Synaptic responses produced in lobster abdominal postural motor neurons by mechanical stimulation of the swimmeret

1. Intracellular recordings were obtained from the somata of identified abdominal postural motor neurons in lobster to examine their subthreshold and suprathreshold responses to tactile stimulation of the swimmeret. 2. Pressure stimulation of the swimmeret surface evoked abdominal extension by producing tonic spiking in the extensor excitors and the synergistic flexor inhibitor (f5) and hyperpolarizing responses in the extensor inhibitor and antagonistic flexor excitors. These responses often continued for several seconds following the termination of the stimulus. The receptive fields of these motor responses extended over most of the swimmeret surface. 3. More localized tactile stimulation of the swimmeret surface elicited EPSPs in f5 and the extensor excitors, and IPSPs in the flexor excitors. The amplitude of these synaptic potentials decreased as the stimulus intensity was reduced. 4. Stimulation of feathered hair (both sexes) and smooth hair (female only) sensilla produced responses characteristic of extension whereas bristly spines on the male accessory lobe excited only two flexor excitors without affecting any of the other postural motor neurons. 5. Summed synaptic responses recorded from the motor neurons differed in their amplitudes and latencies according to the type of mechanoreceptor stimulated-cuticular receptors, feathered hairs or smooth hairs. Stimulation of the swimmeret cuticle produced the strongest responses (shortest latency, largest amplitude), while feathered hair stimulation initiated the weakest responses (longest latency, smallest amplitude). 6. The relatively long latencies (greater than 35 ms) and the complex form of the EPSPs and IPSPs indicate the involvement of multisynaptic interneuronal pathways in the reflex arcs.     

Sexually dimorphic mechanosensitive swimmeret sensilla affect abdominal posture in the lobster

The sensilla on the male and female second swimmerets are sexually dimorphic. Female swimmerets contain many long "smooth hairs" (long simple setae) on the coxa and rami. The endopodite of the male swimmeret has an accessory lobe covered with short "bristly spines" (serrate setae). In both sexes the swimmeret rami are lined by "feathered hairs" (plumose setae). The influence of mechanosensory stimulation of these sensilla upon abdominal tonic motor activity was analyzed in an in vitro swimmeret-nerve cord preparation. Movement of several clusters of smooth hairs produced an abdominal extension program by exciting the flexor inhibitor f5, inhibiting the flexor excitors, and activating several extensors. Stimulation of the male bristly spines excited the medium-sized flexor excitors f3 and f4. In both sexes the feathered hairs did not generate any response to mechanical stimulation. We infer that in nongravid females the smooth hairs are involved in receiving mechanosensitive cues to support abdominal extension. Bristly spines may contribute to postural adjustments that assist mating. The long latencies of these responses and their propagation to adjacent ganglia suggest that they are mediated by postural interneurons rather than by direct afferent terminations on postural motoneurons.     

Intersegmental modulation of abdominal postural responses initiated by mechanostimulation of the swimmeret in lobster

In a multiganglionic preparation of the lobster abdominal nerve cord, composed of the first through fifth ganglia (A1-A5) and attached second swimmeret, tactile stimulation of the cuticular surface of the swimmeret initiates a postural motor program in A2 for abdominal extension, whereas deflection of feathered hair sensilla that fringe the swimmeret rami does not affect postural motor activity recorded from A2 (Kotak and Page, 1986a). This report demonstrates that partial isolation of A2 from adjacent abdominal ganglia by sectioning the A1-A2 or the A2-A3 connectives both increases the strength of the extension response evoked by cuticular stimulation and disinhibits a postural flexion inhibition response initiated by feathered hair stimulation. Complete isolation of A2, by cutting the A1-A2 and the A2-A3 connectives, further increases the strength of these postural responses. Intersegmental inhibition of these responses originates in the ganglia adjacent to A2, since mechanoresponsiveness of A2 is not affected by resection of a more distant connective (A3-A4). These results provide evidence for the presence in adjacent abdominal ganglia of intersegmental interneurons that regulate the access of swimmeret sensory activity to the postural motor neurons in A2.     

State-dependent responses of two motor systems in the crayfish,Pacifastacus leniusculus

The expression of both swimmeret and postural motor patterns in crayfish (Pacifastacus leniusculus) were affected by stimulation of a second root of a thoracic ganglion. The response of the swimmeret system depended on the state of the postural system. In most cases, the response of the swimmeret system outlasted the stimulus.Stimulation of a thoracic second root also elicited coordinated responses from the postural system, that outlasted the stimulus. In different preparations, either the flexor excitor motor neurones or the extensor excitor motor neurones were excited by this stimulation. In every case, excitation of one set of motor neurones was accompanied by inhibition of that group's functional antagonists.This stimulation seemed to coordinate the activity of both systems; when stimulation inhibited the flexor motor neurones, then the extensor motor neurones and the swimmeret system were excited. When stimulation excited the flexor motor neurones, then the extensor motor neurones and the swimmeret system were inhibited.Two classes of interneurones that responded to stimulation of a thoracic second root were encountered in the first abdominal ganglion. These interneurones could be the pathway that coordinates the response of the postural and swimmeret systems to stimulation of a thoracic second root.Abbreviations TSR thoracic second root - epsp excitatory post-synaptic potential - ipsp inhibitory post-synaptic potential - EJP excitatory jonctional potential - PS power-stroke - RS return-stroke - INT interneurone - N1 first segmental nerve - N2 second segmental nerve - N3 third segmental nerve - A1 abdominal ganglion 1     

Innervation and motor patterns of the abdominal superficial flexor muscles in larval lobsters

The pattern of innervation and motor program of the abdominal superficial flexor muscle was investigated electrophysiologically in larval lobsters (Homarus americanus). The muscle receives both excitatory and inhibitory innervation in the larval as well as in the embryonic stages. Individual muscle fibers receive a single inhibitory neuron (f5) and a maximum of three excitors. Based on spike heights these axons belong to either the small (f1 or f2) or large (f3, f4) motoneurons. While the small axons preferentially innervate the medial muscle fibers the large axons innervate medial as well as lateral fibers. This larval pattern of innervation resembles the pattern in the adult lobster. The resemblance extends to the firing patterns as well with both large and small excitors firing spontaneously. Furthermore, evoked activity in the larvae produces reciprocal (and occasionally cyclical) bursts of excitor and inhibitor neurons denoting abdominal extension and flexion and resembling the firing patterns in adults. Consequently motor programs employed in steering the pelagic larvae are reminiscent of the programs for maintaining posture in the benthic adult lobsters.     

Asynchronous swimmeret beating during defense turns in the crayfish, Procambarus clarkii

Swimmeret beating was monitored in freely moving specimens of the crayfish Procambarus clarkii as they exhibited defense turn responses to tactile stimuli. Analysis of videotape records revealed alterations in swimmeret beating during turning responses compared to straight, forward walking. During turns, swimmerets beat with shorter periods and smaller amplitude power strokes than during straight walking. Coordination between swimmerets also changed. Swimmerets on the side toward which the animal turned tended to lag behind their contralateral partners, rather than beat in synchrony as in straight walking, and ipsilateral coordination was loosened relative to straight walking. Asynchronous swimmeret beating accompanied asymmetric motions of the uropods in a manner similar to that observed during statocyst-dependent equilibrium reactions in P. clarkii, but removal of the statoliths did not eliminate turn-associated responses of the swimmerets. The coordinated action of the swimmerets and uropods may contribute to the torque that rotates the animal in the yaw plane. Implications of the observed changes in swimmeret coordination for understanding the underlying neuronal control system are discussed.     

The abdominal motor system of the crayfish, Cherax destructor. II. Morphology and physiology of the deep extensor motor neurons

Two opposing muscle systems underlie abdominal contractions during escape swimming in crayfish. In this study we used extracellular and intracellular stimulation, recording and dye-filling to systematically identify each of the five deep extensor excitors and single inhibitor of the crayfish, Cherax destructor. Functional associations of each neuron were characterised by recording its responses to sensory and abdominal cord inputs, its extensor muscle innervation pattern, and its relationships with other neurons. Each excitor receives excitatory input from the tonic abdominal stretch receptors and the largest neuron also receives input from the phasic stretch receptor. The two largest excitors innervate the muscle bundle containing the fastest fibres and may be electronically coupled. The smaller neurons may also be electronically coupled and innervate the remaining deep extensor fibres which display dynamic characteristics from fast to medium-fast. The inhibitor does not receive input from the stretch receptors, but is strongly excited by tactile afferents. The implications of these findings for the current models of the control of abdominal tailflips and swimming are discussed. Accepted: 21 June 1998     

Mechanosensory afferents innervating the swimmerets of the lobster

The mechanosensory innervation of the lobster (Homarus americanus) swimmeret was examined by electrophysiologically recording afferent spike responses initiated by localized mechanical stimulation of the caudal surface of the swimmeret. Two functional groups of subcuticular hypodermal mechanoreceptors innervate the swimmeret. Afferents of one group innervate the small discrete "ridges" of calcified cuticle lining the margins of both swimmeret rami. Putative ridge receptors are bipolar sensory neurons responding phasically to deformation of the ridge cuticle with the number and frequency of impulses produced dependent on stimulus strength and velocity. Afferents of the second group, which innervate substantial areas of hypodermis underlying the soft, flexible cuticular regions of the swimmeret, were designated "wide-field" hypodermal mechanoreceptors. These neurons have multiterminal receptive fields and respond phaso-tonically to cuticular distortion. The response properties of both types of hypodermal mechanoreceptors imply that they are activated during the characteristic beating movements of the swimmerets.     

Influence of walking on swimmeret beating in the lobster Homarus gammarus

Influence of walking on swimmeret beating in intact lobsters, Homarus gammarus, has been analyzed using a treadmill experimental device. Belt movement activates both leg stepping and swimmeret beating. The simultaneity of the onset of the two motor systems in this situation is demonstrated to be the result of a startle response initiated when the belt begins to move. This reaction consists of a non-specific motor activity involving several antagonist postural and dynamic muscles. Abdominal extension and vigorous swimmeret beating are the main featurs of this reaction. The main characteristics of the swimmeret beating as defined by Davis (1969) has been observed here in sequences without walking. However during long walking sequences a very different swimmeret beating pattern occurs. It is suggested that this slow swimmeret beating is completely subordinate to the walking rhythm during sequences of absolute coordination. In more rapid swimmeret beating a relative coordination with leg stepping is very common. The functional meaning of this linkage between legs and swimmerets is discussed.     

Transformation of the afferent tactile signal into a motor command in the cat motor cortex

Activity of 112 neurons of the precruciate motor cortex in cats was studied during a forelimb placing reaction to tactile stimulation of its distal parts. The latent period of response of the limb to tactile stimulation was: for flexors of the elbow (biceps brachii) 30–40 msec, for the earliest reponses of cortical motor neurons about 20 msec. The biceps response was observed 5–10 msec after the end of stimulation of the cortex with a series of pulses lasting 25 msec. Two types of excitatory responses of the neurons were identified: responses of sensory type observed to each tactile stimulation of the limb and independent of the presence or absence of motion, and responses of motor type, which developed parallel with the motor response of the limb and were not observed in the absence of motion. The minimal latent period of the responses of motor type was equal to the latent period of the sensory responses to tactile stimulation (20±10 msec). Stimulation of the cortex through the recording microelectrode at the site of derivation of unit activity, which increased during active flexion of the forelimb at the elbow (11 stimuli at intervals of 2.5 msec, current not exceeding 25 µA), in 70% of cases evoked an electrical response in the flexor muscle of the elbow.M. V. Lomonosov Moscow State University. Translated from Neirofiziologiya, Vol. 9, No. 2, pp. 115–123, March–April, 1977.     

Models of learning based on the plastic properties of the "placing reaction" in cats]

A possibility of functional reorganization of initial sensorimotor connections of the forepaw has been shown on seven cats. The main initial relationships between the afferent tactile input and motor output for the ulnar joint of the cat forepaw are as follows: tactile stimulation of the dorsal surface of the paw produces a flexion in the ulnar joint ("placing reaction"), and that of the ventral surface, an extension of the paw in the ulnar joint ("magnetic reflex"); simultaneous tactile stimulation of the ventral surface of the paw blocks the "placing reaction" evoked by a touch of the dorsal side. Extinction was produced of the above unconditioned connections and elaboration of a new "cross" connection consisting in that tactile stimulation of the ventral side of the paw resulted in flexion in the ulnar joint.     

The abdominal motor system of the crayfish, Cherax destructor. I. Morphology and physiology of the superficial extensor motor neurons

Using extracellular and intracellular stimulation, recording and dye-filling, we identified and studied the superficial extensor motor neurons of the crayfish, Cherax destructor. Functional associations of each neuron were characterised by recording its responses to sensory and abdominal cord inputs, its extensor muscle innervation pattern and its relationships with other neurons. Two clear associations were found among the six neurons of each segment. A medium-sized excitor (no. 3), that innervates a substantial percentage of extensor muscle fibres, and the largest excitor (no. 6), recruited during peak, excitation, were inhibited by input from unknown interneurons that excited the common inhibitor (no. 5). Likewise, these excitors received excitatory input when the inhibitor was silent. Another medium-sized neuron (no. 4) that innervates many muscle fibres was co-active with one of the small excitors (no. 2). The two medium-sized neurons were never active at the same time, and these two groupings may be determined by pre-motor interneurons. The implications of these findings for our understanding of motor control in this system are discussed. Accepted: 21 June 1998     

Neural mechanisms governing distribution of cardiac output in an isopod crustacean,Bathynomus doederleini: reflexes controlling the cardioarterial valves

In Bathynomus doederleini all of the cardioarterial valves located at the origin of the lateral arteries are dilated by impulses of lateral cardiac nerves. Tactile stimuli applied to sensillar setae depress impulse activities of the 1st and 5th lateral cardiac nerves. The 1st lateral cardiac nerve controls the valve of the lateral artery which runs to the walking-legs and viscera. The 5th lateral cardiac nerve controls the valve of the lateral artery which runs to the swimmeret muscles. The response indicates that tactile receptor reflexes bring about decreased haemolymph flow to the organs. Augmented swimmeret movements were always accompanied by an increased firing rate in the 5th lateral cardiac nerve. Artificial full protraction of swimmerets simultaneously induced excitation of the 5th lateral cardiac nerve and inhibition of the 1st lateral cardiac nerve. The excitation corresponds to an increase in haemolymph flow to the swimmerets, and the inhibition a decrease in haemolymph flow to walking-legs and viscera. Three kinds of mechanoproprioceptors which were activated by swimmeret movements were found. Two of the mechanoproprioceptors are located at the base of the basipodite. The other mechanoproprioceptor supplies processes to a nerve to the retractor muscles. Activation of three kinds of mechanoproprioceptors, induced by artificial swimmeret protraction, triggered lateral cardiac nerve reflex responses.Abbreviations LA lateral artery - LCN lateral cardiac nerve - RMN nerve to retractor muscles - StR stretch receptor     

Development of the gin trap reflex inManduca sexta: a comparison of larval and pupal motor responses

1. Responses of motor neurons in larvae and pupae of Manduca sexta to stimulation of tactile sensory neurons were measured in both semi-intact, and isolated nerve cord preparations. These motor neurons innervate abdominal intersegmental muscles which are involved in the production of a general flexion reflex in the larva, and the closure reflex of the pupal gin traps. 2. Larval motor neurons respond to stimulation of sensory neurons innervating abdominal mechanosensory hairs with prolonged, tonic excitation ipsilaterally, and either weak excitation or inhibition contralaterally (Figs. 4A, 6). 3. Pupae respond to tactile stimulation of mechanosensory hairs within the gin traps with a rapid closure reflex. Motor neurons which innervate muscles ipsilateral to the stimulus exhibit a large depolarization, high frequency firing, and abrupt termination (Figs. 2, 4B). Generally, contralateral motor neurons fire antiphasically to the ipsilateral motor neurons, producing a characteristic triphasic firing pattern (Figs. 7, 8) which is not seen in the larva. 4. Pupal motor neurons can also respond to sensory stimulation with other types of patterns, including rotational responses (Fig. 3A), gin trap opening reflexes (Fig. 3B), and 'flip-flop' responses (Fig. 9). 5. Pupal motor neurons, like larval motor neurons, do not show oscillatory responses to tonic current injection, nor do motor neurons of either stage appear to interact synaptically with one another. Most pupal motor neurons also exhibit i-V properties similar to those of larval motor neurons (Table 1; Fig. 10). Some pupal motor neurons, however, show a marked non-linear response to depolarizing current injection (Fig. 11).     

Habituation and dishabituation mediated by the peripheral and central neural circuits of the siphon of aplysia

The siphon withdrawal response evoked by a weak tactile (water drop) or light stimulus is mediated primarily by neurons in the siphon. Central neurons (abdominal ganglion) contribute very little since the response amplitude and latency are not changed following removal of the abdominal ganglion. Similarly, habituation and dishabituation of this withdrawal response are not different after removal of the abdominal ganglion, indicating that the peripheral neural circuit in the isolated siphon can mediate habituation itself, and thus has many of the properties attributed to central neurons. Responses evoked by electrical stimulation of the siphon nerve habituate, depending upon the stimulus intensity and interval. These habituated responses may be dishabituated by tactile or light stimulation of the siphon. These results show that each neural system, peripheral and central, has an excitatory modulatory influence on the other. Normally adaptive siphon responses must be shaped by the integrated activity of both of these neural systems.     

Habituation and dishabituation mediated by the peripheral and central neural circuits of the siphon of Aplysia.

The siphon withdrawal response evoked by a weak tactile (water drop) or light stimulus is mediated primarily by neurons in the siphon. Central neurons (abdominal ganglion) contribute very little since the response amplitude and latency are not changed following removal of the abdominal ganglion. Similarly, habituation and dishabituation of this withdrawal response are not different after removal of the abdominal ganglion, indicating that the peripheral neural circuit in the isolated siphon can mediate habituation itself, and thus has many of the properties attributed to central neurons. Response evoked by electrical stimulation of the siphon nerve habituate, depending upon the stimulus intensity and interval. These habituated responses may be dishabituated by tactile or light stimulation of the siphon. These results show that each neural system, peripheral and central, has an excitatory modulatory influence on the other. Normally adaptive siphon responses must be shaped by the integrated activity of both of these neural systems.     

Synaptic interactions among neurons that coordinate swimmeret and abdominal movements in the crayfish

1. Many interneurons in the crayfish (Procambarus clarkii) abdominal nervous system influence two behaviors, abdominal positioning and swimmeret movements. Such neurons are referred to as dual output cells. Other neurons which influence either one behavior or the other are single output cells. 2. Extensive synaptic interactions were observed between both dual and single output neurons involved in the control of abdominal positioning and swimmeret movements. Over 60% of all neuron pairs examined displayed interactions. Pairs of agonist neurons displayed excitatory interactions, while pairs of antagonists had inhibitory interactions. This pattern of interaction was observed in about 75% of interactive neuron pairs whether abdominal positioning or swimmeret outputs were considered. 3. Evidence for both serial and parallel connectivity, as well as, reciprocal or looping connections was observed. Looping connections can be found both between the abdominal positioning and swimmeret systems and within each system. 4. Most (28/34) single output neurons were not presynaptic to dual output neurons. No single output neurons were found to excite dual output neurons to spiking, although inhibitory interactions and weak excitations were observed. 5. Abdominal positioning inhibitors displayed properties consistent with a role in mediating some of the coordination between the swimmeret and abdominal positioning systems. 6. None of the dual output neurons examined influenced the swimmeret motoneurons directly.     

Motor programs for abdominal positioning in crayfish

Summary Using chronically implanted suction electrodes (Fig. 2), records were obtained from the tonic abdominal flexor motor neurons of crayfish while they were undergoing various self-generated movements (Fig. 3). The main behavior examined in this study was one of abdominal extension (Fig. 1), a response which could be evoked repeatedly. Other stereotyped movements were also observed. Each class of behavior we examined has been evoked previously in dissected preparations by stimulating command interneurons, allowing comparison of selfgenerated and electrically evoked motor patterns.During abdominal extension, the flexor inhibitor neuron was observed to fire in a characteristic way (Fig. 4 left, Fig. 5) that was not materially altered even if the associated movements were prevented by rigid restraint (Fig. 4 right). These self-generated motor programs resembled those obtained from command fiber stimulation, both in detail and reproducibility, suggesting that the normal means of executing such stereotyped behavior in these animals is via selected command interneurons.Central reciprocity between the tonic flexor motor neurons and the flexor inhibitor was observed routinely in self-generated programs (Figs. 3, 6, 7), as was seen in dissected animals under command fiber control. The incidence of failure of reciprocity, however, appears to be more common in natural programs than in those evoked by direct stimulation of command interneurons.This work was supported by NIH Grant NS-05423-07 (JLL). Support for one of us (A. C. E.) was obtained in part from NIH Training Grant 2T01 GM-00836-08. We gratefully acknowledge the technical assistance of Mr. Gregg Holmes, and note also the interest and valuable discussions offered by Dr. Lon Wilkens, Mr. George Wolfe and Mr. Terry Page.     

Intersegmental coordination of swimmeret rhythms in isolated nerve cords of crayfish

Summary In crayfish,Pacifastacus leniusculus, abdominal ganglia that can generate the motor pattern normally associated with swimmeret beating continue to do so when the number of connected ganglia is reduced from six to two. The period and phase of the rhythm produced by these shortened chains of ganglia are the same as those produced by the full abdominal nerve cord. These results demonstrate that interactions between any two neighboring ganglia suffice to establish the metachronal phase-lag characteristic of the swimmeret rhythm.Several kinds of interganglionic interneurons that are part of the swimmeret system originate in each abdominal ganglion. These premotor interneurons receive synaptic input in the ganglion of origin and project to other ganglia. Axons from interganglionic neurons also terminate in each ganglion, and some of these terminals receive PSPs from the swimmeret pattern generators in the ganglion where they terminate. Currents injected into these interneurons and axon terminals can reset the swimmeret rhythm. These results demonstrate that premotor interganglionic interneurons exist that have the properties required to coordinate adjacent ganglia. The structures and physiological properties of these interneurons are described and discussed in the context of Stein's model of intersegmental coordination in the swimmeret system.