCO led to an
increased depolarization in levator motoneurons and an increased
hyperpolarization in the slow depressor motoneuron (N 5 3) as
compared with the inactive state (Fig. 4, A and B). On some
occasions we observed a slight depolarization of depressor motoneurons that preceded their stimulus-induced hyperpolarization
(see Fig. 4B). Relaxation of the fCO led to an increased depolarization in depressor motoneurons compared with the inactive
animal (Fig. 4B). Termination of levator motoneuronal activity
during relaxation signals from the fCO was the result of the
membrane potential returning to the level before fCO stimulation
without the occurrence of a marked hyperpolarization. It is not
clear as yet as to the repolarization in levator motoneurons results
from an inhibitory influence or from discontinuation of an excitatory influence (N 5 3; Fig. 4A).
ROLE OF SENSORY SIGNALS IN INTERJOINT COORDINATION
focused mainly on the role of fCO elongation, but we also will
report briefly the results from fCO relaxation.
First, we investigated whether the starting position of the
fCO movement (i.e., the starting angle of the FT joint) affected
the induction of transition in motoneuronal activity between
levator and depressor motoneurons (N 5 4; Fig. 6). For elongation stimuli, we tested fCO stimuli of constant amplitude
(60°) from different starting positions (145, 120, and 95°) and
compared the probability of induction of a transition in activity
from depressor to levator motoneuron activity. Elongation
stimuli at the fCO could elicit the transitions in motoneuron
activity independent from the starting position (Fig. 6A). There
was no difference in the probability for eliciting a transition in
motoneuronal activity with respect to the starting position for
stimuli from 95 and 120°. However, probability was decreased
slightly for stimuli starting from 145° (Fig. 6B).
Second, we investigated whether the latency of onset of
levator motoneuron activity after the start of fCO elongation
depended on the starting position of the stimulus. We tested
this for stimuli with a common velocity of 120°/s (Fig. 6C)
from three different starting positions. There was no significant
difference in the latency of levator motoneuron activation for
the starting positions 95 and 120°. Only in case of the most
extended fCO starting position (145°), was the latency significantly longer (P , 0.01).
Third, we investigated the relation between the switch in
activities of the trochanteral motoneurons and the angular
change in the FT joint from stimulus onset (Fig. 6D). We
stimulated the fCO with ramp-and-hold stimuli of constant
amplitude but from three differing starting positions. The
change in fCO position at the time of transition from depressor
to levator activity during the ramp stimulus was evaluated in
relation to stimulus onset, and the equivalent joint angle was
calculated and plotted versus the joint angle of the starting
position. Figure 6D shows that the transition between motoneuronal activity occurred irrespective of the starting position. This result furthermore shows that there is obviously no
fixed position at which the transition in activity between both
motoneuron pools occurs (see also Fig. 2).
Finally, we tested whether there was a correlation between
maximal motoneuron activity during bursts of activity induced
and the starting position of the stimulus (Fig. 6E). For the extracellularly recorded levator motoneurons, we evaluated the maximum compound discharge rate in nerve C1 induced by fCO
elongation. Maximum levator motoneuron activity during the
burst initiated by fCO elongation was similar for stimuli starting
from 95 and 120° but significantly lower at 145° (Fig. 6E). These
results were different from the situation in the inactive state in
which levator activity induced by fCO elongation does show a
marked dependence on fCO position (Fig. 6E, ‚).
Similar results were obtained for the transition between
levator and depressor motoneuron activity induced by fCO
relaxation (not shown).
Role of velocity signals from the fCO
To investigate what influence velocity signals from the fCO
may have on the induction of a transition in activity between
trochanteral motoneurons (Fig. 7A), we first tested the probability of initiation of a transition for six different elongation
stimulus velocities, i.e., 20, 60, 120, 200, 600, and 1,200°/s
(Fig. 7B). There was no significant difference in the probability
for the induction of a transition between the different stimulus
velocities.
Second, we investigated whether the maximal motoneuronal
activity induced by fCO stimuli in trochanteral motoneuron
pools was correlated with stimulus velocity. We evaluated the
maximum frequency in levator nerve C1 that was elicited
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FIG. 6. A: influence of starting position of fCO movement on the release of
a transition in trochanteral activity in the active animal. Please note that in the
3 sample recordings a transition between depressor and levator motoneuron
activity occurs independent of the starting position at the fCO. B: plot of the
frequency of occurrence of transition between depressor and levator motoneuron activity vs. 3 different starting positions (N 5 4; n from 89 to 131). F,
values of individuals; E, mean for the pooled samples. C: latency of onset of
levator motoneuron activity after the onset of an fCO elongation stimulus
(velocity: 120°/s). F, values of individual animals tested (N 5 4; n from 12 to
26); E, mean values 6 SD (see METHODS for evaluation procedures). Please
note the latency of onset of levator activity is significantly (*) prolonged at a
starting position of 145°. D: plot of the angular change in femur-tibia (FT) joint
after stimulus onset at which the transition from depressor to levator activity
during fCO elongation vs. starting position of the stimulus. Values of all tested
velocities were pooled. F, values of 4 individual animals (n from 38 to 50); E,
mean values 6 SD for the sample. E: plot of the maximal frequency of levator
motoneuron activity, recorded from the levator nerve C1 induced by fCO
elongation vs. the starting position of fCO elongation. F, values of 4 individual
animals (n from 42 to 69); E, means 6 SD of the sample. Please note the
maximal levator activity is significantly (*) reduced with a starting position of
145°. For better comparison to the situation in the inactive animal mean values
for levator motoneuron activation in 2 inactive animals are given as well (‚; n
from 11 to 21).
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itative way by inducing or releasing transitions of activity
between both motoneuron pools of the CT joint.
Influence of sensory signals from the fCO on rhythmic
activity in trochanteral motoneurons of the otherwise
isolated and deafferented mesothoracic ganglion activated
by muscarinic agonists
during bursts of activity in trochanteral motoneuron pools by
ramp-and-hold stimuli at the fCO (Fig. 7A). We did not detect
any correlation between fCO stimulus velocities and maximum
motoneuronal activity (Fig. 7C). This situation strongly differs
from the inactive state of the animal, in which marked velocity
dependency of levator activity has been described (Fig. 7C, ‚)
(see also Hess and Büschges 1997)
Similar results were obtained for the transition between
levator and depressor motoneuron activity induced by fCO
relaxation (not shown).
In summary, movement signals from the fCO can induce
specific transitions in activity between the trochanteral levator and depressor motoneurons in the active stick insect.
The direction of movement appears to be the most relevant
feature for the transition induced. Position signals were
found to have no qualitative influence on the probability of
generation of the transitions but appear to affect the actual
activity of trochanteral motoneurons within the transition.
Elongation signals from the fCO were found to induce a
transition from depressor to levator activity and relaxation
signals induce the reverse transition. In the active state, in
contrast to the inactive state, we could not find a consistent
quantitative dependence of the performance of these transitions on fCO stimulus parameters (position and velocity). In
the active state, movement signals from the fCO can induce
activity changes in trochanteral motoneuron pools in a qual-
FIG. 8. Reset of the pilocarpine induced rhythmic activity in trochanteral
motoneurons by stimulation of the fCO. A: fCO elongation (Pos) terminated
ongoing depressor activity and induced levator activity (Lev). Relaxation of
the fCO did reset the rhythm by restarting it with the depressor phase of the
cycle (Dep). Arrowheads denote the expected time of occurrence of the onset
of depressor activity in the undisturbed situation. B: fCO elongation during the
levator phase of the cycle prolonged the levator activity. Subsequent relaxation
of the fCO did reset the rhythm by restarting rhythmic activity with the
depressor phase of the cycle.
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FIG. 7. Influence of stimulus velocity on the generation of transition in
activity between depressor and levator motoneurons. A: sample recordings
from 1 experiment showing that transition in activity can be elicited with
different stimulus velocities for fCO elongation. B: plot of the probability of
occurrence of transition in activity from depressor to levator motoneurons vs.
fCO elongation stimulus velocity. F, values of individual animals (N from 3 to
8, n from 56 to 216); E, mean of the pooled data. C: plot of the maximum
activation of levator motoneurons as recorded from the levator nerve C1
induced by fCO elongation vs. stimulus velocity. F, values of individual
animals (N from 2 to 5; n from 4 to 55); E, mean 6 SD of the sample. For
comparison to the situation in the inactive animal, mean values of maximal
levator motoneuron activation on the same stimuli in inactive animals are
given (‚ triangles; n from 6 to 12).
From the preceding results, the conclusion arises that signals
from the fCO may exhibit their influence on activity of trochanteral motoneurons by affecting central rhythm-generating
networks driving the motoneuron pools (Bässler 1993;
Büschges et al. 1995). To test this hypothesis, a preparation
was needed that had to meet two criteria: first, in contrast to the
active animal, such a preparation should exhibit regular rhythmic activity in leg motoneuronal pools. Second, it should allow
the stimulation of fCO afferents in an otherwise completely
isolated and deafferented situation to exclude any reafferent
effects on motor activity arising from other sense organs of the
middle leg. This can be achieved in a completely isolated and
deafferented thoracic ganglion in which central neuronal networks driving leg motoneuron pools can be activated pharmacologically by the muscarinic agonist pilocarpine (Büschges et
al. 1995).
Regular rhythmic activity was induced in trochanteral motoneurons by topical application of pilocarpine (Fig. 8). During
fictive rhythmic activity, sensory signals from the fCO strongly
affected trochanteral motoneuron activity in a way similar to
the one found in the active behavioral state of the animal.
Elongation of the fCO always reproducibly initiated levator
motoneuron activity and terminated depressor motoneuron activity if delivered during the depressor phase (Fig. 8A). In case
fCO elongation was delivered during levator activity, it was
enhanced and the burst duration in levator motoneurons could
ROLE OF SENSORY SIGNALS IN INTERJOINT COORDINATION
be prolonged (Fig. 8B). Relaxation signals from the fCO did
initiate depressor activity and terminated levator motoneuron
activity, if present (Fig. 8). Relaxation and elongation signals
from the fCO did induce a complete reset of the rhythm
generated (Fig. 8, A and B; compare arrowheads), as shown in
four experiments.
Furthermore, continual stimulation of the fCO with ramp-andhold stimuli could entrain rhythmic burst activity in trochanteral
motoneurons (N 5 15, Fig. 9, A and B). Levator activity was
elicited by fCO elongation and depressor activity was elicited by
fCO relaxation. fCO stimulation could entrain rhythmic activity
above and below the inherent rate of the preparation (Fig. 9, Ai
and B) provided that stimulation frequency was close to the
inherent frequency of the preparation. However, it partially failed
when the discrepancy was too large (Fig. 9Aii). This finding
closely resembled the situation in a fraction of the active animals
(see Fig. 1D) when trochanteral motoneuron activity sometimes
was coupled to continual fCO stimulation. We did not yet investigate systematically the frequency range of fCO stimulation that
could entrain the rhythm in trochanteral motoneurons. The membrane potential of trochanteral motoneurons was modulated by
fCO stimuli in the same way as in the active behavioral state. This
is shown for the slow depressor motoneuron in Fig. 9B (see Fig.
4B for comparison).
DISCUSSION
We have shown that movement signals from the FT joint do
take part in patterning motoneuronal activity of the CT joint in
the active behavioral state with the locomotor system being
active. Elongation of the fCO, mimicking joint flexion, induced
a transition from depressor to levator activity and relaxation of
the fCO, mimicking joint extension, induced the opposite transition. Compared with the interjoint reflex response of the
inactive state, the influence of sensory signals from the fCO in
the active state represents a drastic increase and thus a qualitative change. This influence of sensory signals from the fCO
was not related to motor activity in the FT-joint motoneuron
pools, i.e., the generation of the reflex reversal. The occurrence
of the activity transitions in the trochanteral motoneurons furthermore appeared to depend on the direction of the fCO
movement, i.e., either extension or flexion of the FT joint only.
The generation of the transitions appeared to be basically
independent of specific stimulus parameters at the fCO, i.e.,
starting position or stimulus velocity. In some animals, trochanteral motoneuron activity did couple tightly to ongoing
fCO stimulation, resembling entrainment of rhythmic motor
activity by sensory stimuli. In fictive, i.e., pilocarpine-activated, rhythmic preparations of the otherwise deafferented and
isolated mesothoracic ganglion fCO stimulation did reset and
entrain the ongoing rhythmic activity in trochanteral motoneurons. In summary, our results strongly suggest that when the
locomotor system is active, movement signals from the fCO do
have access to central rhythm generating networks that drive
trochanteral motoneurons.
Role of sensory signals from the fCO in interjoint
coordination between FT and CT joint in the active
behavioral state
First evidence for influences of sensory signals from the FT
joint on the activity of trochanteral motoneurons was derived
from experiments in which sensory input from the fCO was
reversed surgically by fixing its apodeme to the flexor muscle.
In these animals (i.e., with a so called ‘‘crossed fCO receptor
apodeme’’), extension of the FT joint during walking movements, now inducing elongation of the fCO, initiated leg levation during walking and severely perturbed the locomotor
output of the leg (‘‘saluting’’) (Bässler 1993; Graham and
Bässler 1981). In the present investigation, we have shown that
elongation signals from the fCO initiate leg levation by eliciting levator motoneuron activity and terminating depressor motoneuron activity.
The present findings may give rise to the assumption that
mainly sensory signals from the fCO determine trochanteral motoneuron activity. However, this view appears too simplistic in the
light of the following arguments: 1) effectiveness of fCO stimulation, as measured by the probability of occurrence for the
transitions, was not as high in the active behavioral state as in
fictive rhythmic preparations (70% in the active animal compared
with 100% in fictive rhythmic preparations), indicating that there
is not a completely fixed relationship between sensory signals
from the fCO and transitions in activity in trochanteral motoneurons and indicating that patterning of activity in trochanteral
motoneurons also is influenced by other sensory and central
influences. 2) Activity of trochanteral motoneurons in the active
state is as well influenced by signals from at least two other sense
organs, load-sensing sense organs, i.e., from the campaniform
sensillae (Bässler 1993), and signals from intrajoint proprioceptors, e.g., the trochanteral hairplates and strand receptors (Bräunig
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FIG. 9. Entrainment of the pilocarpine induced rhythmic activity in trochanteral motoneurons by signals from the fCO. Ai: on continual stimulation
of the fCO, each fCO elongation elicited levator motoneuron (Lev) activation
and each relaxation stimulus elicited depressor motoneuron (Dep) activation.
Cycle period of rhythmic activity was 4.7 6 0.5 s before stimulation and 4.6 6
0.9 s after stimulation. Ramp-and-hold stimulus period was 4 s. ii: please note
that rhythmic activity in trochanteral motoneurons was not entrained with
stimulus protocol exceeding the inherent frequency of the preparation twofold
(example given on right; see text). Cycle period of rhythmic activity was 4.2 6
0.1 s before and 4.2 6 0.1 s after fCO stimulation. Ramp-and-hold stimulus
period was 2 s. B: intracellular recording from SDTr during entrainment of
rhythmic activity. ■, time of occurrence and expected time of occurrence of a
depressor motoneuron burst before and during stimulation of the fCO, respectively.
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Neuronal control networks governing active leg movements
Our results may appear interesting in the light of the present
understanding of movement generation in multijointed limbs.
This is because data from ‘‘fictive rhythmic’’ preparations of
locomotor systems emphasized the major role of ‘‘centrally
preprogrammed’’ coupling between adjacent leg joints by the
action of a common central pattern generator for locomotion
(e.g., crayfish: Crachri and Clarac 1990; locust: Ryckebusch
and Laurent 1993; cat: summary in Grillner 1981). Flexibility
of the locomotor output generated and its proprioceptive regulation, however, resulted in the formulation of more complex
ideas on the construction of pattern generators for locomotion,
i.e., the ‘‘unit-burst generator concept’’ (summary in Grillner
1981) and the ‘‘module concept’’ (summary in Bässler 1993).
Our findings clearly indicate a pivotal role of sensory signals in
the establishment of interjoint coordination during locomotion. In
the stick insect walking system, individual central rhythm-gener-
ating premotor networks exist for the different leg joints of each
leg (Bässler and Wegner 1983; Büschges et al. 1995). Recently
evidence was presented for central as well as peripheral signals
contributing to interjoint coordination during the execution of
active leg movements (Bässler 1993; Büschges et al. 1995). Up to
now, however, it still remained unclear whether there was a direct
influence of sensory signals of one leg joint on the rhythmgenerating networks of the adjacent leg joint. From our experiments, it has become clear that indeed sensory signals from
proprioceptors of one leg joint do have access to rhythm generating networks of adjacent leg joints.
It is not clear yet, how this influence is mediated. This
applies specifically for sensory-motor pathways that underlie
interjoint posture control action in the inactive state (Hess and
Büschges 1997). Direct as well as polysynaptic pathways have
been described that transfer information from the fCO onto
trochanteral motoneurons. Preliminary data suggest their contribution. For example, interneurons contributing to interjoint
reflex action in the inactive animal by disinhibition of levator
motoneurons, i.e., Li1 and Li2, do show drastically enhanced
inhibitory synaptic inputs during fCO-induced levator activation in the active behavioral state (unpublished observation).
In the crayfish, evidence was presented for the phasic control
of the efficacy of direct pathways from sensory signals from
one leg joint, i.e., the coxa-basopodit joint, to motoneurons of
the adjacent thoraco-coxal joint to contribute to interjoint reflex
action on the adjacent during the exhibition of rhythmic motor
activity (El Manira et al. 1991). This control of synaptic
efficacy was provided by phasic presynaptic inhibition of sensory afferents by signals from central rhythm generating networks. In the stick insect, it is not clear yet which mechanisms
mediate the influence of sensory signals from the fCO onto
trochanteral motoneuron pools in the active animal. Mechanisms similar to the ones described in crayfish may contribute
to the increased influence of sensory signals from the fCO in
the active behavioral state, in comparison with the inactive
animal. Future investigations will have to unravel the neuronal
mechanisms that mediate the influence of sensory signals from
the fCO on rhythm generation in the trochanteral motoneurons.
The authors acknowledge the steady support provided by U. Bässler. Furthermore we thank U. Bässler, S. Grillner, G. Wendler, H. Scharstein, J.
Schmidt, and H. Fischer for fruitful discussions during the course of the work
and/or for comments on the manuscript. We are grateful for the helpful
suggestions of two anonymous referees.
This work was supported by Deutsche Forschungsgemeinschaft Grants
Bu857/2-2 and /6-1. A. Büschges is a Heisenberg-fellow of the Deutsche
Forschungsgemeinschaft. The experiments comply with ‘‘Principles of Animal
Care,’’ (no. 0.86-23, revised 1985) and with current laws in Germany.
Present address of D. Hess: Nobel Institute for Neurophysiology, Dept. of
Neuroscience, Karolinska Institutet, 17177 Stockholm, Sweden.
Present address and address for reprint requests: A. Büschges, Dept. of
Animal Physiology, Institute of Zoology, University of Köln, Weyertal 119,
50923 Köln, Germany.
Received 2 October 1998; accepted in final form 16 December 1998.
REFERENCES
ANDERSSON, O. AND GRILLNER, S. Peripheral control of the cat’s step cycle. II.
Entrainment of the central pattern generators for locomotion by sinusoidal
hip movements during fictive locomotion. Acta Physiol. Scand. 118: 229 –
239, 1983.
ANGEL, M. J., GUERTIN, P., JIMÉNEZ, I., AND MCCREA, D. A. Group I extensor
afferents evoke disynaptic EPSPs in cat hindlimb extensor motoneurons
during fictive locomotion. J. Physiol. (Lond.) 494: 851– 861, 1996.
Downloaded from http://jn.physiology.org/ by 10.220.33.5 on June 18, 2017
and Hustert 1983; Schmitz 1985). These sensory systems contribute to the patterning of trochanteral motoneuron activity in the
active animal (Bässler 1993; Schmitz and Schöwerling 1992).
The influence of sensory signals from the fCO on CT-joint
motoneuron activity may contribute to the coordination of movements between both leg joints when the locomotor system is
active. This becomes obvious from the interjoint coordination
during searching and walking movements in the single-leg preparation (Bässler et al. 1991; Haas et al. 1996) and from the role
that exhibition of the reflex reversal in the FT-intrajoint control
networks plays in the generation of the locomotor cycle: 1) during
walking movements in the single leg preparation, front legs and
middle legs flex the FT joint during stance and extend the FT joint
during swing. Concurrently during late stance and early swing, the
CT joint is levated and the CT joint is depressed in late swing after
extension of the FT joint. The interjoint coordination is similar for
both leg joints during searching movements (Bässler 1993). 2)
There was no fixed coupling between the generation of the reflex
reversal (‘‘active reaction’’) (Bässler 1988) in the FT joint and the
generation of a transition in activity between trochanteral motoneurons. Bässler (1988) has shown that the initiation of extensor
activity in the second part (part II) of the active reaction after the
reflex reversal (part I) (Bässler 1988) reflects a portion of the
locomotor cycle, i.e., the transition from stance to swing. Transition between trochanteral depressor to levator activity was independent of the active reaction of the extensor motoneurons. It
mostly occurred rather late during fCO elongation, i.e., FT-joint
flexion, and the levator activity initiated could outlast the stimulus
(Figs. 1–3), suggesting that sensory signals from the fCO may
contribute to levator activation at the end of stance and the begin
of swing. Thus our data indicate that movement signals from the
fCO can contribute to establishing proper interjoint coordination
between FT joint and CT joint.
However, with respect to an immediate functional interpretation of the gathered results toward an understanding of walking
pattern generation in the intact walking stick insect middle leg, it
should be kept in mind that marked appropriate changes in the
angle of the FT joint during stance only occur in the front leg,
whereas they are much more subtle for the middle leg (Bässler
1988). This restriction, however, does not affect our basic finding,
that sensory signals from the fCO take part in patterning of motor
activity in the CT joint.
ROLE OF SENSORY SIGNALS IN INTERJOINT COORDINATION
GRILLNER, S. Neurobiological bases of rhythmic motor acts in vertebrates.
Science 228: 143–149, 1985.
GRILLNER, S. AND WALLÉN, P. Is there a peripheral control of the central pattern
generators in the dogfish? Brain Res. 127: 291–295, 1977.
GRILLNER, S. AND ZANGGER, P. On the central generation of locomotion in the
low spinal cat. Exp. Brain Res. 43: 241–261, 1979.
HAAS, R., DITTBERNER, O., AND BÜSCHGES, A. A ‘‘semi-intact’’ single-walking
preparation for the investigation of interleg reflexes between middle legs in
the stick insect. In: Proceeding of the 24th Göttingen Neurobiology Conference, edited by N. Elsner and H. U. Schnitzler. New York: Georg Thieme
Verlag, 1996, vol. 2, Poster 103.
HESS, D. AND BÜSCHGES, A. Sensorimotor pathways involved in interjoint
reflex action of an insect leg. J. Neurobiol. 33: 891–913, 1997.
HOFMANN, T. AND BÄSSLER, U. Anatomy and physiology of trochanteral
campaniform sensilla in the stick insect, Cuniculina impigra. Physiol. Entomol. 7: 413– 426, 1982.
MARQUARDT, F. Beiträge zur Anatomie der Muskulatur und der peripheren Nerven
von Carausius morosus. Zool. Jahrb. Abt. Anat. Ontol. 66: 63–128, 1940.
PEARSON, K. G. Common principles of motor control in vertebrates and
invertebrates. Annu. Rev. Neurosci. 16: 265–297, 1993.
PEARSON, K. G. AND COLLINS, D. F. Reversal of influence of group Ib afferents
from plantaris on activity in medial gastrocnemius during locomotor activity. J. Neurophysiol. 70: 1009 –1017, 1993.
PEARSON, K. G. AND ILES, J. F. Nervous mechanisms underlying intersegmental
co-ordination of leg movements during walking in the cockroach. J. Exp.
Biol. 58: 725–744, 1973.
PROCHAZKA, A. Proprioceptive feedback and movement regulation. In: Handbook of Physiology. Exercise: Regulation and Integration of Multiple Systems. New York: Am. Physiological Soc., 1996, sect. 12, p. 89 –127.
REYE, D. N. AND PEARSON, K. G. Entrainment of the locust central flight
oscillator by wing stretch receptor stimulation. J. Comp. Physiol. [A] 162:
77– 89, 1988.
ROBERTSON, G. A., MORTIN L. I., KEIFER, J., AND STEIN, P.S.G. Three forms of
the scratch reflex in the spinal turtle: central generation of motor pattern.
J. Neurophysiol. 53: 1517–1534, 1985.
ROSSIGNOL, S., LUND, J. P., AND DREW, T. Neural control of rhythmic movements in vertebrates. In: The Role of Sensory Inputs in Regulating Patterns
of Rhythmical Movements in Higher Vertebrates, edited by A. Cohen, S.
Rossignol, and S. Grillner. New York: Wiley, 1988, chapt. 7, p. 201–283.
RYCKEBUSCH, S. AND LAURENT, G. Rhythmic pattern evoked in locust leg
motor neurons by the muscarinic agonist pilocarpine. J. Neurophysiol. 69:
1583–1595, 1993.
SACHS, L. Angewandte Statistik. VIII. Auflage. Berlin: Springer Verlag, 1997.
SCHMITZ, J. Control of the leg joints in stick insects: differences in the reflex
properties between the standing and the walking states. In: Insect Locomotion. Proceedings of Symposium 4.5 from the XVII International Congress of
Entomology, edited by M. Gewecke and G. Wendler. Berlin: Verlag Paul
Parey, 1985, p. 27–32.
SCHMITZ, J., BÜSCHGES, A., AND DELCOMYN, F. An improved electrode design
for en passant recording from small nerves. Comp. Biochem. Physiol. A
Physiol. 91: 769 –772, 1988.
SCHMITZ, J., DEAN, J., AND KITTMANN, R. Central projections of leg sense
organs in Carausius morosus. Zoomorphology 111: 19 –33, 1991.
SCHMITZ, J.AND SCHÖWERLING, H. No effects of coxo-trochanteral proprioceptors on extensor tibiae motoneurons in posture control. In: Proceeding of the
20th Göttingen Neurobiology Conference, edited by N. Elsner and D. W.
Richter. Stuttgart, New York: Georg Thieme Verlag, 1992, poster 118.
SILLAR K. T., SKORUPSKI, P., ELSON, R. C., AND BUSH, B.M.H. Two identified
afferent neurons entrain a central locomotor rhythm generator. Nature 323:
440 – 443, 1986.
SKORUPSKI, P. AND SILLAR, K. T. Phase-dependent reversal of reflexes mediated by the thoracocoxal muscle receptor organ in the crayfish, Pacifastacus
leniusculus. J. Neurophysiol. 55: 689 – 695, 1986.
STORRER, J., BÄSSLER, U., AND MAYER, S. Motor neurons in the meso- and
metathoracic ganglion of the stick insect, Carausius morosus. Zool. Jahrb.
Physiol. 90: 359 –374, 1986.
WEIDLER, D. J. AND DIECKE, F.P.J. The role of cations in conduction in the
central nervous system of the herbivorous insect Carausius morosus. Z. Vgl.
Physiol. 64: 372–399, 1969.
WEILAND, G. AND KOCH, U. T. Sensory feedback during active movements of
stick insects. J. Comp. Physiol. [A] 133: 137–156, 1987.
WENDLER, G. Laufen und Stehen der Stabheuschrecke Carausius morosus:
Sinnesborstenfelder in den Beinen als Glieder von Regelkreisen. Z. Vgl.
Physiol. 48: 198 –250, 1964.
Downloaded from http://jn.physiology.org/ by 10.220.33.5 on June 18, 2017
BARTLING, C. Die Bewegungen der Stabheuschrecke Carausius morosus in
verschiedenen Laufsituationen (Masters thesis). Bielefeld, Germany: University of Bielefeld, 1993.
BÄSSLER, U. Reversal of a reflex to a single motoneuron in the stick insect
Carausius morosus. Biol. Cybern. 24: 47– 49, 1976.
BÄSSLER, U. Sense organs in the femur of the stick insect and their relevance
to the control of position of the femur-tibia-joint. J. Comp. Physiol. [A] 121:
99 –113, 1977.
BÄSSLER, U. Neuronal Basis of Elementary Behavior in Stick Insects. Berlin:
Springer Verlag, 1983.
BÄSSLER, U. Functional principles of pattern generation for walking movements of stick insect forelegs: the role of the femoral chordotonalorgan
afferences. J. Exp. Biol. 136: 125–147, 1988.
BÄSSLER, U. The walking- (and searching-) pattern generator of stick insects,
a modular system composed of reflex chains and endogenous oscillators.
Biol. Cybern. 69: 305–317, 1993.
BÄSSLER, U. AND BÜSCHGES, A. Pattern generation for stick insect walking
movements—multisensory control of a locomotion program. Brain Res.
Rev. 27: 65– 88, 1998.
BÄSSLER, U., ROHRBACHER, J., KARG, G., AND BREUTEL, G. Interruption of
searching movements of partly restrained front legs of stick insects, a model
situation for the start of a stance phase? Biol. Cybern. 65: 507–514, 1991.
BÄSSLER, U. AND WEGNER, U. Motor output of the denervated thoracic ventral
nerve cord in the stick insect Carausius morosus. J. Exp. Biol. 105: 127–145,
1983.
BRÄUNIG, P. AND HUSTERT, R. Proprioceptive control of a muscle receptor
organ in the locust. Brain Res. 274: 341–343, 1983.
BÜSCHGES, A. Nonspiking pathways in a joint-control loop of the stick insect
Carausius morosus. J. Exp. Biol. 151: 133–160, 1990.
BÜSCHGES, A. AND EL MANIRA, A. Sensory pathways and their modulation in
the control of locomotion. Curr. Opin. Neurobiol. 8: 733–739, 1998.
BÜSCHGES, A., SCHMITZ, J., AND BÄSSLER, U. Rhythmic pattern in the thoracic
nerve cord of the stick insect induced by pilocarpine. J. Exp. Biol. 198:
435– 456, 1995.
CHENG, J., STEIN, R. B., JOVANOVIC, K., YOSHIDA, K., BENNET, D. J., AND HAU,
Y. Identification, localization, and modulation of neural networks for walking in the mudpuppy (Necturus maculatus) spinal cord. J. Neurosci. 18:
4295– 4304, 1998.
CHRACHRI, A. AND CLARAC, F. Fictive locomotion in the fourth thoracic ganglion of the crayfish, Procambarus clarkii. J. Neurosci. 10: 707–719, 1990.
CLARAC, F. How do sensory and motor signals interact during locomotion? In:
Motor Control: Concepts and Issues, edited by D. R. Humphrey and H.-J.
Freund. New York: John Wiley, 1991, p. 199 –221.
CONWAY, B. A., HULTBORN, H., AND KEIN, O. Proprioceptive inputs reset central
locomotor rhythm in the spinal cat. Exp. Brain Res. 68: 643– 656, 1987.
CRUSE, H. The function of the legs in the free walking stick insect, Carausius
morosus. J. Comp. Physiol. [A] 112: 235–262, 1976.
CRUSE, H. Coactivating influence between neighbouring legs in walking insects. J. Exp. Biol. 114: 513–519, 1985.
DICAPRIO, R. A. AND CLARAC, F. Reversal of a walking leg reflex elicited by
a muscle receptor. J. Exp. Biol. 90: 197–203, 1981.
DIXON, W. J. AND MASSEY, F. J. Introduction to statistical analysis (3rd ed.).
New York: McGraw Hill, 1969.
DRIESANG, R. AND BÜSCHGES, A. Physiological changes in central neuronal
pathways contributing to the generation of a reflex reversal. J. Comp.
Physiol. 179: 45–57, 1996.
DUYSENS, J. AND TAX, A.A.M. Interlimb reflexes during gait in cat and man. In:
Interlimb Coordination: Neuronal, Dynamical and Cognitive Constraints,
edited by S. P. Swinnen, H. Heuer, J. Massion, and P. Caesar. London:
Academic Press, 1994, p. 97–126.
EL MANIRA, A., DICAPRIO, R. A., CATTAERT, D., AND CLARAC, F. Monosynaptic interjoint reflexes and their central modulation during fictive locomotion in crayfish. Eur. J. Neurosci. 3: 1219 –1231, 1991.
FOTH, E. AND BÄSSLER, U. Leg movements of stick insect walking with five
legs on a treadwheel and with one leg on a motor-driven belt. I. General
results and 1:1 coordination. Biol. Cybern. 51: 313–318, 1985.
GRAHAM, D. AND BÄSSLER, U. Effects of afference sign reversal on motor activity
in walking stick insect (Carausius morosus). J. Exp. Biol. 91: 179–193, 1981.
GRILLNER, S. Locomotion in vertebrates: central mechanisms and reflex interactions. Physiol. Rev. 55: 247–304, 1975.
GRILLNER, S. Control of locomotion in bipeds, tetrapods and fish. In: Handbook of
Physiology. The Nervous System. Motor Control, edited by V. B. Brooks.
Bethesda, MD: Am. Physiol. Soc., 1981, sect. 1, vol. 2, p. 1179–1236.
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