Role of type-specific neuron properties in a spinal cord motor network

Recent recordings from spinal neurons in hatchling frog tadpoles allow their type-specific properties to be defined. Seven main types of neuron involved in the control of swimming have been characterized. To investigate the significance of type-specific properties, we build models of each neuron type and assemble them into a network using known connectivity between: sensory neurons, sensory pathway interneurons, central pattern generator (CPG) interneurons and motoneurons. A single stimulus to a sensory neuron initiates swimming where modelled neuronal and network activity parallels physiological activity. Substitution of firing properties between neuron types shows that those of excitatory CPG interneurons are critical for stable swimming. We suggest that type-specific neuronal properties can reflect the requirements for involvement in one particular network response (like swimming), but may also reflect the need to participate in more than one response (like swimming and slower struggling).

[1]  Nicholas Dale,et al.  Coordinated Motor Activity in Simulated Spinal Networks Emerges from Simple Biologically Plausible Rules of Connectivity , 2004, Journal of Computational Neuroscience.

[2]  A. Roberts,et al.  Glutamate and acetylcholine corelease at developing synapses. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[3]  Alan Roberts,et al.  Modelling Inter-Segmental Coordination of Neuronal Oscillators: Synaptic Mechanisms for Uni-Directional Coupling During Swimming in Xenopus Tadpoles , 2002, Journal of Computational Neuroscience.

[4]  S. Grillner,et al.  Cellular bases of a vertebrate locomotor system–steering, intersegmental and segmental co-ordination and sensory control , 2002, Brain Research Reviews.

[5]  Alan Roberts,et al.  Dorsal spinal interneurons forming a primitive, cutaneous sensory pathway. , 2004, Journal of neurophysiology.

[6]  F. Kuenzi,et al.  Xenopus embryonic spinal neurons recorded in situ with patch‐clamp electrodes – conditional oscillators after all? , 2003, The European journal of neuroscience.

[7]  Michael Schaefer,et al.  Neurotransmitter properties of spinal interneurons in embryonic and larval zebrafish , 2004, The Journal of comparative neurology.

[8]  Alan Roberts,et al.  A direct comparison of whole cell patch and sharp electrodes by simultaneous recording from single spinal neurons in frog tadpoles. , 2004, Journal of neurophysiology.

[9]  Alan Roberts,et al.  The Influence of Magnesium lons on the NMDA Mediated Responses of Ventral Rhythmic Neurons in the Spinal Cord of Xenopus Embryos , 1989, The European journal of neuroscience.

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

[11]  N. Dale,et al.  Experimentally derived model for the locomotor pattern generator in the Xenopus embryo. , 1995, The Journal of physiology.

[12]  S. Soffe.  Roles of Glycinergic Inhibition and N‐Methyl‐D‐Aspartate Receptor Mediated Excitation in the Locomotor Rhythmicity of One Half of the Xenopus Embryo Central Nervous System , 1989, The European journal of neuroscience.

[13]  S. Soffe,et al.  Two distinct rhythmic motor patterns are driven by common premotor and motor neurons in a simple vertebrate spinal cord , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[14]  A. Roberts,et al.  The neuromuscular basis of swimming movements in embryos of the amphibian Xenopus laevis. , 1982, The Journal of experimental biology.

[15]  D. Parker.  Spinal-cord plasticity , 2000, Molecular Neurobiology.

[16]  Alan Roberts,et al.  Primitive Roles for Inhibitory Interneurons in Developing Frog Spinal Cord , 2004, The Journal of Neuroscience.

[17]  L. Nowak,et al.  Magnesium gates glutamate-activated channels in mouse central neurones , 1984, Nature.

[18]  Spinal-Cord plasticity: independent and interactive effects of neuromodulator and activity-dependent plasticity. , 2000, Molecular neurobiology.

[19]  Alan Roberts,et al.  Early functional organization of spinal neurons in developing lower vertebrates , 2000, Brain Research Bulletin.

[20]  S. Hunt,et al.  Sensory physiology, anatomy and immunohistochemistry of Rohon‐Beard neurones in embryos of Xenopus laevis. , 1984, The Journal of physiology.

[21]  J. Lübke,et al.  Functional Properties of AMPA and NMDA Receptors Expressed in Identified Types of Basal Ganglia Neurons , 1997, The Journal of Neuroscience.

[22]  A. Roberts,et al.  Persistent Responses to Brief Stimuli: Feedback Excitation among Brainstem Neurons , 2006, The Journal of Neuroscience.

[23]  A. Hodgkin,et al.  A quantitative description of membrane current and its application to conduction and excitation in nerve , 1990 .

[24]  Alan Roberts,et al.  The Spinal Interneurons and Properties of Glutamatergic Synapses in a Primitive Vertebrate Cutaneous Flexion Reflex , 2003, The Journal of Neuroscience.

[25]  A. Roberts,et al.  Mutual Re‐excitation with Post‐Inhibitory Rebound: A Simulation Study on the Mechanisms for Locomotor Rhythm Generation in the Spinal Cord of Xenopus Embryos , 1990, The European journal of neuroscience.

[26]  Alan Roberts,et al.  Functional projection distances of spinal interneurons mediating reciprocal inhibition during swimming in Xenopus tadpoles , 2001, The European journal of neuroscience.

[27]  S. Soffe,et al.  Transitions between two different motor patterns in Xenopus embryos , 1996, Journal of Comparative Physiology A.

[28]  S. Hestrin,et al.  Properties of GABAA Receptors Underlying Inhibitory Synaptic Currents in Neocortical Pyramidal Neurons , 1997, The Journal of Neuroscience.

[29]  Alan Roberts,et al.  The morphology and distribution of ‘Kolmer–Agduhr cells’, a class of cerebrospinal-fluid-contacting neurons revealed in the frog embryo spinal cord by GABA immunocytochemistry , 1987, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[30]  Pierre Meyrand,et al.  Electrical coupling induces bistability of rhythms in networks of inhibitory spiking neurons , 2005, The European journal of neuroscience.

[31]  Local effects of glycinergic inhibition in the spinal cord motor systems for swimming in amphibian embryos. , 1996, Journal of neurophysiology.

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

[33]  J. Fellous,et al.  A role for NMDA-receptor channels in working memory , 1998, Nature Neuroscience.

[34]  Alan Roberts,et al.  Motoneurons of the axial swimming muscles in hatchling Xenopus tadpoles: Features, distribution, and central synapses , 1999, The Journal of comparative neurology.

[35]  S. Soffe,et al.  Activity of myotomal motoneurons during fictive swimming in frog embryos. , 1982, Journal of neurophysiology.

[36]  Y. Koninck,et al.  Four cell types with distinctive membrane properties and morphologies in lamina I of the spinal dorsal horn of the adult rat , 2002, The Journal of physiology.

[37]  J. Faber,et al.  Normal table of Xenopus laevis (Daudin). A systematical and chronological survey of the development from the fertilized egg till the end of metamorphosis. , 1956 .

[38]  Ronald L Calabrese,et al.  Detailed model of intersegmental coordination in the timing network of the leech heartbeat central pattern generator. , 2004, Journal of neurophysiology.

[39]  K. Sillar,et al.  A neuronal mechanism for sensory gating during locomotion in a vertebrate , 1988, Nature.

[40]  Anders Lansner,et al.  Neural mechanisms potentially contributing to the intersegmental phase lag in lamprey , 1999, Biological Cybernetics.

[41]  Wulfram Gerstner,et al.  Spiking Neuron Models , 2002 .

[42]  A. Ribera,et al.  Primary sensory neurons express a Shaker-like potassium channel gene , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[43]  K. Sillar,et al.  Characterization and Function of Spinal Excitatory Interneurons with Commissural Projections in Xenopus laevis embryos , 1990, The European journal of neuroscience.

[44]  A. Roberts,et al.  Defining classes of spinal interneuron and their axonal projections in hatchling Xenopus laevis tadpoles , 2001, The Journal of comparative neurology.

[45]  Alan Roberts,et al.  Spinal Inhibitory Neurons that Modulate Cutaneous Sensory Pathways during Locomotion in a Simple Vertebrate , 2002, The Journal of Neuroscience.

[46]  A. Roberts,et al.  Non‐linear summation of excitatory synaptic inputs to small neurones: a case study in spinal motoneurones of the young Xenopus tadpole , 1998, The Journal of physiology.

[47]  S. Grillner,et al.  Mechanisms of Rhythm Generation in a Spinal Locomotor Network Deprived of Crossed Connections: The Lamprey Hemicord , 2005, The Journal of Neuroscience.

[48]  Gail Mandel,et al.  Distribution of prospective glutamatergic, glycinergic, and GABAergic neurons in embryonic and larval zebrafish , 2004, The Journal of comparative neurology.

[49]  N Dale,et al.  Reciprocal inhibitory interneurones in the Xenopus embryo spinal cord. , 1985, The Journal of physiology.

[50]  A. Roberts,et al.  Asymmetries in sensory pathways from skin to motoneurons on each side of the body determine the direction of an avoidance response in hatchling Xenopus tadpoles , 1998, The Journal of physiology.

[51]  K. Keefe,et al.  Evidence for functionally distinct synaptic NMDA receptors in ventromedial versus dorsolateral striatum. , 2003, Journal of neurophysiology.

[52]  N. Dale,et al.  Kinetic characterization of the voltage‐gated currents possessed by Xenopus embryo spinal neurons. , 1995, The Journal of physiology.