Thoracic leg motoneurons in the isolated CNS of adult Manduca produce patterned activity in response to pilocarpine, which is distinct from that produced in larvae

Abstract. In the hawkmoth, Manduca sexta, thoracic leg motoneurons survive the degeneration of the larval leg muscles to innervate new muscles of the adult legs. The same motoneurons, therefore, participate in the very different modes of terrestrial locomotion that are used by larvae (crawling) and adults (walking). Consequently, changes in locomotor behavior may reflect changes in both the CNS and periphery. The present study was undertaken to determine whether motor patterns produced by the isolated CNS of adult Manduca, in the absence of sensory feedback, would resemble adult specific patterns of coordination. Pilocarpine, which evokes a fictive crawling motor pattern from the isolated larval CNS, also evoked robust patterned activity from leg motoneurons in the isolated adult CNS. As in the larva, levator and depressor motoneurons innervating the same leg were active in antiphase. Unlike fictive crawling, however, bursts of activity in levator or depressor motoneurons of one leg alternated with bursts in the homologous motoneurons innervating the opposite leg of the same segment and the leg on the same side in the adjacent segment. The most common mode of intersegmental activity generated by the isolated adult CNS resembled an alternating tripod gait, which is displayed, albeit infrequently, during walking in intact adult Manduca. A detailed analysis revealed specific differences between the patterned motor activity that is evoked from the isolated adult CNS and activity patterns observed during walking in intact animals, perhaps indicating an important role for sensory feedback. Nevertheless, the basic similarity to adult walking and clear distinctions from the larval fictive crawling pattern suggest that changes within the CNS contribute to alterations in locomotor activity during metamorphosis.

[1]  J. L. Eaton Nervous system of the head and thorax of the adult tobacco hornworm, Manduca sexta (Lepidoptera: Sphingidae) , 1974 .

[2]  J. Truman,et al.  Metamorphosis of the insect nervous system: changes in morphology and synaptic interactions of identified neurones , 1982, Nature.

[3]  P Bräunig The peripheral and central nervous organization of the locust coxo-trochanteral joint. , 1982, Journal of neurobiology.

[4]  J. Truman,et al.  Cell death in invertebrate nervous systems. , 1984, Annual review of neuroscience.

[5]  J. Truman,et al.  Postembryonic neurogenesis in the CNS of the tobacco hornworm, Manduca sexta. I. Neuroblast arrays and the fate of their progeny during metamorphosis , 1987, The Journal of comparative neurology.

[6]  R. Levine,et al.  Neural control of leg movements in a metamorphic insect: Sensory and motor elements of the larval thoracic legs in Manduca sexta , 1988, The Journal of comparative neurology.

[7]  R. Levine,et al.  Neural control of leg movements in a metamorphic insect: Persistence of larval leg motor neurons to innervate the adult legs of Manduca sexta , 1988, The Journal of comparative neurology.

[8]  B. Trimmer,et al.  Effects of Nicotinic and Muscarinic Agents on an Identified Motoneurone and its Direct Afferent Inputs in Larval Manduca Sexta , 1989 .

[9]  J. Weeks,et al.  Respecification of larval proleg motoneurons during metamorphosis of the tobacco hornworm, Manduca sexta: segmental dependence and hormonal regulation. , 1989, Journal of neurobiology.

[10]  G. Jacobs,et al.  Postsynaptic changes at a sensory-to-motoneuron synapse contribute to the developmental loss of a reflex behavior during insect metamorphosis , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[11]  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.

[12]  R. Levine,et al.  Postembryonic neuronal plasticity and its hormonal control during insect metamorphosis. , 1990, Annual review of neuroscience.

[13]  N. Spitzer,et al.  A developmental handshake: neuronal control of ionic currents and their control of neuronal differentiation. , 1991, Journal of neurobiology.

[14]  J. Truman,et al.  The regulation of transmitter expression in postembryonic lineages in the moth Manduca sexta. I. Transmitter identification and developmental acquisition of expression , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[15]  R. Levine,et al.  Calcium and potassium currents in leg motoneurons during postembryonic development in the hawkmoth Manduca sexta. , 1992, The Journal of experimental biology.

[16]  A. Bekoff Neuroethological approaches to the study of motor development in chicks: achievements and challenges. , 1992, Journal of neurobiology.

[17]  R. Levine,et al.  Effects of the steroid hormone, 20-hydroxyecdysone, on the growth of neurites by identified insect motoneurons in vitro. , 1992, Developmental biology.

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

[19]  R. Levine,et al.  Dendritic reorganization of an identified neuron during metamorphosis of the moth Manduca sexta: the influence of interactions with the periphery. , 1993, Journal of neurobiology.

[20]  S. Ryckebusch,et al.  Interactions between segmental leg central pattern generators during fictive rhythms in the locust. , 1994, Journal of neurophysiology.

[21]  R. Levine,et al.  Steroid hormone effects on neurons subserving behavior , 1995, Current Opinion in Neurobiology.

[22]  LC Streichert,et al.  Decreased monosynaptic sensory input to an identified motoneuron is associated with steroid-mediated dendritic regression during metamorphosis in Manduca sexta , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[23]  R. Levine,et al.  Remodeling of the insect nervous system , 1995, Current Opinion in Neurobiology.

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

[25]  R. Anderson,et al.  Leg proprioceptors of the tobacco hornworm, Manduca sexta: Organization of central projections at larval and adult stages , 1996, Microscopy research and technique.

[26]  R. Levine,et al.  Locomotory behavior in the hawkmoth Manduca sexta: kinematic and electromyographic analyses of the thoracic legs in larvae and adults. , 1996, The Journal of experimental biology.

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

[28]  R. Levine,et al.  Synaptic interactions between a muscle-associated proprioceptor and body wall muscle motor neurons in larval and Adult manduca sexta. , 1996, Journal of neurophysiology.

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

[30]  R. Levine,et al.  Remodeling of the peripheral processes and presynaptic terminals of leg motoneurons during metamorphosis of the hawkmoth, Manduca sexta , 1996, The Journal of comparative neurology.

[31]  R. Levine,et al.  Development of adult thoracic leg muscles during metamorphosis of the hawk moth Manduca sexta , 1997, Cell and Tissue Research.

[32]  P. Meyrand,et al.  Development of rhythmic pattern generators , 1998, Current Opinion in Neurobiology.

[33]  R. Levine,et al.  Ecdysteroid control of ionic current development in Manduca sexta motoneurons. , 1998, Journal of neurobiology.

[34]  R. Levine,et al.  Steroid hormone enhancement of neurite outgrowth in identified insect motor neurons involves specific effects on growth cone form and function. , 1999, Journal of neurobiology.

[35]  H. Pflüger Neuromodulation during motor development and behavior , 1999, Current Opinion in Neurobiology.

[36]  C. Consoulas Remodeling of the leg sensory system during metamorphosis of the hawkmoth, Manduca sexta , 2000, The Journal of comparative neurology.

[37]  C Duch,et al.  Remodeling of Membrane Properties and Dendritic Architecture Accompanies the Postembryonic Conversion of a Slow into a Fast Motoneuron , 2000, The Journal of Neuroscience.

[38]  K. Sillar,et al.  The development of neuromodulatory systems and the maturation of motor patterns in amphibian tadpoles , 2000, Brain Research Bulletin.

[39]  R. Levine,et al.  Remodeling of the femoral chordotonal organ during metamorphosis of the hawkmoth, Manduca sexta , 2000, The Journal of comparative neurology.

[40]  R. Levine,et al.  Comparison of identified leg motoneuron structure and function between larval and adult Manduca sexta , 2000, Journal of Comparative Physiology A.

[41]  C Duch,et al.  Postembryonic development of the dorsal longitudinal flight muscle and its innervation in Manduca sexta , 2000, The Journal of comparative neurology.

[42]  Carsten Duch,et al.  Behavioral transformations during metamorphosis: remodeling of neural and motor systems , 2000, Brain Research Bulletin.

[43]  R. Levine,et al.  Dendritic Remodeling and Growth of Motoneurons during Metamorphosis of Drosophila melanogaster , 2002, The Journal of Neuroscience.

[44]  R. Levine,et al.  Changes in calcium signaling during postembryonic dendritic growth in Manduca sexta. , 2002, Journal of neurophysiology.

[45]  Laura M. Griffin,et al.  Sensory organs of the thoracic legs of the moth Manduca sexta , 1990, Cell and Tissue Research.