Activity of individual reticulospinal neurons during different forms of locomotion in the lamprey

Lamprey (a lower vertebrate) can employ different modes of locomotion, i.e. swimming in open water and crawling in tight places. Swimming is due to the periodic waves of lateral undulations with reciprocal activity of right and left muscles. In contrast, crawling (forward and backward) is based on single waves with coactivation of muscles on two sides. Basic mechanisms of swimming and, most likely, crawling reside in the spinal cord, and are activated by supraspinal commands. The main source of these commands is the reticulospinal (RS) system. The goal of the present experiments was to characterize the activity of individual RS neurons during swimming and during crawling in a U‐shaped tunnel. The activity was recorded by means of chronically implanted electrodes in freely behaving animals. All recorded RS neurons were active during swimming but silent in quiescent animals. Many of them (61%) showed phasic modulation of their firing rate approximately in phase with the activity of ipsilateral rostral muscles. The majority of the neurons (80%) were also active during crawling. Many of them either increased or decreased their activity during crawling as compared to the background activity. These changes were better correlated with the direction of progression (forward or backward) than with the direction of turning in the tunnel (right or left). No correlation of the activity of RS neurons during locomotion and their sensory inputs was found. The results of this study suggest that different modes of locomotion in lampreys can be caused by considerably overlapping groups of RS neurons.

[1]  S. Grillner,et al.  The role of spinal cord inputs in modulating the activity of reticulospinal neurons during fictive locomotion in the lamprey , 1989, Brain Research.

[2]  S. Rossignol,et al.  LOCOMOTION IN LAMPREY AND TROUT: THE RELATIVE TIMING OF ACTIVATION AND MOVEMENT , 1989 .

[3]  R. Gregor,et al.  Adaptive control for backward quadrupedal walking. IV. Hindlimb kinetics during stance and swing. , 1993, Journal of neurophysiology.

[4]  S Grillner,et al.  Heterogeneity of the Population of Command Neurons in the Lamprey , 2001, The Journal of Neuroscience.

[5]  S. Rossignol,et al.  Discharge patterns of reticulospinal and other reticular neurons in chronic, unrestrained cats walking on a treadmill. , 1986, Journal of neurophysiology.

[6]  S. Grillner,et al.  The edge cell, a possible intraspinal mechanoreceptor. , 1984, Science.

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

[8]  S. Grillner,et al.  Phasic modulation of reticulospinal neurones during fictive locomotion and other types of spinal motor activity in lamprey , 1989, Brain Research.

[9]  R Nieuwenhuys,et al.  Topological analysis of the brain stem of the lamprey Lampetra fluviatilis , 1972, The Journal of comparative neurology.

[10]  L. M. Frolich,et al.  KINEMATIC AND ELECTROMYOGRAPHIC ANALYSIS OF THE FUNCTIONAL ROLE OF THE BODY AXIS DURING TERRESTRIAL AND AQUATIC LOCOMOTION IN THE SALAMANDER AMBYSTOMA TIGRINUM , 1992 .

[11]  B. Jayne,et al.  Muscular mechanisms of snake locomotion: an electromyographic study of the sidewinding and concertina modes of Crotalus cerastes, Nerodia fasciata and Elaphe obsoleta. , 1988, The Journal of experimental biology.

[12]  S. Grillner,et al.  Synaptic effects of intraspinal stretch receptor neurons mediating movement-related feedback during locomotion , 1990, Brain Research.

[13]  C. Rovainen.  Synaptic interactions of reticulospinal neurons and nerve cells in the spinal cord of the sea lamprey , 1974, The Journal of comparative neurology.

[14]  R. Dubuc,et al.  Differential contribution of reticulospinal cells to the control of locomotion induced by the mesencephalic locomotor region. , 2003, Journal of neurophysiology.

[15]  S. Grillner,et al.  Reticulospinal neurons in lamprey: transmitters, synaptic interactions and their role during locomotion. , 1988, Archives italiennes de biologie.

[16]  G. Orlovsky,et al.  Non-undulatory locomotion in the lamprey , 2001, Neuroreport.

[17]  A. Thorstensson,et al.  How is the normal locomotor program modified to produce backward walking? , 2004, Experimental Brain Research.

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

[19]  S. Grillner,et al.  Müller cells and other reticulospinal neurones are phasically active during fictive locomotion in the isolated nervous system of the lamprey , 1986, Neuroscience Letters.

[20]  S. Grillner,et al.  Neuronal Control of Locomotion 'From Mollusc to Man ' , 1999 .

[21]  I. Engberg,et al.  An electromyographic analysis of muscular activity in the hindlimb of the cat during unrestrained locomotion. , 1969, Acta physiologica Scandinavica.

[22]  Richard C. Snyder,et al.  Quadrupedal and Bipedal Locomotion of Lizards , 1952 .

[23]  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.

[24]  T. Deliagina,et al.  Responses of reticulospinal neurons in intact lamprey to vestibular and visual inputs. , 2000, Journal of neurophysiology.

[25]  Adam G. Davidson,et al.  Movement-related and preparatory activity in the reticulospinal system of the monkey , 2004, Experimental Brain Research.

[26]  S. Grillner,et al.  Monosynaptic excitatory amino acid transmission from the posterior rhombencephalic reticular nucleus to spinal neurons involved in the control of locomotion in lamprey. , 1989, Journal of neurophysiology.

[27]  S. Grillner,et al.  The intrinsic function of a motor system — from ion channels to networks and behavior 1 1 Published on the World Wide Web on 22 November 2000. , 2000, Brain Research.

[28]  S. Grillner,et al.  Vestibular control of swimming in lamprey , 1992, Experimental Brain Research.

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

[30]  R. Zernicke,et al.  Adaptive control for backward quadrupedal walking. I. Posture and hindlimb kinematics. , 1990, Journal of neurophysiology.

[31]  G. Orlovsky,et al.  Encoding and decoding of reticulospinal commands , 2002, Brain Research Reviews.

[32]  Sten Grillner,et al.  Role of dermal photoreceptors and lateral eyes in initiation and orientation of locomotion in lamprey , 1993, Behavioural Brain Research.

[33]  Ullén,et al.  Spatial orientation in the lamprey. I. Control of pitch and roll , 1995, The Journal of experimental biology.

[34]  S. Mori,et al.  Biomechanical constraints in hindlimb joints during the quadrupedal versus bipedal locomotion of M. fuscata. , 2004, Progress in brain research.

[35]  S. Grillner,et al.  On the Generation and Performance of Swimming in Fish , 1976 .

[36]  B. Jayne,et al.  Comparative three-dimensional kinematics of the hindlimb for high-speed bipedal and quadrupedal locomotion of lizards , 1999, The Journal of experimental biology.

[37]  M. Ronan.  Origins of the descending spinal projections in petromyzontid and myxinoid agnathans , 1989, The Journal of comparative neurology.

[38]  M. Sirota,et al.  Stimulation of the mesencephalic locomotor region elicits controlled swimming in semi‐intact lampreys , 2000, The European journal of neuroscience.

[39]  R. Harris-Warrick,et al.  Strychnine eliminates alternating motor output during fictive locomotion in the lamprey , 1984, Brain Research.

[40]  J.T. Buchanan,et al.  The neuronal network for locomotion in the lamprey spinal cord: Evidence for the involvement of commissural interneurons , 1995, Journal of Physiology-Paris.

[41]  J A Vilensky,et al.  Do quadrupeds require a change in trunk posture to walk backward? , 2000, Journal of biomechanics.

[42]  C. Rovainen.  Physiological and anatomical studies on large neurons of central nervous system of the sea lamprey (Petromyzon marinus). I. Müller and Mauthner cells. , 1967, Journal of neurophysiology.

[43]  S. Grillner,et al.  Activity of reticulospinal neurons during locomotion in the freely behaving lamprey. , 2000, Journal of neurophysiology.