Synaptic drive contributing to rhythmic activation of motoneurons in the deafferented stick insect walking system

A general feature of motor patterns for locomotion is their cyclic and alternating organization. In walking, for example, rhythmic activity in leg motoneurons innervating antagonistic muscles of a joint is primarily antiphasic within each cycle. We investigate which role central pattern generating networks play in the generation of leg motoneuron activity in the absence of sensory feedback. We elicited activity in antagonistic flexor and extensor tibiae motoneurons in the deafferented mesothoracic ganglion of the stick insect by mechanically stimulating the head or abdomen, while recording intracellularly from their neuropilar processes. In most cases, tactile stimulation induced coactivation of tibial motoneurons. However, in ≈ 25% of the trials, tibial motoneurons generated alternating cycles consisting of bursts of action potentials that were terminated by strong inhibitory synaptic inputs. Injection of depolarizing current increased the amplitude of the inhibitory phase of the oscillation, while hyperpolarizing current decreased it and revealed a tonic depolarization of the motor neurons during the bout of rhythmic motor activity. The same results were gathered from recording tibial leg motoneurons during ‘twitching’ motor activity in decerebrated animals. Our results indicate that alternating rhythmic motoneuron activity in the deafferented stick insect walking system results from phasic inhibitory drive provided by central pattern generating networks. This inhibitory input patterns the firing of the motoneurons that results from a tonic depolarizing drive. This tonic depolarizing drive was also observed in tibial motoneurons of the deafferented mesothoracic ganglion during walking movements of the intact ipsilateral front leg.

[1]  S. Grillner Control of Locomotion in Bipeds, Tetrapods, and Fish , 1981 .

[2]  P A Getting,et al.  Motor organization of Tritonia swimming. II. Synaptic drive to flexion neurons from premotor interneurons. , 1982, Journal of neurophysiology.

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

[4]  Professor Dr. Ulrich Bässler Neural Basis of Elementary Behavior in Stick Insects , 1983, Studies of Brain Function.

[5]  S. H. Chandler,et al.  Characterization of synaptic potentials in hindlimb extensor motoneurons duringl-DOPA-induced fictive locomotion in acure and chronic spinal cats , 1984, Brain Research.

[6]  S. Grillner,et al.  Dorsal and ventral myotome motoneurons and their input during fictive locomotion in lamprey , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[7]  S. Soffe,et al.  Synaptic potentials in motoneurons during fictive swimming in spinal Xenopus embryos. , 1985, Journal of neurophysiology.

[8]  L. Jordan,et al.  Excitatory and inhibitory postsynaptic potentials in alpha-motoneurons produced during fictive locomotion by stimulation of the mesencephalic locomotor region. , 1985, Journal of neurophysiology.

[9]  S. Soffe,et al.  Spinal Interneurones and Swimming in Frog Embryos , 1986 .

[10]  U. Bässler,et al.  Motoneurone im Meso- und Metathorakalganglion der Stabheuschrecke Carausius morosus , 1986 .

[11]  J. Schmitz,et al.  An improved electrode design for en passant recording from small nerves. , 1988, Comparative biochemistry and physiology. A, Comparative physiology.

[12]  G. Laurent,et al.  Intersegmental interneurons can control the gain of reflexes in adjacent segments of the locust by their action on nonspiking local interneurons , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

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

[15]  K. Pearson Common principles of motor control in vertebrates and invertebrates. , 1993, Annual review of neuroscience.

[16]  Y. Arshavsky,et al.  Neuronal control of swimming locomotion: analysis of the pteropod mollusc Clione and embryos of the amphibian Xenopus , 1993, Trends in Neurosciences.

[17]  J. Dean,et al.  Intersegmental and local interneurons in the metathorax of the stick insect Carausius morosus that monitor middle leg position. , 1994, Journal of neurophysiology.

[18]  J. C. Smith,et al.  Neural control of respiratory pattern in mammals: an overview , 1995 .

[19]  J. Schmitz,et al.  Rhythmic patterns in the thoracic nerve cord of the stick insect induced by pilocarpine , 1995, The Journal of experimental biology.

[20]  A. Büschges Role of local nonspiking interneurons in the generation of rhythmic motor activity in the stick insect. , 1995, Journal of neurobiology.

[21]  E. Marder,et al.  Principles of rhythmic motor pattern generation. , 1996, Physiological reviews.

[22]  F. Clarac,et al.  The synaptic drive from the spinal locomotor network to motoneurons in the newborn rat , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[23]  R. Levine,et al.  Crawling motor patterns induced by pilocarpine in isolated larval nerve cords of Manduca sexta. , 1996, Journal of neurophysiology.

[24]  M. Burrows The Neurobiology of an Insect Brain , 1996 .

[25]  A. Büschges Inhibitory synaptic drive patterns motoneuronal activity in rhythmic preparations of isolated thoracic ganglia in the stick insect , 1998, Brain Research.

[26]  A. Büschges,et al.  Sensory pathways and their modulation in the control of locomotion , 1998, Current Opinion in Neurobiology.

[27]  U. Bässler,et al.  Pattern generation for stick insect walking movements—multisensory control of a locomotor program , 1998, Brain Research Reviews.

[28]  S. Grillner,et al.  Neuronal Control of LocomotionFrom Mollusc to Man , 1999 .

[29]  A K Tryba,et al.  Multi-joint coordination during walking and foothold searching in the Blaberus cockroach. II. Extensor motor neuron pattern. , 2000, Journal of neurophysiology.

[30]  A. Büschges,et al.  Pattern generation for walking and searching movements of a stick insect leg. II. Control of motoneuronal activity. , 2001, Journal of neurophysiology.

[31]  E. Marder,et al.  Central pattern generators and the control of rhythmic movements , 2001, Current Biology.

[32]  U. Bässler,et al.  The role of sensory signals from the insect coxa-trochanteral joint in controlling motor activity of the femur-tibia joint. , 2001, Journal of neurophysiology.

[33]  S. Grillner The motor infrastructure: from ion channels to neuronal networks , 2003, Nature Reviews Neuroscience.

[34]  Dirk Bucher,et al.  Interjoint coordination in the stick insect leg-control system: the role of positional signaling. , 2003, Journal of neurophysiology.

[35]  Brian Mulloney,et al.  During Fictive Locomotion, Graded Synaptic Currents Drive Bursts of Impulses in Swimmeret Motor Neurons , 2003, The Journal of Neuroscience.

[36]  A. Büschges,et al.  Control of flexor motoneuron activity during single leg walking of the stick insect on an electronically controlled treadwheel. , 2003, Journal of neurobiology.

[37]  D. Weidler,et al.  The role of cations in conduction in the central nervous system of the herbivorous insect Carausius morosus , 1969, Zeitschrift für vergleichende Physiologie.

[38]  Ulrich Bässler,et al.  The walking-(and searching-) pattern generator of stick insects, a modular system composed of reflex chains and endogenous oscillators , 1993, Biological Cybernetics.

[39]  H. Pflüger The control of the rocking movements of the phasmidCarausius morosus Br. , 2004, Journal of comparative physiology.

[40]  Ansgar Büschges,et al.  Distributed processing on the basis of parallel and antagonistic pathways simulation of the femur-tibia control system in the stick insect , 1996, Journal of Computational Neuroscience.

[41]  Über rhythmische Erscheinungen bei der Stabheuschrecke Carausius morosusBr. , 1956, Zeitschrift für vergleichende Physiologie.

[42]  D. Graham Effects of circum-oesophageal lesion on the behaviour of the stick insect Carausius morosus , 1979, Biological Cybernetics.

[43]  P. Wallén,et al.  Origin of phasic synaptic inhibition in myotomal motoneurons during fictive locomotion in the lamprey , 1993, Experimental Brain Research.

[44]  K. G. Pearson,et al.  Patterns of synaptic input to identified flight motoneurons in the locust , 1984, Journal of Comparative Physiology A.