Origin of phasic synaptic inhibition in myotomal motoneurons during fictive locomotion in the lamprey

The periodic membrane potential fluctuations in motoneurons during fictive locomotion in the lamprey, a primitive vertebrate, involve phasic synaptic excitation and inhibition. This paper investigates the origin of the phasic synaptic input to lamprey myotomal motoneurons in the in vitro spinal cord preparation with regard to the relative contribution of descending propriospinal input from interneurons in the local segment. The synaptic drive to myotomal motoneurons in the most rostral and the most caudal part of the spinal cord preparation are compared before and after selective spinal cord lesions. Current clamp recordings of the same cell before and after lesion showed that neither the excitatory phase nor the inhibitory phase was abolished after interruption of the descending or the ascending ipsilateral input, or after interrupting crossing segmental input by a local longitudinal midline incision. None of these sources thus appears to be alone responsible for the phasic synaptic drive. To quantitatively evaluate these effects, and in particular the contribution from the descending propriospinal fibres to the inhibitory phase, voltage clamp recordings were made in combination with a spinal cord hemisection just rostral to the motoneuron. The input from propriospinal interneurons in approximately 15 rostral segments may be responsible for as much as 70% of the phase of inhibitory current during the locomotor cycle. In accordance with these findings, a similar voltage clamp analysis of rostrally and caudally located motoneurons showed that the average peak-to-peak amplitude of the current fluctuations in rostral cells was approximately 50% of that in caudal cells.

[1]  C. Rovainen,et al.  Fast and slow motoneurons to body muscle of the sea lamprey. , 1971, Journal of neurophysiology.

[2]  S. Grillner,et al.  Central Generation of Locomotion in Vertebrates , 1976 .

[3]  W. W. Stewart,et al.  Functional connections between cells as revealed by dye-coupling with a highly fluorescent naphthalimide tracer , 1978, Cell.

[4]  S. Grillner,et al.  Does the central pattern generation for locomotion in lamprey depend on glycine inhibition? , 1980, Acta physiologica Scandinavica.

[5]  J. Buchanan,et al.  Activities of identified interneurons, motoneurons, and muscle fibers during fictive swimming in the lamprey and effects of reticulospinal and dorsal cell stimulation. , 1982, Journal of neurophysiology.

[6]  J. Buchanan Identification of interneurons with contralateral, caudal axons in the lamprey spinal cord: synaptic interactions and morphology. , 1982, Journal of neurophysiology.

[7]  S. Soffe,et al.  Tonic and phasic synaptic input to spinal cord motoneurons during fictive locomotion in frog embryos. , 1982, Journal of neurophysiology.

[8]  C. Perret Centrally generated pattern of motoneuron activity during locomotion in the cat. , 1983, Symposia of the Society for Experimental Biology.

[9]  P. Wallén,et al.  On the control of myotomal motoneurones during "fictive swimming" in the lamprey spinal cord in vitro. , 1983, Acta physiologica Scandinavica.

[10]  P. Wallén,et al.  Fictive locomotion in the lamprey spinal cord in vitro compared with swimming in the intact and spinal animal. , 1984, The Journal of physiology.

[11]  P. Wallén,et al.  do the Motoneurones Constitute a Part of the Spinal Network Generating the Swimming Rhythm in the Lamprey , 1984 .

[12]  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.

[13]  Peter Wallén,et al.  Phasic Control of Vertebrate Motoneurones During Rhythmic Motor Acts, with Special Reference to Fictive Locomotion in the Lamprey , 1986 .

[14]  S. Grillner,et al.  Dual-component synaptic potentials in the lamprey mediated by excitatory amino acid receptors , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[15]  N. Dale Excitatory synaptic drive for swimming mediated by amino acid receptors in the lamprey , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[16]  S. Grillner,et al.  N-methyl-D-aspartate receptor-induced, inherent oscillatory activity in neurons active during fictive locomotion in the lamprey , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[17]  S. Grillner,et al.  Identification of excitatory interneurons contributing to generation of locomotion in lamprey: structure, pharmacology, and function. , 1989, Journal of neurophysiology.

[18]  S. Grillner,et al.  Neuronal network generating locomotor behavior in lamprey: circuitry, transmitters, membrane properties, and simulation. , 1991, Annual review of neuroscience.

[19]  O. Kiehn Plateau potentials and active integration in the ‘final common pathway’ for motor behaviour , 1991, Trends in Neurosciences.

[20]  S. Grillner,et al.  A new population of neurons with crossed axons in the lamprey spinal cord , 1991, Brain Research.

[21]  S. Grillner,et al.  Neural mechanisms of intersegmental coordination in lamprey: local excitability changes modify the phase coupling along the spinal cord. , 1992, Journal of neurophysiology.

[22]  S. Grillner,et al.  The neurophysiological bases of undulatory locomotion in vertebrates , 1993 .

[23]  J. A. Kahn Patterns of synaptic inhibition in motoneurons and interneurons during fictive swimming in the lamprey, as revealed by Cl− injections , 1982, Journal of comparative physiology.

[24]  Anders Lansner,et al.  Computer simulation of the segmental neural network generating locomotion in lamprey by using populations of network interneurons , 2004, Biological Cybernetics.

[25]  P. Wallén,et al.  The neuronal correlate of locomotion in fish , 1980, Experimental Brain Research.