Rhythmic patterns in the thoracic nerve cord of the stick insect induced by pilocarpine

Bath application of the muscarinic agonist pilocarpine onto the deafferented stick insect thoracic nerve cord induced long-lasting rhythmic activity in leg motoneurones. Rhythmicity was induced at concentrations as low as 1x10(-4) mol l-1 pilocarpine. The most stable rhythms were reliably elicited at concentrations from 2x10(-3) mol l-1 to 5x10(-3) mol l-1. Rhythmicity could be completely abolished by application of atropine. The rhythm in antagonistic motoneurone pools of the three proximal leg joints, the subcoxal, the coxo-trochanteral (CT) and the femoro-tibial (FT), was strictly alternating. In the subcoxal motoneurones, the rhythm was characterised by the retractor burst duration being correlated with cycle period, whereas the protractor burst duration was almost independent of it. The cycle periods of the rhythms in the subcoxal and CT motoneurone pools were in a similar range for a given preparation. In contrast, the rhythm exhibited by motoneurones supplying the FT joint often had about half the duration. The pilocarpine-induced rhythm was generated independently in each hemiganglion. There was no strict intersegmental coupling, although the protractor motoneurone pools of the three thoracic ganglia tended to be active in phase. There was no stereotyped cycle-to-cycle coupling in the activities of the motoneurone pools of the subcoxal joint, the CT joint and the FT joint in an isolated mesothoracic ganglion. However, three distinct 'spontaneous, recurrent patterns' (SRPs) of motoneuronal activity were reliably generated. Within each pattern, there was strong coupling of the activity of the motoneurone pools. The SRPs resembled the motor output during step-phase transitions in walking: for example, the most often generated SRP (SRP1) was exclusively exhibited coincident with a burst of the fast depressor trochanteris motoneurone. During this burst, there was a switch from subcoxal protractor to retractor activity after a constant latency. The activity of the FT joint extensor motoneurones was strongly decreased during SRP1. SRP1 thus qualitatively resembled the motoneuronal activity during the transition from swing to stance of the middle legs in forward walking. Hence, we refer to SRPs as 'fictive step-phase transitions'. In intact, restrained animals, application of pilocarpine also induced alternating activity in antagonistic motoneurone pools supplying the proximal leg joints. However, there were marked differences from the deafferented preparation. For example, SRP1 was not generated in the latter situation. However, if the ipsilateral main leg nerve was cut, SRP1s reliably occurred. Our results on the rhythmicity in leg motoneurone pools of deafferented preparations demonstrate central coupling in the activity of the leg motoneurones that might be incorporated into the generation of locomotion in vivo.

[1]  Nervous rhythm arising from rivalry of antagonistic reflexes: Reflex stepping as outcome of double reciprocal innervation , 1913 .

[2]  E. Holst.  Die relative Koordination , 1939 .

[3]  Donald M. Wilson.  The Central Nervous Control of Flight in a Locust , 1961 .

[4]  C. Wiersma,et al.  AUTOGENIC RHYTHMICITY IN THE ABDOMINAL GANGLIA OF THE CRAYFISH: THE CONTROL OF SWIMMERET MOVEMENTS. , 1964, Comparative biochemistry and physiology.

[5]  G. S. Watson,et al.  Statistical methods for the analysis of problems in animal orientation and certain biological rhythms , 1966 .

[6]  K G Pearson,et al.  Properties of action potentials from insect motor nerve fibres. , 1970, The Journal of experimental biology.

[7]  A. Selverston,et al.  The stomatogastric nervous system: Structure and function of a small neural network , 1976, Progress in Neurobiology.

[8]  F. Delcomyn.  Neural basis of rhythmic behavior in animals. , 1980, Science.

[9]  G. Wendler,et al.  Motor output to the protractor and retractor coxae muscles in stick insects walking on a treadwheel , 1981 .

[10]  U. Bässler,et al.  EFFECTS OF AFFERENCE SIGN REVERSAL ON MOTOR ACTIVITY IN WALKING STICK INSECTS (CARAUSIUS MOROSUS) , 1981 .

[11]  D. Graham,et al.  Behaviour and Motor Output of Stick Insects Walking on a Slippery Surface: I. Forward Walking , 1983 .

[12]  U. Bässler,et al.  Motor Output of the Denervated Thoracic Ventral Nerve Cord in the Stick Insect Carausius Morosus , 1983 .

[13]  J. Dean,et al.  Stick Insect Locomotion on a Walking Wheel: Interleg Coordination of Leg Position , 1983 .

[14]  W. Kristan,et al.  Neurons controlling the initiation, generation and modulation of leech swimming. , 1983, Symposia of the Society for Experimental Biology.

[15]  S. Grillner,et al.  The effect of dorsal root transection on the efferent motor pattern in the cat's hindlimb during locomotion. , 1984, Acta physiologica Scandinavica.

[16]  J. Dean,et al.  Stick Insect Locomotion on a Wheel: Patterns Of Stopping And Starting , 1984 .

[17]  D. Graham,et al.  A preparation of the stick insect Carausius morosus for recording intracellularly from identified neurones during walking , 1984 .

[18]  S. Grillner.  Neurobiological bases of rhythmic motor acts in vertebrates. , 1985, Science.

[19]  K. Pearson,et al.  Neural circuits in the flight system of the locust. , 1985, Journal of neurophysiology.

[20]  D. Graham,et al.  Behaviour and Motor Output for an Insect Walking on a Slippery Surface: II. Backward Walking , 1985 .

[21]  D. Graham.  Pattern and Control of Walking in Insects , 1985 .

[22]  K. G. Pearson,et al.  Are there Central Pattern Generators for Walking and Flight in Insects , 1985 .

[23]  K. Pearson,et al.  Intracellular recordings from interneurones and motoneurones during bilateral kicks in the locust: implications for mechanisms controlling the jump , 1986 .

[24]  A. Chrachri,et al.  Induction of rhythmic activity in motoneurons of crayfish thoracic ganglia by cholinergic agonists , 1987, Neuroscience Letters.

[25]  D. Sattelle,et al.  Molecular properties and functions of insect acetylcholine receptors , 1987 .

[26]  J. Schmitz,et al.  THE TREADING-ON-TARSUS REFLEX IN STICK INSECTS: PHASE-DEPENDENCE AND MODIFICATIONS OF THE MOTOR OUTPUT DURING WALKING , 1989 .

[27]  Recording from visible neurone somata in the desheathed metathoracic ganglion of the plasmid Extatosoma tiaratum , 1989 .

[28]  P A Getting,et al.  Emerging principles governing the operation of neural networks. , 1989, Annual review of neuroscience.

[29]  A. Büschges.  Processing of sensory input from the femoral chordotonal organ by spiking interneurones of stick insects , 1989 .

[30]  A. Chrachri,et al.  Fictive locomotion in the fourth thoracic ganglion of the crayfish, Procambarus clarkii , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[31]  H. Cruse.  What mechanisms coordinate leg movement in walking arthropods? , 1990, Trends in Neurosciences.

[32]  A. Büschges.  Nonspiking pathways in a joint-control loop of the stick insect Carausius morosus. , 1990 .

[33]  J. Dean.  Effect of load on leg movement and step coordination of the stick insect Carausius morosus , 1991 .

[34]  J. Schmitz,et al.  Intracellular recordings from nonspiking interneurons in a semiintact, tethered walking insect. , 1991, Journal of neurobiology.

[35]  R. Pitman,et al.  Characterization of receptors mediating the actions of dopamine on an identified inhibitory motoneurone of the cockroach. , 1991, The Journal of experimental biology.

[36]  A. Selverston,et al.  Mechanisms of gastric rhythm generation in the isolated stomatogastric ganglion of spiny lobsters: bursting pacemaker potentials, synaptic interactions, and muscarinic modulation. , 1992, Journal of neurophysiology.

[37]  S. Ryckebusch,et al.  Rhythmic patterns evoked in locust leg motor neurons by the muscarinic agonist pilocarpine. , 1993, Journal of neurophysiology.

[38]  J. Schmitz.  LOAD-COMPENSATING REACTIONS IN THE PROXIMAL LEG JOINTS OF STICK INSECTS DURING STANDING AND WALKING , 1993 .

[39]  H. Cruse,et al.  CONTROL OF BODY HEIGHT IN A STICK INSECT WALKING ON A TREADWHEEL , 1993 .

[40]  M. Burrows,et al.  Distribution of acetylcholine receptors in the central nervous system of adult locusts , 1993, The Journal of comparative neurology.

[41]  G Laurent,et al.  Rhythmic modulation of the responsiveness of locust sensory local interneurons by walking pattern generating networks. , 1994, Journal of neurophysiology.