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PMID: 17267556 Published · ppublish English Comparative Study Journal Article Research Support, Non-U.S. Gov't

Sensory-motor transformation by individual command neurons.

Zelenin PV, Orlovsky GN, Deliagina TG

Abstract

Animals and humans maintain a definite body orientation in space during locomotion. Here we analyze the system for the control of body orientation in the lamprey (a lower vertebrate). In the swimming lamprey, commands for changing the body orientation are based on vestibular information; they are transmitted to the spinal cord by reticulospinal (RS) neurons. The aim of this study was to characterize the sensory-motor transformation performed by individual RS neurons. The brainstem-spinal cord preparation with vestibular organs was used. For each RS neuron, we recorded (1) its vestibular responses to turns in different planes and (2) responses in different motoneuron pools of the spinal cord to stimulation of the same RS neuron; the latter data allowed us to estimate the direction of torque (caused by the RS neuron) that will rotate the animal's body during swimming. For each of the three main planes (roll, pitch, and yaw), two groups of RS neurons were found; they were activated by rotation in opposite directions and caused the torques counteracting the rotation that activated the neuron. In each plane, the system will stabilize the orientation at which the two groups are equally active; any deviation from this orientation will evoke a corrective motor response. Thus, individual RS neurons transform sensory information about the body orientation into the motor commands that cause corrections of orientation. The closed-loop mechanisms formed by individual neurons of a group operate in parallel to generate the resulting motor responses.

MeSH Terms
Action Potentials/physiology Animals Lampreys Motor Activity/physiology Neural Pathways/physiology Neurons, Afferent/physiology Orientation/physiology Swimming/physiology
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Zelenin Pavel V
The Nobel Institute for Neurophysiology, Department of Neuroscience, Karolinska Institute, SE-171 77 Stockholm, Sweden. Pavel.Zelenin@ki.se
Orlovsky Grigori N
Deliagina Tatiana G
References (28)
28 references, click to expand
  1. Neuronal mechanisms for the control of body orientation in Clione I. Spatial zones of activity of different neuron groups.
    J Neurophysiol. 1999 Aug;82(2):687-99 PMID: 10444666
  2. Activity of reticulospinal neurons during locomotion in the freely behaving lamprey.
    J Neurophysiol. 2000 Feb;83(2):853-63 PMID: 10669499
  3. Responses of reticulospinal neurons in intact lamprey to vestibular and visual inputs.
    J Neurophysiol. 2000 Feb;83(2):864-78 PMID: 10669500
  4. Heterogeneity of the population of command neurons in the lamprey.
    J Neurosci. 2001 Oct 1;21(19):7793-803 PMID: 11567070
  5. Modifications of vestibular responses of individual reticulospinal neurons in lamprey caused by unilateral labyrinthectomy.
    J Neurophysiol. 2002 Jan;87(1):1-14 PMID: 11784725
  6. Responses of reticulospinal neurons in intact lamprey to pitch tilt.
    J Neurophysiol. 2002 Sep;88(3):1136-46 PMID: 12205135
  7. Comparative neurobiology of postural control.
    Curr Opin Neurobiol. 2002 Dec;12(6):652-7 PMID: 12490255
  8. Encoding and decoding of reticulospinal commands.
    Brain Res Brain Res Rev. 2002 Oct;40(1-3):166-77 PMID: 12589915
  9. The pattern of motor coordination underlying the roll in the lamprey.
    J Exp Biol. 2003 Aug;206(Pt 15):2557-66 PMID: 12819263
  10. Comparison of the motor effects of individual vestibulo- and reticulospinal neurons on dorsal and ventral myotomes in lamprey.
    J Neurophysiol. 2003 Nov;90(5):3161-7 PMID: 12917388
  11. Vestibular control of swimming in lamprey. II. Characteristics of spatial sensitivity of reticulospinal neurons.
    Exp Brain Res. 1992;90(3):489-98 PMID: 1426109
  12. Vestibular control of swimming in lamprey. III. Activity of vestibular afferents: convergence of vestibular inputs on reticulospinal neurons.
    Exp Brain Res. 1992;90(3):499-507 PMID: 1426110
  13. Activity of individual reticulospinal neurons during different forms of locomotion in the lamprey.
    Eur J Neurosci. 2005 Nov;22(9):2271-82 PMID: 16262665
  14. Neural bases of postural control.
    Physiology (Bethesda). 2006 Jun;21:216-25 PMID: 16714480
  15. Responses of reticulospinal neurons in the lamprey to lateral turns.
    J Neurophysiol. 2007 Jan;97(1):512-21 PMID: 17079339
  16. Reticulospinal neurons in lamprey: transmitters, synaptic interactions and their role during locomotion.
    Arch Ital Biol. 1988 Oct;126(4):317-45 PMID: 2904246
  17. Discharge patterns of reticulospinal and other reticular neurons in chronic, unrestrained cats walking on a treadmill.
    J Neurophysiol. 1986 Feb;55(2):375-401 PMID: 3950696
  18. Topological analysis of the brain stem of the lamprey Lampetra fluviatilis.
    J Comp Neurol. 1972 Jun;145(2):165-77 PMID: 5030641
  19. Inherent asymmetry and reflex modulation of the locust flight motor pattern.
    J Exp Biol. 1968 Jun;48(3):631-41 PMID: 5697834
  20. Physiological and anatomical studies on large neurons of central nervous system of the sea lamprey (Petromyzon marinus). I. Müller and Mauthner cells.
    J Neurophysiol. 1967 Sep;30(5):1000-23 PMID: 6069724
  21. Postspike facilitation of forelimb muscle activity by primate corticomotoneuronal cells.
    J Neurophysiol. 1980 Oct;44(4):751-72 PMID: 6253604
  22. Activation of NMDA-receptors elicits "fictive locomotion" in lamprey spinal cord in vitro.
    Acta Physiol Scand. 1981 Dec;113(4):549-51 PMID: 6291323
  23. Neural networks that co-ordinate locomotion and body orientation in lamprey.
    Trends Neurosci. 1995 Jun;18(6):270-9 PMID: 7571002
  24. Visual input affects the response to roll in reticulospinal neurons of the lamprey.
    Exp Brain Res. 1993;95(3):421-8 PMID: 8224067
  25. Descending control of turning locomotor activity in larval lamprey: neurophysiology and computer modeling.
    J Neurophysiol. 1997 Jul;78(1):214-28 PMID: 9242275
  26. Spatial orientation in the lamprey. I. Control of pitch and roll
    J Exp Biol. 1995;198(Pt 3):665-73 PMID: 9318405
  27. Control of spatial orientation in a mollusc.
    Nature. 1998 May 14;393(6681):172-5 PMID: 9603520
  28. Differential effects of the reticulospinal system on locomotion in lamprey.
    J Neurophysiol. 1998 Jul;80(1):103-12 PMID: 9658032
Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
1529-2401
Published
2007-01-31
Pages
1024-32
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC6673182
Subset
IM
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