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Rapid mechano-sensory pathways code leg impact and elicit very rapid reflexes in insects

Markus Höltje and Reinhold Hustert^*

Institut für Zoologie und Anthropologie der Universität Göttingen, Berliner Str. 28, D-37073 Göttingen, Germany

View larger version (34K): [in a new window]   Fig. 1. Features of the depressor trochanteris system. (A) Schematic view of the three main parts of the depressor trochanteris (M103a, M103d and M103b/c) in a cross-section of half of the locust mesothorax. Cx, coxa; Tr, trochanter; Fe, femur; Ti, tibia; Ta, tarsus. (B) Morphology of the fast and slow depressor motoneurons of M103d, viewed in mesothoracic hemiganglia. The nerves are numbered. (C) Simultaneous recordings from the three thoracic nerves that supply the M103 as a whole. Upon stimulation by touching the ventral coxa with a small brush, the motor patterns appear similar, with some tonically active units of small amplitude and bursts of larger amplitude spikes occurring upon stimulation. (D) Intracellular recording of summating excitatory junction potentials (EJPs) in a fibre of M103d resulting from efferent spikes (small amplitudes) recorded from nerve N3C2. (E) Intracellular recordings of EJPs in a fibre of M103d evoked by efferent spikes (lower trace) of the fast-depressor motoneuron (upper trace; large amplitude potentials) recorded at nerve N3C2.

View larger version (35K): [in a new window]   Fig. 2. Afferent conduction times of different mechanoreceptors on the segments of the middle leg of Schistocerca gregaria. Signal averages (64 sweeps) are triggered by the action potential from the vicinity of the soma (upper trace) and afferent in the main leg nerve root at the ganglion (lower trace). (A) Posterior overview of leg segments and location of some of their mechanoreceptors. (B) Averages axonal conduction time of campaniform sensilla (CS) afferents from the posterior trochanteral group (trCS5). (C) Averages axonal conduction time of CS afferents from the posterior femoral group (feCS2). (D) Axonal conduction time of CS afferents from the two distal tibial CS (tiCS5). (E) Comparison of axonal conduction times of tibial spur CS afferents (1–8) from the posterior row of receptors (means ± S.D.; N=5).

View larger version (29K): [in a new window]   Fig. 3. Force transfer from the tarsus to the coxa of a locust middle leg. (A) A piezo-ceramic tongue bends during a 2 ms ramp (and hold) voltage step and indents the tarsus at one pulvillus with a force of 0.1 mN locally. The connected force transducer records the tension (lower trace in the centre) where the stimulus is applied, while the upper transducer, with the coxa glued onto it, records the transferred tensile force (upper trace in the centre; averaged 64x) after a latency of less than 1 ms. Arrows indicate direction of forces. (B) Recording afferents with a suction electrode from nerve stump from the antero-dorsal groups of trochanteral sensilla trCS1–3 while applying an antero-dorsally directed ramp stimulus (arrow) of approximately 0.1 mN to a proximal (posterior) pulvillus. (C) Recording as in B but over a larger time-scale and averaged 64x. The first afferent spikes arise 3 ms after the start of ramp stimulus [arrowheads mark electrical artefacts (art.) from the ramp generator].

View larger version (19K): [in a new window]   Fig. 4. Postsynaptic effects of femoral and tibial campaniform sensilla (CS) on the activity of the motoneurons of muscle M103d. (A) Spikes of a CS (feCS2; lower trace) are followed 1:1 by depolarisations or even spike generation in the fast-depressor motoneuron (upper trace). (B) Averaged data from A: the constant central delay of 2 ms indicates a direct connection. The amplitude of the excitatory postsynaptic potential (EPSP) is approximately 7 mV (signal average of 64 sweeps). (C) Four superimposed sweeps in the slow-depressor motoneuron (upper trace) triggered from a CS afferent (feCS2; recorded at nerve 5bc2). The EPSPs are evoked after a constant central delay of 1.5 ms. (D) Bursts of spikes (large potentials; lower trace) from a CS (tiCS5; recorded in nerve 5B1k) on the dorsal tibia inhibit spike generation in the fast-depressor motoneuron (upper trace).

View larger version (24K): [in a new window]   Fig. 5. Afferents from distal mechanoreceptors causing excitatory postsynaptic potentials (EPSPs) in slow- and fast-depressor motoneurons of muscle M103d. (A) Spikes from a posterior spur afferent evoke EPSPs in the fast-depressor motoneuron. A central latency of 4 ms (mean not shown here) indicates a polysynaptic connection. (B) Tibial hair afferents cause EPSPs in the slow-depressor motoneuron with a central latency of 5 ms, indicating polysynaptic connectivity.

View larger version (18K): [in a new window]   Fig. 6. Responses of the fast-depressor motoneuron of M103d to converging inputs from a femoral (feCS2) campaniform sensillum and a posterior spur afferent. (A) Single feCS2 spikes as well as short bursts of the spur afferent are followed by excitatory postsynaptic potentials (EPSPs) in the motoneuron. When the afferent spikes of both receptors reach the motoneuron at about the same time they are able to elicit spikes. (B) Individual spikes from both types of receptors arising 16 ms apart evoke only EPSPs in the fast-depressor motoneuron. Conductance delays are 2 ms for feCS2 and 12 ms for the spur afferent, and EPSP amplitudes differ. (C) When the spur afferent arises 6 ms before the campaniform sensillum, both effects summate and elicit spikes.