scholarly journals Central Synaptic Coupling of Walking Leg Motor Neurones in the Crayfish: Implications for Sensorimotor Integration

1988 ◽  
Vol 140 (1) ◽  
pp. 355-379
Author(s):  
PETER SKORUPSKI ◽  
KEITH T. SILLAR

We present electrophysiological evidence for the presence of central output synapses on crayfish walking leg motor neurones. The effect of these central outputs is that a motor neurone can exert tonic graded control over other motor neurones without the requirement for spiking. Excitatory interactions among synergists and inhibitory interactions among antagonists are described. This central coupling among leg motor neurones profoundly affects their responses to afferent input from an identified stretch receptor, the thoracocoxal muscle receptor organ (TCMRO). Injecting current into a motor neurone can change the gain of TCMRO reflexes in other motor neurones. Some motor neurones are also capable of reversing the sign of TCMRO reflexes by inhibiting reflex firing of antagonists and facilitating reflex activity in synergists. The implications of these central interactions of motor neurones in motor control are discussed.

1999 ◽  
Vol 202 (2) ◽  
pp. 183-191 ◽  
Author(s):  
B.J. Mccarthy ◽  
D.L. Macmillan

The activity of the superficial extensor motor neurones was recorded during slow abdominal extension in the crayfish Cherax destructor. Postural extensions were evoked by lowering a platform from beneath the suspended crayfish. During extensions where the abdomen was physically blocked from achieving full extension, the largest superficial extensor motor neurone (SEMN6) fired at a higher rate than during unhindered extensions. Blocking a segment neighbouring that being examined also increased SEMN6 activity, demonstrating an intersegmental spread of the reflex. The increase in SEMN6 firing rate occurred in the absence of activity in the sensory neurone of the tonic muscle receptor organ, demonstrating that the tonic sensory neurone is not necessary for load compensation during these abdominal extensions in C. destructor. The findings support earlier evidence suggesting that other receptor systems can mediate load compensation in the abdomen of the crayfish.


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).


1975 ◽  
Vol 62 (1) ◽  
pp. 99-114
Author(s):  
CM Ballintijn ◽  
OS Bamford

The response of single respiratory neurones in the medulla oblongata of carp to short twitches of individual respiratory muscles were analysed. The muscle contractions were obtained through automatic electrical stimulation and could be consistently elicited in a predetermined phase relation to the ventilatory cycle. The results show that, apart from nerve cells which take part in long-term processing of proprioceptive information from several sources, neurones also exist which possess the properties of elements of a peripheral proprioceptive control loop such as tension receptor neurones, length or stretch receptor neurones and motor neurones.


1986 ◽  
Vol 126 (1) ◽  
pp. 445-452
Author(s):  
KEITH T. SILLAR ◽  
ROBERT C. ELSON

Intracellular recordings have been made from walking-leg motor neurones of the crayfish, Pacifastacus leniusculus, in isolated preparations of the thoracic ganglia. Some motor neurones display slow depolarizations that can drive bursts of spikes and resemble ‘plateau’ potentials described in other invertebrate and vertebrate neurones. Evidence is presented which suggests that the potentials are regenerative and endogenous to the motor neurones, and are not the result of feedback from a neural network. These potentials can be induced by synaptic inputs from the non-spiking afferent neurones of the thoracic-coxal muscle receptor organ, a basal limb proprioceptor. Reflex input from this receptor is augmented during the active depolarization of the motor neurone. The results are discussed in terms of the control of rhythmic motor output and the central modulation of reflexes in the crayfish's thoracic nervous system.


1999 ◽  
Vol 202 (2) ◽  
pp. 171-181 ◽  
Author(s):  
B.J. Mccarthy ◽  
D.L. Macmillan

Electrical recordings were made from the sensory neurone of the tonic muscle receptor organ in the abdomen of the intact, freely behaving crayfish Cherax destructor. Slow extensions of the abdomen were evoked by lowering a platform from beneath the suspended crayfish, and the movements and tonic sensory neurone activity were video-recorded simultaneously. The recordings showed that the tonic sensory neurone was active when the abdomen was fully flexed prior to the extension. When the extension began, however, the sensory neurone ceased firing shortly after movement was detected, irrespective of the load applied to the abdomen. When the abdomen was physically blocked from extending fully, the sensory neurone did not fire. The tonic muscle receptor organ is considered to be the length-detecting sensor for a load-compensating servo-loop, but the results demonstrate that its activity pattern during extensions evoked by a platform-drop in C. destructor are not consistent with that role.


1968 ◽  
Vol 48 (2) ◽  
pp. 389-404
Author(s):  
JOAN JOHNSTON KENDIG

1. Techniques are described for recording in locust thoracic ganglia from single units identifiable as the motor neurones of specific flight muscles. 2. There are at least two kinds of excitatory interactions among flight-muscle motor neurones. A spike in one motor neurone may be electrically transmitted to another with little delay but much attenuation. Stimulation of a group of motor neurones produces a second, probably chemically transmitted, potential with a latency of 5-6 msec. 3. No short-term inhibitory interactions between motor neurones were observed. 4. Activity in one motor unit of the flight system has long-term effects on the motor neurones of other units, excitatory in some cases and inhibitory in others. 5. Single impulses in sensory neurones have little effect on motor neurones; sustained sensory input to a motor neurone produces a slow depolarization and increase in impulse frequency. 6. Antidromic impulses in one group of motor neurones can entrain orthodromic impulses in another motor neurone. 7. These data are discussed with reference to the hypothesis that the pattern of locust flight--rhythmic synchronous bursts of synergist activity, strict alternation between antagonists--can be produced by motor neurone interactions alone.


1983 ◽  
Vol 218 (1210) ◽  
pp. 95-110 ◽  

(i) Following previous work on the morphological and physiological properties of the two distal joints (J2, J3) of the atenna of the rock lobster Palinurus vulgaris , the mechanical, muscular and proprioceptive organization of the two proximal joints between the antennal segments S1 and S2 (J1) and between S1 and the cephalothorax (J0) have now been studied. (ii) Articulated by two classical condyles, J1 moves in a mediolateral plane. One external rotator muscle (ER) and three internal rotator muscles (IR1, IR2, IR3) subserve its movements. J0 is articulated by two different systems: a classical ventrolateral condyle and a complex sliding system constituted by special cuticular structures on the dorsomedial side of the S1 segment and on the rostrum between the two antennae. J0 moves in the dorsoventral plane by means of a levator muscle (Lm) and a depressor muscle (Dm). A third muscle, the lateral tractor muscle (LTm), associated with J0 and lying obliquely across S1, may modulate the level of friction between the S1 segment and the rostrum. (iii) Proprioception in J1 is achieved by a muscle receptor organ AMCO-J1 (antennal myochordotonal organ for the J1 joint) associating a small accessory muscle (S1.am) located in the proximal part of the S1 segment and a chordotonal organ inserted proximally on the S1.am muscle and distally on the S2 segment. J0 proprioception is ensured by a simple chordotonal organ (CO-J0) located in the anterior part of the cephalothorax. (iv) The S1.am muscle is innervated by three motoneurons characterized by their very small diameters and inducing respectively tonic excitatory postsynaptic potentials, phasic excitatory postsynaptic potentials and inhibitory postsynaptic potentials. Anatomical and physiological observations suggest functional correlation between S1.am and IR1 motor innervation. (v) Mechanical and muscular organization of J0 and J1 are compared with that of the other joints of the antenna. The properties of the AMCO-J1 proprioceptor are discussed in relation to the other muscle receptor organs described in crustaceans.


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.


1982 ◽  
Vol 96 (1) ◽  
pp. 325-341
Author(s):  
MALCOLM BURROWS

Simultaneous intracellular recordings have been made from the two expiratory, and from the two inspiratory motor neurones which have their axons in the unpaired median nerves of the thoracic ganglia. Each motor neurone has an axon that branches to innervate muscles on the left and on the right side of one segment. The expiratory neurones studied were those in the meso- and meta-thoracic ganglia which innervate spiracular closer muscles. The depolarizing synaptic potentials underlying the spikes during expiration are common to the two closer motor neurones in a particular segment. Similarly, during inspiration when there are usually no spikes, the hyperpolarizing, inhibitory potentials are also common to both motor neurones. The synaptic input to the neurones can be derived from four interneurones; two responsible for the depolarizing potentials during expiration and two for the inhibitory potentials during inspiration. The inspiratory neurones studied were those in the abdominal ganglia fused to the metathoracic ganglion which innervate dorso-ventral abdominal muscles. During inspiration the two motor neurones of one segment spike at a similar and steady frequency. The underlying synaptic input to the two is common. During expiration, when there are usually no spikes, the hyperpolarizing synaptic potentials are also common to both neurones. In addition they match exactly the depolarizing potentials occurring at the same time in the closer motor neurones. The same set of interneurones could be responsible. No evidence has been revealed to indicate that the two closer, or the two inspiratory motor neurones of one segment are directly coupled by electrical or chemical synapses. The morphology of both types of motor neurone is distinct from that of other motor neurones in these ganglia. Both types branch extensively in both the left and in the right areas of the neuropile.


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