Rapid mechano-sensory pathways code leg impact and elicit very rapid reflexes in insects
Institut für Zoologie und Anthropologie der Universität Göttingen, Berliner Str. 28, D-37073 Göttingen, Germany
* Author for correspondence (e-mail: rhuster{at}gwdg.de)
Accepted 13 May 2003
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Summary |
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Key words: mechanosensory afferent, leg impact, timing, motor response, landing, locomotion, locust, Schistocerca gregaria
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Introduction |
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Previously, it was hypothesised
(Wilson, 1965) that insects
stepping at high frequencies, such as cockroaches or flies, might only use an
integrated signal from all leg afferents for the sensory control of walking
rather than the detailed signals of contact, load and joint angles in each leg
during a step. By contrast, Jindrich and Full
(2002
) postulate that
deviations of a running cockroach from its path are compensated mainly by
viscoelastic components in the skeletomotor system of the legs. This mechanism
would prevail over sensorimotor responses, with delays in the range of
1015 ms for cockroach motor responses, as found by Ridgel et al.
(2001
) after stimulation of
tibial campaniform sensilla (CS). However, if leg contact is monitored by
proximal CS, the delay for reflex support and load compensation may be reduced
sufficiently to allow neural properties to affect movement even at relatively
rapid walking speeds. To test this hypothesis, we studied the timing and
cooperation of distal and proximal mechanoreceptors for the middle legs of
locusts, which basically perform a rowing-type movement about an axis
transverse to the body during walking
(Hustert, 1983
). In these
legs, the depressor muscles support the ipsilateral half of the body regularly
when the animal walks in tripod gait. As an indicator of the speed of sensory
information processing and of reflex convergence, we selected motoneurons of
the tripartite depressor trochanteris muscle (M103;
Snodgrass, 1929
). This muscle
is in close proximity to the CNS and is most important for keeping the body
above ground and therefore should receive the earliest afferent commands
available from the periphery.
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Materials and methods |
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Intracellular recordings
A wax-coated steel platform was used to stabilize the meso- and
metathoracic ganglia. The ganglionic sheath of the mesothoracic ganglion was
treated for 2 min with a 1% (w/v) solution of protease (Sigma type XIV) to
facilitate penetration of the ganglion with glass microelectrodes.
Microelectrodes were either filled with 2 mol l-1 potassium
acetate or 1 mol l-1 lithium chloride when used for later staining
with Lucifer yellow (only in the tips), giving a tip resistance of 4080
M.
The dye was applied iontophoretically by 500 ms pulses of negative current
at 1 Hz. Motoneurons were identified by correlating the spikes recorded
intracellularly from neuropilar processes, while extracellular potentials were
recorded from the efferent nerve 3C2 with a pair of 50 µm steel wires. The
M103d fast motoneuron could also be identified as eliciting visible
twitch-contractions of M103d upon stimulation (nomenclature of thoracic nerves
according to Campbell,
1961).
Afferent spike recordings
Spikes from single tibial hair sensilla were recorded by placing a
saline-filled microelectrode over the cut shaft of the trichoid sensillum
(Hodgson et al., 1955).
Afferent spikes from the exteroceptive campaniform sensilla (CS) at the base
of each tibial spur were recorded with hook electrodes at the peripheral
nerves 5B3 (anterior row of spurs) or 5B4 (posterior row of spurs) located
just beneath the ventral cuticle close to the receptors
(Mücke, 1991
).
In order to record afferent discharges selectively via the proprioceptive CS on various leg segments, an electrolytically sharpened tungsten wire was carefully pushed through the dome-shaped structure of the sensillum to make contact with the receptor haemolymph.
Trochanteral groups of CS were recorded in isolated legs with suction
electrodes from the proximal stumps of their afferent nerve (5B2a), in which
at least one large trachea was opened to the air at the saline surface, while
the persistent pumping of the myogenic accessory leg heart of the trochanter
(Hustert, 1999) maintained
saline flow in the leg. This expands viability of the preparation from several
minutes to several hours.
Motoneuron identification
Backfills of motor nerves were made to reveal the innervation of the
mesothoracic depressor trochanteris muscle and central branching pattern of
each motoneuron. After removal of the thoracic ganglia from the animal, the
cut end of the particular nerve was placed in a miniature VaselineTM
well, filled with a near-saturation solution of 3000 Mr
dextrane conjugated with the fluorescent dyes fluorescein isothiocyanate
(FITC) or tetraethyl-rhodamine-isothiocyanate (TRITC) (obtained from Molecular
Probes Europe, Leiden, The Netherlands). The preparations were immersed in
saline and incubated for 24 h at 4°C to allow diffusion of the dye
throughout the neurons. After dissecting out the ganglia, they were fixated in
4% paraformaldehyde, dehydrated in ethanol and, after clearing in methyl
salicylate, were viewed under a Leitz Aristoplan epifluorescence microscope
and drawn or photographed from whole mounts.
Receptor stimulation
All receptors were stimulated mechanically. In the case of the hair
sensilla, a blunt microelectrode was glued to a piezoelectric tongue driven by
a function generator and mounted onto a micromanipulator. Ramp-like
deflections were used to stimulate the hair sensilla. The tibial spurs were
deflected by a minuten pin fixed to the piezoelectric tongue. The
proprioceptive CS were stimulated directly by applying pressure perpendicular
to the surface of the cuticle close to the receptor with a minuten pin. In
some cases, the tungsten electrode itself was pushed carefully towards the
sensillum to elicit spikes.
In order to define delays between afferent spike generation of two different receptor types, e.g. a tibial spur and a trochanteral CS, a two-channel function generator driving two piezoelectric devices was used for the exact timing of receptor stimulation.
Conduction measurements
Afferent conduction times to the CNS were measured by recording
extracellularly from a peripheral site of the particular nerve close to the
mechanoreceptor and at the main leg nerve 5 where it enters the ganglion.
Central latencies could thus be estimated by subtracting this time of spike
propagation from the overall delay to the postsynaptic potential
(Laurent and Hustert, 1988).
In most cases, signal averaging was used.
Mechano-sensory conduction
Delays between impact-like tension changes onto the tarsus and first
afferent spikes in the proximal CS were measured in middle legs, excised
carefully at the thoracocoxal joint. The leg was positioned as in the standing
animal, with the coxa, trochanter and femur horizontal and the tibia vertical.
Only the coxa was fixed on a small platform ventrally, and dorsal parts of the
coxa and trochanter levator muscles were removed. The tendon of the trochanter
depressor was also pinned with a minuten pin to the platform. This avoided
dorsal excursions of the leg when mechanical stimuli directed dorsally at the
tarsus were applied by a piezoelectric bender from below.
Force measurements
Measurements of the time required for the transfer of force from the tip to
the base of a leg were also performed on a fresh, isolated middle leg in the
natural positions of still stance. The ventral coxa was mounted onto a force
transducer while forces from the tarsus were applied via one pad
(pulvillus). A piezoelectric tongue (bimorphic piezoceramic strip; Valvo
PXE70; Valvo, Hamburg, Germany) with a minuten needle extending from its
moveable end was mounted on another force transducer. The strain produced by
the piezoelectric tongue during ramp-like deflection (generated by a function
generator) was monitored when the minuten pin indented the highly elastic
tarsal pulvillus. By mounting the device on a micromanipulator, the tip of the
pin could touch the tarsal pulvilli very delicately so that just the area
around one of the canal sensilla (Kendall,
1970) was indented by the stimulus. This strain was sufficient to
be recorded via the whole leg as a force at the coxa-attached
transducer.
Recording and analysis
Recordings were displayed on a digital oscilloscope (Hitachi, Fukuoka,
Japan) and stored on magnetic tape for later computer analysis by Neurolab 7.0
(Hedwig and Knepper, 1992) and
Datapac 2000 (RUN Technologies, Mission Viejo, CA, USA) software.
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Results |
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Afferent conduction times in the leg
In order to see which afferent signals of mechanosensory neurons are the
first to reach the CNS after the mechanical contact, conduction times from
mechanosensory cells to the CNS were compared for different parts of the leg.
Three types of receptors can encode leg contact directly or indirectly
(Fig. 2A): (1) tarsal and
tibial mechanoreceptive hairs, being bent by touch, (2) a campaniform
sensillum (CS) at the base of each moveable tibial spur and (3) CS, singularly
or in groups, on the cuticle of all leg segments but the coxa. All record load
or strain from nearby or further away, e.g. when the tarsus or tibia contact
the substrate. During locust walking or landing, the tactile hairs that
completely cover the tibia or tarsus are often the first to encounter the
substrate in structured terrain. Afferent conduction times to the CNS are at
least 8 ms and even more than 12 ms from the distal hairs
(Fig. 2) as the rather distal
long unguis hairs, that have monosynaptic connections to motoneurons of the
depressor tarsi (Laurent and Hustert,
1988). None of these seem suitable to convey information on
substrate contact rapidly to the CNS. The CS of spines from different
locations on the tibia may also be the first sensilla to encounter mechanical
contact. Their afferents reach the CNS with a very similar delay of about
89 ms, since their individual conduction times compensate for their
proximo-distal position on the tibia (Fig.
2E). The CS that are located on the leg cuticle at varying
distances to the thorax mainly record strain between the body and the
substrate due to gravity or muscular tension
(Hustert, 1985
). The most
proximal of these are the trochanteral and femoral CS, which show the shortest
conduction times to the CNS (Fig.
2B,C; in the range of 1 ms).
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This observation led us to pursue the hypothesis that, after leg impact on distal segments, the proximal CS afferents could be the first of all sensory inputs from the leg to reach the CNS upon leg-to-substrate contact due to cuticular strain conducted rapidly in the leg.
Force transfer and sensory responses upon leg contact
The transfer of force to proximal leg segments upon slight indentation of a
tarsal pulvillus occurs within 1 ms (Fig.
3A). Proximally, such forces are recorded by trochanteral and
femoral CS. Responses of trochanteral CS can be recorded readily from their
afferent nerves while natural force transfer to the sensilla from the distal
leg occurs. The first afferent responses are elicited about 3 ms after the
onset of a dorsally directed ramp stimulus applied to the tarsus
(Fig. 3B,C). The signals from
the CS reach the CNS 34 ms after stimulus onset and form the most rapid
pathway indicating that forces are applied to the leg.
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The first incoming afferents from the proximal CS can initiate the first
efferent responses to leg impact in the leg depressor motoneurons. In response
to the same stimulus, mechanosensory afferents arrive 4 ms later from more
distal locations on the leg (Fig.
2).
Sensori-motor connections
Central timing and cooperation of afferents from selected single proximal
and distal sensilla were studied by recording the postsynaptic responses in
the fast and the slow motoneuron of the trochanter depressor M103d.
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Cooperation of afferents
Converging inputs onto the M103d motoneurons were elicited by stimulating
selectively a single posterior spur and the feCS2, since this may reflect the
situation of recording primary substrate contact by a tibial spur exiting its
sensory neuron and, by high-speed propagation of tension in the leg cuticle,
the feCS2 sensilla as well (Fig.
3). When single afferents from these mechanoreceptors produce
overlapping EPSPs in the M103d fast motoneuron they elicit spikes
(Fig. 6A,C), which cannot be
achieved by their isolated single EPSPs. So, for single afferent spikes, only
a precise timing of their onset in the periphery within a range of 47
ms delay from spur to feCS discharge could elicit motoneuron spikes reliably.
A comparable convergence occurs on the M103d slow motoneuron.
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Discussion |
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We have shown for locusts that when a leg makes contact with a substrate
the impact causes a shock wave of strain in the leg that progresses from the
tarsus proximally in the cuticle or often from the tibia in structured
terrain (Laurent and Hustert,
1988) or on stems (Hassenstein and Hustert, 1995) and
arrives at the body in less than 1 ms. This wave is far ahead of action
potentials conducted axonally from distal mechanoreceptors that were
stimulated directly by the same contact. The most proximal mechanoreceptors
able to detect this shock wave are CS of the proximal femur and trochanter,
which code and conduct this information within 1 ms to synapses in the CNS.
Motoneurons of the depressor trochanteris system receive these afferents
directly and can immediately release their efferent commands that increase
muscle tension and thereby keep the body off the ground. This rapid reflex
takes 57 ms from the time of mechanical contact to the first efferent
potentials arriving at the depressor trochanteris; in summary (1) 1 ms or less
for conduction of force in the leg cuticle, (2) 12 ms for raising the
receptor potential to spiking threshold in the CS, (3) 1 ms for the sensory
afferent conduction to the CNS, (4) 12 ms for the central delay and (5)
1ms for efferent conduction in the motoneuron to the neuromuscular
synapse. The delay until muscle tension rises after neuromuscular transmission
depends on the prevailing tension of the muscle.
The most obvious use of this pathway for a locust is when landing on a substrate with the legs after jumping or flight. It should be noted that the proximity of the depressor trochanteris muscles to the CNS also contributes to very low reflex times.
In cyclic movements, such as walking of cats and cockroaches
(Gorassini et al., 1994;
Delcomyn, 1973
), anticipation
of the forthcoming substrate contact of a leg starts depressor muscle
activities regularly before leg impact. After substrate contact of a toe in
cats, foot depressor activation increases rapidly within 1025 ms.
Timing is similar in leg depressors of running cockroaches
(Watson and Ritzman, 1998
;
Tryba and Ritzmann, 2000
). The
role of sensory feedback may differ at swing-to-stance transitions in locusts
and cockroach middle legs since in cockroaches the anterior sides of the leg
segments always face the substrate (steps mainly by pushing movements) while
in rowing movements in locusts anterior and posterior sides often alternate in
facing the substrate.
The basic problem of adequate timing of sensory input for motor control
also exists during rapid cyclic movements such as the wingbeat of insects,
which seems to be resolved by fast-conducting axonal pathways with
monosynaptic (locusts; Burrows,
1975; Stevenson,
1997
) and even electrotonic connections (flies;
Fayyazuddin and Dickinson,
1996
).
Walking in locusts also requires rapid switching of activity in antagonistic muscles timed by mechanoreceptors at the transitions from swing to stance phases. The rapidly conducting afferents we studied can encode tarsal or tibial contact and contribute to the transition from swing to stance.
Functionally analogous systems with strain-sensitive mechanoreceptors on
proximal leg segments have been described for other animal taxa; for example,
in the legs of crustaceans (Leibrock et
al., 1996), arachnids
(Seyfarth, 1978
) and
vertebrates (Conway et al.,
1987
).
The timing of afferents arriving at the CNS after leg contact
A major problem for fast motor responses was described for running
cockroaches by Wilson (1965):
after substrate contact in each step, long conduction times in afferent axons
from tarsal mechanoreceptors would result in very late motor response. In the
locust also, tactile afferents that monitor leg contacts directly arise from
tarsal and/or tibial mechanoreceptors, many of which have many monosynaptic
connections to tarsal depressor motoneurons
(Burrows and Pflüger,
1988
; Burrows,
1996
; Laurent and Hustert,
1988
). We concluded that, generally, mechanoreceptors located
closer to the CNS might be responsible for the earliest arrival of afferents
at the CNS after substrate contact. This requires that these mechanoreceptors
respond to even a slight touch on distal leg segments conducted to them
rapidly via the leg cuticle. An impact-released shock wave travels
longitudinally in the leg and, due to the cuticular material of the leg, its
speed should be 3500 m s-1 (as in wood;
Kusch, 1976
) or faster.
Therefore, we could demonstrate that tarsal contact immediately leads to
altered tensile forces in the proximal leg segments
(Hustert, 1995
;
Fig. 3) and therefore also in
the trochanteral CS, which respond to changing strain on the tarsus from
levels of 1 mN to 5 mN (freshly moulted vs four-week-old adults,
respectively; Wienicke, 1995
).
Their sensory neurons conduct with the fastest known speed of middle leg
mechanoreceptor axons to the CNS, where the first afferent information on
tarsal/tibial impact arrives after about 4 ms. The transfer of strain to
proximal leg cuticle is at least 6 ms faster than the axonal spike transferred
from distal mechanoreceptors in response to the same stimulus. Therefore, the
strain-sensitive proximal CS are the first to report limb contact to CNS
neurons, which in turn can organise the most rapid motor responses.
It is very unlikely that alternative pathways such as via the
subgenual organ in the tibia or other scolopidial organs can send the first
information on vibration or increasing strain caused by leg contact, since
they are located near the middle of the leg and are surrounded by haemolymph
in which `vibratory' shock waves proceed `only' at about 1500 m s-1
(as in water; Kusch, 1976).
Nevertheless, mechanical conduction via cuticle and/or haemolymph
out-racing afferent and interneuron pathways from the area of primary
mechanical contact can occur along the insect body. Such pathways of
mechanical conduction may elicit mechanosensory responses, as described for
sternal and tergal chordotonal organs of the locust abdomen
(Hustert, 1975
) and also the
rapid reflexes from the tip of the cockroach abdomen to thoracic ganglia,
which are faster than reflexes mediated by their giant interneurons
(Pollack et al., 1995
).
Cooperation of mechanoreceptor effects on depressor motoneurons
Convergent reflexes after selective stimulation and recording of two
proprioceptors simultaneously were previously shown to excite thoraco-coxal
rotator (Hustert, 1983) and
femoral (Jellema and Heitler,
1997
) motoneurons.
Afferents from the posterior tibial spurs (rarely from anterior spurs)
affect both the fast and the slow M103d motoneurons of the depressor
trochanteris polysynaptically, indicating that this reflex system can subserve
clasping reflexes with the lower leg segments, which are necessary for holding
the locust on its substrate when landing, walking
(Laurent and Hustert, 1988),
climbing or turning for hiding
(Hassenstein and Hustert,
1999
) on rough terrain, stems, grasses or sticks. In locusts that
climb stems, several spurs of a leg are stimulated at the same time so that
their postsynaptic effects summate reliably (all have nearly the same
conductance time to the CNS) and release efferent spikes at the motoneuron
level.
The observation that anterior spurs of the middle legs do not influence the
trochanter depressor motoneurons is probably due to the fact that they are
normally stimulated in the late stance phase during walking when the release
of the leg from the substrate is pending and when depressor activation would
be antagonistic to the regular walking movements. Nevertheless, the situation
may change when locusts climb up or down a stem
(Hustert, 1985).
We showed that afferents from the groups of CS on the proximal leg segments
activate the slow and fast-depressor trochanteris (M103d) motoneurons
directly. Single femoral CS spikes drive their membrane potential near the
firing threshold for action potentials, which indicates an efficient reflex
coupling from the proximal leg CS. Modulations of this effect could arise from
converging inputs that inhibit the motoneurons and from presynaptic influences
directly on the CS afferents, as indicated by morphological studies
(Watson and England,
1991).
By contrast, in phasmids (Stein and
Schmitz, 1999), trochantero-femoral CS themselves influence other
types of leg mechanoreceptor afferents presynaptically. If that applied also
to locusts, the proximal CS afferents arriving first at the CNS after a leg
impact could diminish the excitatory efficiency of delayed afferents from
distal mechanoreceptors in response to the same stimulus. The proximal CS
afferents themselves, being the first to arrive in the CNS, should evade any
presynaptic effects from other afferents that respond to the same leg contact.
One may speculate that it may be a major advantage of PAD (primary afferent
depolarisation) occurring in leg afferents that they can diminish late
responses by late and less specific mechanosensory afferents during a
movement.
Specificity of responses
For the trCS5 (Hustert,
1985) and feCS2 (similar cap orientation;
Hustert et al., 1981
) on the
posterior face of the middle leg, the optimal stimulus is compression. This
type of strain occurs when the tibia is bent posteriorly after it has rotated
behind the point at which femur and body axis are perpendicular. Locusts often
prefer this range of movement in middle leg stepping
(Burns, 1973
) so the feCS2 and
trCS5 would be active throughout the stance phase. Leg motor coordination
during uphill and downhill walking should be controlled specifically by the
opposing groups of trochanteral CS on the anterior (trCS1) and posterior
(trCS5) face of the middle leg (Hustert,
1985
). The trCS1 was shown to excite the posterior rotator of the
coxa strongly and it contributes to leg retraction at the transition from
swing to stance in wide steps.
By contrast, inhibition of the depressor trochanteris motoneurons arises
from the pair of medial CS of the dorsal tibia (tiCS5;
Fig. 4D), which is comparable
to its homologue in cockroaches (Ridgel et
al., 1999). This reflex is similar to the polysynaptic effects
from the more proximal medial CS group (tiCS3;
Mücke, 1991
) on the tibia
onto the slow extensor tibia motoneuron in the middle leg
(Newland and Emptage,
1996
).
For the fine control of movements by the different afferents converging from a leg, the relative postsynaptic potential amplitudes, temporal coincidence or temporal sequence of their effects at the motoneuron level should be important.
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Acknowledgments |
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