Octopamine modulates the responses and presynaptic inhibition of proprioceptive sensory neurones in the locust Schistocerca gregaria

1997 ◽  
Vol 200 (9) ◽  
pp. 1317-1325 ◽  
Author(s):  
T Matheson

A multineuronal proprioceptor, the femoral chordotonal organ (feCO), monitors the position and movements of the tibia of an insect leg. Superfusing the locust metathoracic feCO with the neuromodulator octopamine, or the octopamine agonist synephrine, affects the position (tonic) component of the organ's response, but not the movement (phasic) component. Both octopamine and synephrine act with the same threshold (10(-6) mol l-1). Individual sensory neurones that respond tonically at flexed tibial angles show increased tonic spike activity following application of octopamine, but those that respond at extended angles do not. Tonic spiking of phaso-tonic flexion-sensitive neurones is enhanced but their phasic spiking is unaffected. Bath application of octopamine to the feCO increases the tonic component of presynaptic inhibition recorded in the sensory terminals, but not the phasic component. This inhibition should at least partially counteract the increased sensory spiking and reduce its effect on postsynaptic targets such as motor neurones. Furthermore, some phasic sensory neurones whose spiking is not affected by octopamine nevertheless show enhanced tonic synaptic inputs. The chordotonal organ is not known to be under direct efferent control, but its output is modified by octopamine acting on its sensory neurones to alter their responsiveness to mechanical stimuli and by presynaptic inhibition acting on their central branches. The effects of this neuromodulator acting peripherally on sensory neurones are therefore further complicated by indirect interactions between the sensory neurones within the central nervous system. Increases of sensory neurone spiking caused by neuromodulators may not necessarily lead to parallel increases in the responses of postsynaptic target neurones.

1995 ◽  
Vol 198 (7) ◽  
pp. 1589-1601 ◽  
Author(s):  
F Kuenzi ◽  
M Burrows

The hair plate proprioceptors at the thoraco-coxal joint of insect limbs provide information about the movements of the most basal joint of the legs. The ventral coxal hair plate of a middle leg consists of group of 10-15 long hairs (70 microns) and 20-30 short hairs (30 microns). The long hairs are deflected by the trochantin as the leg is swung forward during the swing phase of walking, and their sensory neurones respond phasically during an imposed deflection and tonically if the deflection is maintained. Selective stimulation of the long hairs elicits a resistance reflex that rotates the coxa posteriorly and is similar to that occurring at the transition from the swing to the stance phase of walking. The motor neurones innervating the posterior rotator and adductor coxae muscles are excited, and those to the antagonistic anterior rotator muscle are inhibited. By contrast, selective stimulation of the short hairs leads only to a weak inhibition of the anterior rotator. The excitatory effects of the long hairs are mediated, in part, by direct connections between their sensory neurones and particular motor neurones. A spike in a sensory neurone elicits a short-latency depolarising postsynaptic potential (PSP) in posterior rotator and adductor motor neurones whose amplitude is enhanced by hyperpolarising current injected into the motor neurone. When the calcium in the saline is replaced with magnesium, the amplitude of the PSP is reduced gradually, and not abruptly as would be expected if an interneurone were interposed in the pathway. Several sensory neurones from long hairs converge to excite an individual motor neurone, evoking spikes in some motor neurones. The projections of the sensory neurones overlap with some of the branches of the motor neurones in the lateral association centre of the neuropile. It is suggested that these pathways would limit the extent of the swing phase of walking and contribute to the switch to the stance phase in a negative feedback loop that relieves the excitation of the hairs by rotating the coxa backwards.


Three types of sensory neurones and two kinds of motor neurones in the segmental ganglion of the leech were examined with the light and electron microscope after intracellular injection of horseradish peroxidase (HRP) for a histological marker. The aim was to develop a method for identifying the synapses of specific cells in the ganglion’s complex neuropil and to form a picture of their distribution and structure. Reaction of HRP with different benzidine derivatives produces opaque and electron dense deposits. For light microscopy a blue stain is formed that makes processes visible in whole mounts millimeters away from the injection site at the soma. The reaction product for electron microscopy is distributed throughout the cytoplasm, yet ultrastructural details are preserved. The sensory neurones that respond specifically to touch or pressure or noxious mechanical stimuli to the skin share in their branching pattern a number of common features. A single process arising from each cell body forms large primary branches that pass through the neuropil and leave the ganglion by the ipsilateral connectives and roots. Within the neuropil these branches give rise to numerous smaller secondary processes. In contrast, the annulus erector and large longitudinal motoneurones send their main process across the ganglion to bifurcate and enter the contralateral roots. Secondary processes of the motoneurones are highly branched and more numerous than those of the sensory cells. Each type of sensory and motor cell is distinguished by the shape, length and distribution of its secondary processes. Secondary processes of sensory neurones exhibit numerous swellings and irregularly shaped fingers. Electron micrographs show that the sensory neurones make synapses at these specializations, each of which contacts several postsynaptic processes. The sensory neurones receive inputs at the same fingers and swellings, an arrangement suggesting that regions within a cell’s arborization may function semi-autonomously. The main process and large branches of the two motor neurones are studded with spines a few micrometres long and a fraction of a micrometre in diameter. Vesicle-containing varicosities from other cells make synaptic contact primarily with the spines, which themselves have few vesicles. These two motor neurones are largely, if not entirely, postsynaptic to other neurones within the leech nervous system.


1995 ◽  
Vol 198 (11) ◽  
pp. 2397-2404 ◽  
Author(s):  
P L Newland ◽  
B Watkins ◽  
N J Emptage ◽  
T Nagayama

A hair plate is present on the proximal anterior face of the pro- and mesothoracic tibiae of the legs of the locust Schistocerca gregaria, but not on the metathoracic legs. The hair plate is in a depression of the cuticle and contains about 11 hairs, which are all polarised with their tips pointing towards the dorsal surface of the tibia. The hairs are all of the same trichoid sensilla type and vary in length from 90 to 140 microns. Associated with the hair plate is a pronounced distal extension of the anterior femoral coverplate, the inner face of which is concave, that makes contact with the hairs during flexion and extension movements of the tibia. During postembryonic development, no tibial hair plate hairs are present in the first four larval stages. In fifth-instar larvae just three hairs are present, while the full complement is attained only after the final moult to adulthood. The distal extension of the posterior coverplate is present through all instar stages, becoming more pronounced after each moult. Sensory neurones innervating the hairs of an adult may be divided into two classes on the basis of their responses. The first type responds phasically to imposed deflections and is velocity-sensitive. The second type responds phasotonically and is also sensitive to the velocity of the stimulus but has an additional tonic component sensitive to maintained angular deflections. Both types of afferents are directionally sensitive and respond best to deflections against the natural bend of the hair, equivalent to extension movements of the tibia.(ABSTRACT TRUNCATED AT 250 WORDS)


1996 ◽  
Vol 199 (3) ◽  
pp. 613-625
Author(s):  
T Jellema ◽  
W Heitler

The metathoracic fast extensor tibiae (FETi) motor neurone of locusts is unusual amongst insect motor neurones because it makes output connections within the central nervous system as well as in the periphery. It makes excitatory chemical synaptic connections to most if not all of the antagonist flexor tibiae motor neurones. The gain of the FETi-flexor connection is dependent on the peripheral conditions at the time of the FETi spike. This dependency has two aspects. First, sensory input resulting from the extensor muscle contraction can sum with the central excitatory postsynaptic potential (EPSP) to augment its falling phase if the tibia is restrained in the flexed position (initiating a tension-dependent reflex) or is free to extend (initiating a movement-dependent resistance reflex). This effect is thus due to simple postsynaptic summation of the central EPSP with peripheral sensory input. Second, the static tibial position at the time of the FETi spike can change the amplitude of the central EPSP, in the absence of any extensor muscle contraction. The EPSP can be up to 30 % greater in amplitude if FETi spikes with the tibia held flexed rather than extended. The primary sense organ mediating this effect is the femoral chordotonal organ. Evidence is presented suggesting that the mechanism underlying this change in gain may be specifically localised to the FETi-flexor connection, rather than being due to general position-dependent sensory feedback summing with the EPSP. The change in the amplitude of the central EPSP is probably not caused by general postsynaptic summation with tonic sensory input, since a diminution in the amplitude of the central EPSP caused by tibial extension is often accompanied by overall tonic excitation of the flexor motor neurone. Small but significant changes in the peak amplitude of the FETi spike have a positive correlation with changes in the EPSP amplitude, suggesting a likely presynaptic component to the mechanism of gain control. The change in amplitude of the EPSP can alter its effectiveness in producing flexor motor output and, thus, has functional significance. The change serves to augment the effectiveness of the FETi-flexor connection when the tibia is fully flexed, and thus to increase its adaptive advantage during the co-contraction preceding a jump or kick, and to reduce the effectiveness of the connection when the tibia is partially or fully extended, and thus to reduce its potentially maladaptive consequences during voluntary extension movements such as thrusting.


1999 ◽  
Vol 202 (16) ◽  
pp. 2151-2159 ◽  
Author(s):  
T. Friedel

Substratum vibrations elicit a fast startle response in unrestrained quiescent desert locusts (Schistocerca gregaria). The response is graded with stimulus intensity and consists of a small, rapid but conspicuous movement of the legs and body, but it does not result in any positional change of the animal. With stimuli just above threshold, it begins with a fast twitch of the hindlegs generated by movements of the coxa-trochanter and femur-tibia joints. With increasing stimulus intensity, a rapid movement of all legs may follow, resulting in an up-down movement of the whole body. The magnitude of both the hindleg movement and electromyographic recordings from hindleg extensor and flexor tibiae muscles increases with stimulus amplitude and reaches a plateau at vibration accelerations above 20 m s(−)(2) (peak-to-peak). Hindleg extensor and flexor tibiae muscles in unrestrained animals are co-activated with a mean latency of 30 ms. Behavioural thresholds are as low as 0. 47 m s(−)(2) (peak-to-peak) at frequencies below 100 Hz but rise steeply above 200 Hz. The response habituates rapidly, and inter-stimulus intervals of 2 min or more are necessary to evoke maximal reactions. Intracellular recordings in fixed (upside-down) locusts also revealed co-activation of both flexor and extensor motor neurones with latencies of approximately 25 ms. This shows that the neuronal network underlying the startle movement is functional in a restrained preparation and can therefore be studied in great detail at the level of identified neurones.


1995 ◽  
Vol 73 (3) ◽  
pp. 923-932 ◽  
Author(s):  
D. Parker

1. The effects of the putative endogenous neuromodulator serotonin (5-HT) on the fast extensor and flexor tibiae motor neurons in the locust (Schistocerca gregaria) metathoracic ganglion, were analyzed. 2. 5-HT consistently increased the duration of the fast extensor spike and usually reduced the afterhyperpolarization, although this effect was less consistent. The spike broadening in the fast extensor was associated with an increase in the amplitude of the excitatory postsynaptic potential (EPSP) evoked monosynaptically in the flexor motor neurons by fast extensor stimulation. 5-HT also increased the membrane resistance of the fast extensor and flexor tibiae motor neurons. 3. The effects of 5-HT were mimicked by bath application of the 5-HT uptake inhibitor imipramine, and blocked by the 5-HT receptor antagonist ketanserin. The effects were also mimicked by dibutryl cyclic AMP, a membrane permeant analogue of cyclic AMP, and by the phosphodiesterase inhibitor 3-isobutyl-1-methyl-xanthine, but not by dibutryl cyclic GMP. The 5-HT-dependent modulation was blocked by the protein kinase A inhibitor H8. In addition, injection of cyclic AMP into the fast extensor or a flexor motor neuron could mimic the effects of 5-HT on these neurons. 4. 5-HT probably broadened the FETi action potential by modulating potassium conductances responsible for spike repolarization. 5. These results show that 5-HT modulates both the fast extensor and flexor tibiae motor neurons, resulting in potentiation of synaptic transmission between these neurons. In addition, the increase in flexor membrane resistance will potentiate other inputs onto these cells, which will affect the output of the motor neurons during locomotion.


2005 ◽  
Vol 93 (2) ◽  
pp. 980-988 ◽  
Author(s):  
Eric J. Schwartz ◽  
Tatyana Gerachshenko ◽  
Simon Alford

Locomotor pattern generation is maintained by integration of the intrinsic properties of spinal central pattern generator (CPG) neurons in conjunction with synaptic activity of the neural network. In the lamprey, the spinal locomotor CPG is modulated by 5-HT. On a cellular level, 5-HT presynaptically inhibits synaptic transmission and postsynaptically inhibits a Ca2+-activated K+ current responsible for the slow afterhyperpolarization (sAHP) that follows action potentials in ventral horn neurons. To understand the contribution of these cellular mechanisms to the modulation of the spinal CPG, we have tested the effect of selective 5-HT analogues against fictive locomotion initiated by bath application of N-methyl-d-aspartate (NMDA). We found that the 5-HT1D agonist, L694-247, dramatically prolongs the frequency of ventral root bursting. Furthermore, we show that L694-247 presynaptically inhibits synaptic transmission without altering postsynaptic Ca2+ -activated K+ currents. We also confirm that 5-HT inhibits synaptic transmission at concentrations that modulate locomotion. To examine the mechanism by which selective presynaptic inhibition modulates the frequency of fictive locomotion, we performed voltage- and current-clamp recordings of CPG neurons during locomotion. Our results show that 5-HT decreases glutamatergic synaptic drive within the locomotor CPG during fictive locomotion. Thus we conclude that presynaptic inhibition of neurotransmitter release contributes to 5-HT–mediated modulation of locomotor activity.


1994 ◽  
Vol 187 (1) ◽  
pp. 305-313
Author(s):  
P Skorupski ◽  
P Vescovi ◽  
B Bush

It is now well established that in arthropods movement-related feedback may produce positive, as well as negative, feedback reflexes (Bassler, 1976; DiCaprio and Clarac, 1981; Skorupski and Sillar, 1986; Skorupski et al. 1992; Vedel, 1980; Zill, 1985). Usually the same motor neurones are involved in both negative feedback (resistance) reflex responses and positive feedback reflexes. Reflex reversal involves a shift in the pattern of central inputs to a motor neurone, for example from excitation to inhibition. In the crayfish, central modulation of reflexes has been described in some detail for two basal limb proprioceptors, the thoracocoxal muscle receptor organ (TCMRO) and the thoracocoxal chordotonal organ (TCCO) (Skorupski et al. 1992; Skorupski and Bush, 1992). Leg promotor motor neurones are excited by stretch of the TCMRO (which, in vivo, occurs on leg remotion) in a negative feedback reflex, but when this reflex reverses they are inhibited by the same stimulus. Release of the TCCO (which corresponds to leg promotion) excites some, but not all, promotor motor neurones in a positive feedback reflex. There are at least two ways in which the reflex control of a muscle may be modulated in this system. Firstly, inputs to motor neurones may be routed via alternative reflex pathways to produce different reflex outputs. Secondly, the pattern of inputs to a motor pool may be inhomogeneous, so that activation of different subgroups of the motor pool causes different outputs. Different crayfish promotor motor neurones are involved in different reflexes. On this basis, the motor neurones may be classified into at least two subgroups: those that are excited by the TCCO in a positive feedback reflex (group 1) and those that are not (group 2). Do these motor neurone subgroups have different effects on the promotor muscle, or is the output of the two promotor subgroups summed at the neuromuscular level? To address this question we recorded from the promotor nerve and muscle in a semi-intact preparation of the crayfish, Pacifastacus leniusculus. Adult male and female crayfish, 8-11 cm rostrum to tail, were decapitated and the tail, carapace and viscera removed. The sternal artery was cannulated and perfused with oxygenated crayfish saline, as described previously (Sillar and Skorupski, 1986).


1992 ◽  
Vol 163 (1) ◽  
pp. 345-358 ◽  
Author(s):  
P. M.J. SHELTON ◽  
R. O. STEPHEN ◽  
J. J.A. SCOTT ◽  
A. R. TINDALL

The mechanical connections of the metathoracic femoral chordotonal organ (mtFCO) with its insertion at the femoro-tibial joint are described. The apodeme complex is shown to consist of a distal cuticular rod that is replaced proximally by dorsal and ventral ligaments. The dorsal ligament is a direct continuation of the distal rod but proximally it is replaced by ligamentous cells. The ventral ligament has no cuticular core and consists of ligamentous cells throughout its length. The ligaments are composed of bundles of connective tissue cells that are each enclosed in an extracellular matrix containing acid-fuchsin-staining fibrils. Internally the cells are packed with microtubules. During extension and flexion of the joint, the two ligaments move differentially. During passive extension of the tibia, the ventral ligament remains taut but the dorsal one buckles to form a slack loop. Direct observation of living preparations shows that the loop is first detectable during extension of the tibia at joint angles greater than about 51°. During flexion, the loop gradually tightens and disappears. It has completely disappeared at joint angles of less than about 36°. Changes in loop shape were demonstrable using preparations in which the tibia was moved sinusoidally ±10° about a mean femoro-tibial angle of 90° and photographs were taken using phase-locked illumination. Other details of the apodeme complex are described and the significance of the findings is discussed in relation to mtFCO function.


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