Bilateral control of hindlimb scratching in the spinal turtle: contralateral spinal circuitry contributes to the normal ipsilateral motor pattern of fictive rostral scratching

In a spinal turtle, unilateral stimulation in the rostral scratch receptive field elicited rhythmic fictive rostral scratching in ipsilateral hindlimb motor neurons; contralateral hip motor activity was also rhythmic and out-of-phase with ipsilateral hip motor activity. When left and right rostral scratch receptive fields were stimulated simultaneously, bilateral rhythmic fictive rostral scratching was produced; left hindlimb scratching was out-of-phase with right hindlimb scratching. Thus, spinal circuits coordinate interlimb phase during bilateral fictive scratching. We examined the contributions of contralateral spinal circuitry to the normal pattern of right hindlimb fictive rostral scratching by removing the left halves of the D7 segment and the hindlimb enlargement (D8-S2 segments). After left- hemicord removal, stimulation in the right rostral scratch receptive field usually elicited a variation of rostral scratching with rhythmic right hip flexor activity and no right hip extensor activity; thus, right hip flexor rhythm generation does not require left hindlimb enlargement circuitry. Normal right hindlimb rostral scratching with rhythmic alternation between hip flexor and extensor activities was rarely observed; thus, contralateral spinal circuitry contributes to the production of normal ipsilateral fictive rostral scratching. After left-hemicord removal, stimulation in the left rostral scratch receptive field elicited rhythmic right hip extensor activity; thus, contralateral spinal circuitry can generate a hip extensor rhythm during ipsilateral rostral scratch receptive field stimulation. Our observations and those of Berkowitz and Stein (1994a,b) support the concept that an ipsilateral hindlimb's normal rostral scratch motor pattern is generated by a modular central pattern generator that is bilaterally distributed in the spinal cord.

[1]  W. Smith The Integrative Action of the Nervous System , 1907, Nature.

[2]  C. Sherrington Flexion‐reflex of the limb, crossed extension‐reflex, and reflex stepping and standing , 1910, The Journal of physiology.

[3]  S. Siegel,et al.  Nonparametric Statistics for the Behavioral Sciences , 2022, The SAGE Encyclopedia of Research Design.

[4]  R. Herman,et al.  Control of Postural Reactions in Man: The Initiation of Gait , 1973 .

[5]  P. Stein Mechanisms of Interlimb Phase Control , 1976 .

[6]  I. M. Gelfand,et al.  Messages conveyed by spinocerebellar pathways during scratching in the cat. II. Activity of neurons of the ventral spinocerebellar tract , 1978, Brain Research.

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

[8]  G. Orlovsky,et al.  Efferent activity during fictitious scratch reflex in the cat. , 1981, Journal of neurophysiology.

[9]  Michael J. O'Donovan,et al.  Actions of FDL and FHL muscles in intact cats: functional dissociation between anatomical synergists. , 1982, Journal of neurophysiology.

[10]  B. Heller Circular Statistics in Biology, Edward Batschelet. Academic Press, London & New York (1981), 371, Price $69.50 , 1983 .

[11]  J. Davenport,et al.  A comparison of the swimming of marine and freshwater turtles , 1984, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[12]  T. Ruigrok,et al.  The organization of motoneurons in the turtle lumbar spinal cord , 1984, The Journal of comparative neurology.

[13]  G. A. Robertson,et al.  Three forms of the scratch reflex in the spinal turtle: central generation of motor patterns. , 1985, Journal of neurophysiology.

[14]  P. Stein,et al.  Three forms of the scratch reflex in the spinal turtle: movement analyses. , 1985, Journal of neurophysiology.

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

[16]  G. A. Robertson,et al.  Synaptic control of hindlimb motoneurones during three forms of the fictive scratch reflex in the turtle. , 1988, The Journal of physiology.

[17]  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.

[18]  P. Stein,et al.  Interruptions of fictive scratch motor rhythms by activation of cutaneous flexion reflex afferents in the turtle , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[19]  P. Stein,et al.  Spinal Cord Circuits for Motor Pattern Selection in the Turtle a , 1989, Annals of the New York Academy of Sciences.

[20]  P. Stein,et al.  Spinal cord segments containing key elements of the central pattern generators for three forms of scratch reflex in the turtle , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[21]  P. Stein,et al.  Cutaneous dermatomes for initiation of three forms of the scratch reflex in the spinal turtle , 1990, The Journal of comparative neurology.

[22]  P. Stein,et al.  Cutaneous stimulation evokes long-lasting excitation of spinal interneurons in the turtle. , 1990, Journal of neurophysiology.

[23]  J. Fetcho,et al.  Spinal network of the Mauthner cell. , 1991, Brain, behavior and evolution.

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

[25]  L. Jordan Brain stem and spinal cord mechanisms for the initiation of locomotion , 1991 .

[26]  H. Hultborn,et al.  Induction of fos expression by activity in the spinal rhythm generator for scratching , 1992, Brain Research.

[27]  B Mulloney,et al.  A separate local pattern-generating circuit controls the movements of each swimmeret in crayfish. , 1993, Journal of neurophysiology.

[28]  A. Berkowitz,et al.  Activity of descending propriospinal axons in the turtle hindlimb enlargement during two forms of fictive scratching: phase analyses , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[29]  P. Stein,et al.  Descending propriospinal axons in the hindlimb enlargement of the red‐eared turle: Cells of origin and funicular courses , 1994, The Journal of comparative neurology.

[30]  P. Stein,et al.  Activity of descending propriospinal axons in the turtle hindlimb enlargement during two forms of fictive scratching: broad tuning to regions of the body surface , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.