The Cerebellum

, Volume 11, Issue 1, pp 212–222 | Cite as

Effects of Leg-to-Body Position on the Responses of Rat Cerebellar and Vestibular Nuclear Neurons to Labyrinthine Stimulation

  • Massimo Barresi
  • Luca Bruschini
  • Guido Li Volsi
  • Diego Manzoni
Article
First Online:

Abstract

The spatial organization of vestibulospinal (VS) reflexes, elicited by labyrinthine signals and related to head motion, depends on the direction of body tilt, due to proprioceptive neck afferents acting through the cerebellar anterior vermis. The responses of Purkinje cells located within this region to labyrinthine stimulation are modulated by the head-to-body position. We investigated, in urethane-anesthetized rats, whether a 90° leg-to-trunk displacement modifies the responses of corticocerebellar and vestibular nuclear neurons to the labyrinthine input, which would indicate that VS reflexes are tuned by the leg-to-trunk position. With this aim, unit activity was recorded during “wobble” stimuli that allow evaluating the gain and spatiotemporal properties of neuronal responses. The response gain of corticocerebellar units showed a significant drop in the leg-rotated position with respect to the control one. Following a change in leg position, a proportion of the recorded neurons showed significant changes in the direction and phase of the response vector. In contrast, vestibular nuclear neurons did not show significant modifications in their response gain and direction. Thus, proprioceptive afferents signaling leg-to-trunk position seem to affect the processing of directional labyrinthine signals within the cerebellar cortex.

Keywords

Cerebellum Vestibular nuclei Vestibulospinal reflex Proprioceptive input Leg rotation 
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Notes

Acknowledgments

The present investigation was supported by grants of the Italian Space Agency (ASI, DCMC project and grant I/R/335/02) and of the University of Pisa. We thank M. Vaglini, G. Bresciani, P. Orsini, G. Montanari, and E. Cardaci for their valuable technical assistance and Mr. G. Bertolini for animal care.

Conflict of interest notification page

We declare that none of the authors has financial or personal relationships (consultancies, stock ownership, equity interests, patent-licensing arrangements) that might bias the submitted paper.

References

  1. 1.
    Roberts TDM. Neurophysiology of Postural Mechanisms. 2nd ed. London: Butterworths; 1978.Google Scholar
  2. 2.
    Horak FB, MacPherson JM. Postural orientation and equilibrium. In: Rowell LB, Shepherd JT, editors. Handbook of Physiology, Section 12: Exercise: Regulation and Integration of Multiple Systems. New York: Oxford University Press; 1996. p. 255–92.Google Scholar
  3. 3.
    Welgampola MS, Colebatch JC. Vestibulospinal reflexes: quantitative effects on sensory feedback and postural task. Exp Brain Res. 2001;139:345–53.PubMedCrossRefGoogle Scholar
  4. 4.
    Cenciarini M, Peterka R. Stimulus-dependent changes in vestibular contribution to human postural control. J Neurophysiol. 2006;95:2733–50.PubMedCrossRefGoogle Scholar
  5. 5.
    Lackner JR, Dizio P, Jeka J, Horak F, Krebs D, Rabin E. Precision contact of the fingertip reduces postural sway of individual with bilateral vestibular loss. Exp Brain Res. 1999;126:459–66.PubMedCrossRefGoogle Scholar
  6. 6.
    Igarashi M, Watanabe T, Maxian PM. Dynamic equilibrium in squirrel monkeys after unilateral and bilateral labyrinthectomy. Acta Otolaryngol. 1970;69:247–53.PubMedCrossRefGoogle Scholar
  7. 7.
    Roberts TD. Reflex balance. Nature. 1973;244:156–8.PubMedCrossRefGoogle Scholar
  8. 8.
    Wilson VJ, Schor RH, Suzuki I, Park BR. Spatial organization of neck and vestibular reflexes acting on the forelimbs of the decerebrate cat. J Neurophysiol. 1986;55:514–26.PubMedGoogle Scholar
  9. 9.
    Magnus R. Korpestellung. Berlin: Springer; 1928.Google Scholar
  10. 10.
    Von Holst E, Mittelstaedt H. Das Reafferenzprinzip (Wechselwirkung zwischen zentralnervensystem und peripherie). Naturwissenschaften. 1950;37:464–76.CrossRefGoogle Scholar
  11. 11.
    Lindsay KW, Roberts TD, Rosemberg JR. Asymmetric tonic labyrinth reflexes and their interaction with neck reflexes in decerebrate cat. J Physiol. 1976;261:583–601.PubMedGoogle Scholar
  12. 12.
    Ezure K, Wilson VJ. Dynamics of the neck-to-forelimb reflexes in the decerebrate cat. J Neurophysiol. 1983;50:688–95.PubMedGoogle Scholar
  13. 13.
    Manzoni D, Pompeiano O, Srivastava UC, Stampacchia G. Responses of forelimb extensors to sinusoidal stimulation of macular labyrinth and neck receptors. Arch Ital Biol. 1983;121:205–14.PubMedGoogle Scholar
  14. 14.
    Zafeiriou DI. Primitive reflexes and postural reactions in the neurodevelopmental examination. Pediatr Neurol. 2004;31:1–8.PubMedCrossRefGoogle Scholar
  15. 15.
    Lund S, Broberg C. Effects of different head positions on postural sway induced by a reproducible vestibular error signal. Acta Physiol Scand. 1983;117:307–9.PubMedCrossRefGoogle Scholar
  16. 16.
    Britton TC, Day BL, Brown P, Rothwell JC, Thompson PD, Marsden CD. Postural electromyographic responses in the arm and leg following galvanic vestibular stimulation in man. Exp Brain Res. 1993;94:143–51.PubMedCrossRefGoogle Scholar
  17. 17.
    Nashner LM, Wolfsen P. Influence of head position and proprioceptive cues on short latency postural reflexes evoked by galvanic stimulation of the human labyrinth. Brain Res. 1974;67:255–68.PubMedCrossRefGoogle Scholar
  18. 18.
    Fitzpatrick R, Burke D, Gandevia SC. Task-dependent reflex responses and movement illusions evoked by galvanic vestibular stimulation in standing humans. J Physiol. 1994;478:363–72.PubMedGoogle Scholar
  19. 19.
    Mergner T, Siebold C, Schweigart G, Becker W. Human perception of horizontal trunk and head rotation in space during vestibular and neck stimulation. Exp Brain Res. 1991;85:389–404.PubMedCrossRefGoogle Scholar
  20. 20.
    Mergner T, Huber W, Becker W. Vestibular-neck interaction and transformation of sensory coordinates. J Vest Res. 1997;7:347–67.CrossRefGoogle Scholar
  21. 21.
    Peterka RJ. Sensorimotor integration in human postural control. J Neurophysiol. 2002;88:1097–118.PubMedGoogle Scholar
  22. 22.
    Mergner T, Maurer C, Peterka RJ. A multisensory posture control model of human upright stance. Prog Brain Res. 2003;171:231–50.Google Scholar
  23. 23.
    Maurer C, Margner T, Peterka RJ. Multisensory control model of human upright stance. Exp Brain Res. 2006;142:189–201.Google Scholar
  24. 24.
    Manzoni D, Pompeiano O, Andre P. Neck influences on the spatial properties of vestibulospinal reflex in decerebrate cats: role of the cerebellar anterior vermis. J Vest Res. 1998;8:283–97.CrossRefGoogle Scholar
  25. 25.
    Kammermaier S, Kleine J, Buttner U. Vestibular-neck interaction in cerebellar patients. Ann N Y Acad Sci. 2009;1164:394–9.CrossRefGoogle Scholar
  26. 26.
    Wilson VJ, Ezure K, Timerick SJ. Tonic neck reflex on the decerebrate cat: response of spinal interneurons to natural stimulation of neck and vestibular receptors. J Neurophysiol. 1984;51:567–77.PubMedGoogle Scholar
  27. 27.
    Pompeiano O, Manzoni D, Srivastava UC, Stampacchia G. Convergence and interaction of neck and macular vestibular inputs on reticulospinal neurons. Neuroscience. 1984;12:111–28.PubMedCrossRefGoogle Scholar
  28. 28.
    Kubin L, Manzoni D, Pompeiano O. Responses of lateral reticular neurons to convergent neck and macular vestibular inputs. J Neurophysiol. 1981;46:48–64.PubMedGoogle Scholar
  29. 29.
    Boyle R, Pompeiano O. Convergence and interaction of neck and macular vestibular inputs on vestibulospinal neurons. J Neurophysiol. 1981;45:852–68.PubMedGoogle Scholar
  30. 30.
    Anastasopoulos D, Mergner T. Canal-neck interaction in vestibular nuclear neurons of the cat. Exp Brain Res. 1982;46:269–80.PubMedCrossRefGoogle Scholar
  31. 31.
    Kasper J, Schor RH, Wilson VJ. Response of vestibular neurons to head rotations in vertical planes. II. Response to the neck stimulation and vestibular-neck interaction. J Neurophysiol. 1988;60:1765–78.PubMedGoogle Scholar
  32. 32.
    Mergner T, Becker W, Deecke L. Canal-neck interaction in vestibular neurons of the cat’s cerebral cortex. Exp Brain Res. 1985;61:94–108.PubMedCrossRefGoogle Scholar
  33. 33.
    Denoth F, Margherini PC, Pompeiano O, Stanojevic M. Responses of Purkinje cells of the cerebellar vermis to neck and macular vestibular inputs. Pflugers Arch. 1979;381:87–98.PubMedCrossRefGoogle Scholar
  34. 34.
    Manzoni D, Pompeiano O, Bruschini L, Andre P. Neck input modifies the reference frame for coding labyrinthine signals in the cerebellar vermis: a cellular analysis. Neuroscience. 1999;3:1095–107.CrossRefGoogle Scholar
  35. 35.
    Shaikh AG, Meng H, Angelaki DE. Multiple reference frames for motion in the primate cerebellum. J Neurosci. 2004;24:4491–7.PubMedCrossRefGoogle Scholar
  36. 36.
    Kleine JF, Guan Y, Kipiani E, Glonti L, Hoshi M, Buttner U. Trunk position influences vestibular responses of fastigial nucleus neurons in the alert monkey. J Neurophysiol. 2004;91:2090–100.PubMedCrossRefGoogle Scholar
  37. 37.
    Grasso C, Barresi M, Scattina E, Orsini P, Vignali E, Bruschini L, et al. Tuning of human vestibulospinal reflexes by leg rotation. Hum Mov Sci. 2011;30:296–313.PubMedCrossRefGoogle Scholar
  38. 38.
    Pompeiano O. Functional organization of the cerebellar projections to the spinal cord. Progr in Brain Res. 1967;25:282–321.CrossRefGoogle Scholar
  39. 39.
    Barresi M, Bruschini L, Manzoni D. Horizontal rotation of the foreleg modifies vestibular responses of vermal P-cells. Acta Physiol. 2006;188(S652, O10):185.Google Scholar
  40. 40.
    Pompeiano O, Andre P, Manzoni D. Spatiotemporal response properties of cerebellar Purkinje cells to animal displacement: a population analysis. Neurosci. 1997;81:609–26.CrossRefGoogle Scholar
  41. 41.
    Schor RH, Miller AD, Tomko DL. Responses to head tilt in cat central vestibular neurons. I. Direction of maximum sensitivity. J Neurophysiol. 1984;51:136–46.PubMedGoogle Scholar
  42. 42.
    Schor RH, Angelaki DE. The algebra of neuronal response vectors. Ann NY Acad Sci. 1992;656:190–204.PubMedCrossRefGoogle Scholar
  43. 43.
    Bush GA, Perachio AA, Angelaki DE. Encoding of head acceleration in vestibular neurons. I. Spatiotemporal response properties to linear acceleration. J Neurophysiol. 1993;69:2039–55.PubMedGoogle Scholar
  44. 44.
    Manzoni D, Andre P, Pompeiano O. Changes in gain and spatiotemporal properties of the vestibulospinal reflex after injection of a GABA-A agonist in the cerebellar anterior vermis. Ves Res. 1997;7:7–20.CrossRefGoogle Scholar
  45. 45.
    Brooks HJ, Cullen KE. Multimodal integration in rostral fastigial nucleus provides an estimate of body movement. J Neurosci. 2009;29:10499–511.PubMedCrossRefGoogle Scholar
  46. 46.
    Bruschini L, Andre P, Pompeiano O, Manzoni D. Responses of Purkinje-cells of the cerebellar anterior vermis to stimulation of vestibular and somatosensory receptors. Neuroscience. 2006;142:235–45.PubMedCrossRefGoogle Scholar
  47. 47.
    Gundappa-Sulur G, De Schutter E, Bower JM. Ascending granule cell axon: an important component of cerebellar cortical circuitry. J Comp Neurol. 1999;408:580–96.PubMedCrossRefGoogle Scholar
  48. 48.
    Llinás R, Sugimori M. Electro-physiological properties of in vitro Purkinje cell dendrites in mammalian cerebellar slices. J Physiol (London). 1980;305:197–213.Google Scholar
  49. 49.
    D’Angelo E, De Zeuwe CI. Timing plasticity in the cerebellum: focus on the granular layer. Trends Neurosci. 2009;31:30–40.CrossRefGoogle Scholar
  50. 50.
    Coulter JD, Mergner T, Pompeiano O. Effect of static tilt on cervical spinoreticular tract neurons. J Neurophysiol. 1976;39:45–62.PubMedGoogle Scholar
  51. 51.
    Kubin L, Magherini PC, Manzoni D, Pompeiano O. Responses of lateral reticular nucleus to sinusoidal rotation of neck in the decerebrate cat. Neurosci. 1981;6:1277–90.CrossRefGoogle Scholar
  52. 52.
    Ito M. The Cerebellum and Neural Control. New York: Raven; 1994.Google Scholar
  53. 53.
    Pompeiano O, Horn E, d’Ascanio P. Locus coeruleus and dorsal pontine reticular influences on the gain of vestibulospinal reflexes. Prog Brain Res. 1991;88:435–62.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  • Massimo Barresi
    • 1
  • Luca Bruschini
    • 1
  • Guido Li Volsi
    • 2
  • Diego Manzoni
    • 1
  1. 1.Department of Physiological SciencesPisa UniversityPisaItaly
  2. 2.Department of Bio-Medical Sciences, Section of PhysiologyCatania UniversityCataniaItaly

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