Specializations in the lumbosacral vertebral canal and spinal cord of birds: evidence of a function as a sense organ which is involved in the control of walking

Review

Abstract

Birds are bipedal animals with a center of gravity rostral to the insertion of the hindlimbs. This imposes special demands on keeping balance when moving on the ground. Recently, specializations in the lumbosacral region have been suggested to function as a sense organ of equilibrium which is involved in the control of walking. Morphological, electrophysiological, behavioral and embryological evidence for such a function is reviewed. Birds have two nearly independent kinds of locomotion and it is suggested that two different sense organs play an important role in their respective control: the vestibular organ during flight and the lumbosacral system during walking.

Keywords

Accessory lobes Vertebral canal Hindlimb motor system Embryonic development Lesions 

References

  1. Baumel JJ, Witmer LM (1993) Osteology. In: Baumel JJ (ed) Handbook of avian anatomy: nomina anatomica avium. Mass. Nuttal Ornithology Club, Cambridge, pp 45–132Google Scholar
  2. Biederman-Thorson M, Thorson J (1973) Rotation-compensating reflexes independent of the labyrinth and the eye. Neuromuscular correlates in the pigeon. J Comp Physiol 83:103–122CrossRefGoogle Scholar
  3. Bilo D, Bilo A (1978) Wind stimuli control vestibular and optokinetic reflexes in the pigeon. Naturwissenschaften 65:161–162CrossRefGoogle Scholar
  4. Birinyi A, Viszokay K, Weber I, Kiehn O, Antal M (2003) Synaptic targets of commissural interneurons in the lumbar spinal cord of neonatal rats. J Comp Neurol 461:429–440CrossRefPubMedGoogle Scholar
  5. Bosco G, Poppele RE (2001) Proprioception from a spinocerebellar perspective. Physiol Rev 81:539–568PubMedGoogle Scholar
  6. Cabot JB, Reiner A, Bogan N (1982) Avian bulbospinal pathways: anterograde and retrograde studies of cells of origin, funicular trajectories, and laminar terminations. In: Kuypers HGJM, Martin GF (eds) Progress in brain research: descending pathways to the spinal cord, vol 57. Elsevier, Amsterdam, pp 79–108Google Scholar
  7. De Gennaro LD (1982) The glycogen body. In: Farner DS, King JR, Parkers KC (eds) Avian biology, vol VI. Academic, New York, pp 341–371Google Scholar
  8. De Gennaro LD, Benzo CA (1978) Ultrastructural characterization of the accessory lobes of Lachi (Hofmann’s nuclei) in the nerve cord of the chick. II. Scanning and transmission electron microscopy with observations on the glycogen body. J Exp Zool 206:229–240CrossRefPubMedGoogle Scholar
  9. Delius JD, Vollrath W (1973) Rotation compensating reflexes independent of the labyrinth. Neurosensory correlates in pigeons. J Comp Physiol 83:123–134CrossRefGoogle Scholar
  10. Eide AL (1996) The axonal projections of the Hofmann nuclei in the spinal cord of the late stage chicken embryo. Anat Embryol 193:543–557CrossRefPubMedGoogle Scholar
  11. Ewald RJ (1892) Physiologische Untersuchungen ueber das Endorgan des Nervus octavus. Bergmann, WiesbadenGoogle Scholar
  12. Grillner S, Williams T, Lagerbäck P-Å (1984) The edge cell, a possible intraspinal mechanoreceptor. Science 223:500–503PubMedCrossRefGoogle Scholar
  13. Grillner S, Deliagina T, Ekeberg Ö, El Manira A, Hill RH, Lansner A, Orlovsky GN, Wallén P (1995) Neural networks controlling locomotion and body orientation in lamprey. Trends Neurosci 18:270–279CrossRefPubMedGoogle Scholar
  14. Grimm F, Reese M, Mittelstaedt H (1997) Extravestibuläre Rezeptoren zur Wahrnehmung der Richtung der Schwerkraft bei der Taube (Columba livia, Gmel. 1789). Verh ber Erkrg Zootiere 38:97–101Google Scholar
  15. Hammar I, Bannatyne BA, Maxwell DJ, Edgley SA, Jankowska E (2004) The actions of monoamines and distribution of noradrenergic and serotoninergic contacts on different subpopulations of commissural interneurons in the cat spinal cord. Eur J Neurosci 19:1305–1316PubMedCrossRefGoogle Scholar
  16. Harrison PJ, Jankowska E, Zytnicki D (1986) Lamina VIII interneurons interposed in crossed reflex pathways in the cat. J Physiol (Lond) 371:147–166Google Scholar
  17. Huber J (1936) Nerve roots and nuclear groups in the spinal cord of the pigeon. J Comp Neurol 65:43–91CrossRefGoogle Scholar
  18. Imhof G (1905) Anatomie und Entwicklungsgeschichte des Lumbalmarkes bei den Vögeln. Archiv für Mikroskopische Anatomie und Entwicklungsgeschichte 65:498–610CrossRefGoogle Scholar
  19. Jankowska E (1992) Interneuronal relay in spinal pathways from proprioceptors. Prog Neurosci 39:335–378CrossRefGoogle Scholar
  20. Jelgersma HC (1951) On the sinus lumbosacralis, spina bifida occulta, and status dysraphicus in birds. Zoologische Mededelingen uitgegeven door het Rijksmuseum van natuurlijke Historie te Leiden 31:95–106Google Scholar
  21. Kölliker A (1902) Über die oberflächlichen Nervenkerne im Marke der Vögel und Reptilien. Z wiss Zool 72:126–180Google Scholar
  22. Lachi P (1889) Alcune particolarita anatomiche del rigonfiamento sacrale nel midollo degli uccelli. Lobi accessori. Att Soc Tosc Sci Nat 10:268–295Google Scholar
  23. Milinski T, Necker R (2001) Histochemical and immunocytochemical investigations of the marginal nuclei in the spinal cord of pigeons (Columba livia). Brain Res Bull 56:15–21CrossRefPubMedGoogle Scholar
  24. Mittelstaedt H (1964) Basic control patterns of orientational homeostasis. Symp Soc Exp Biol 18:365–385PubMedGoogle Scholar
  25. Möller W (1989) Immunzytochemische Zelltypisierung des Glykogenkörpers der Vögel. Verh Anat Ges 82:979–980Google Scholar
  26. Necker R (1992) Spinal neurons projecting to anterior or posterior cerebellum in the pigeon. Anat Embryol 185:325–334CrossRefPubMedGoogle Scholar
  27. Necker R (1997) Projections of the marginal nuclei in the spinal cord of the pigeon. J Comp Neurol 377:95–104CrossRefPubMedGoogle Scholar
  28. Necker R (1999) Specializations in the lumbosacral spinal cord of birds: morphological and behavioural evidence for a sense of equilibrium. Eur J Morphol 37:211–214CrossRefPubMedGoogle Scholar
  29. Necker R (2001) Spinocerebellar projections in the pigeon with special reference to the neck region of the body. J Comp Neurol 429:403–418CrossRefPubMedGoogle Scholar
  30. Necker R (2002) Mechanosensitivity of spinal accessory lobe neurons in the pigeon. Neurosci Lett 320:53–56CrossRefPubMedGoogle Scholar
  31. Necker R (2004) Histological and immunocytochemical characterization of neurons located in the white matter of the spinal cord of the pigeon. J Chem Neuroanat 27:109–117CrossRefPubMedGoogle Scholar
  32. Necker R (2005a) Are paragriseal cells in the avian lumbosacral spinal cord displaced ventral spinocerebellar neurons? Neurosci Lett 382:56–60CrossRefGoogle Scholar
  33. Necker R (2005b) The structure and development of avian lumbosacral specializations of the vertebral canal and the spinal cord with special reference to a possible function as a sense organ of equilibrium. Anat Embryol 210:59–74CrossRefGoogle Scholar
  34. Necker R, Janßen A, Beissenhirtz T (2000) Behavioral evidence of the role of lumbosacral anatomical specializations in pigeons in maintaining balance during terrestrial locomotion. J Comp Physiol A 186:409–412CrossRefPubMedGoogle Scholar
  35. Orlovsky GN, Deliagina TG, Grillner S (1999) Neuronal control of locomotion. From mollusc to man. Oxford University Press, Oxford, 322 ppGoogle Scholar
  36. Reese M (1995) Ort und Art der extravestibulären Rezeptoren zur Wahrnehmung der Richtung der Schwerkraft bei der Taube (Columba livia, Gmel. 1789). Dissertation, University of MünchenGoogle Scholar
  37. Rosenberg J, Necker R (2002) Ultrastructural characterization of the accessory lobes of Lachi in the lumbosacral spinal cord of the pigeon with special reference to intrinsic mechanoreceptors. J Comp Neurol 447:274–285CrossRefPubMedGoogle Scholar
  38. Schroeder DM, Murray RG (1987) Specializations within the lumbosacral spinal cord of the pigeon. J Morphol 194:41–53CrossRefGoogle Scholar
  39. Singer J (1884) Zur Kenntnis der motorischen Functionen des Lendenmarks der Taube. Sitzungs-Berichte Akad Wiss Wien, Math-nat Kl 89 (III), pp 167–185Google Scholar
  40. Streeter GL (1904) The structure of the spinal cord of the ostrich. Am J Anat 3:1–27CrossRefGoogle Scholar
  41. Terni T (1926) Sui nuclei marginali del midollo spinale dei Sauropsidi. Arch Ital Anat Embriol 23:610–628Google Scholar
  42. Trendelenburg W (1906) Über die Bewegung der Vögel nach Durchschneidung der Rückenmarkswurzeln. Arch Physiol, pp 1–126Google Scholar
  43. Watterson RL (1949) Development of the glycogen body of the chick spinal cord. I. Normal morphogenesis, vasculogenesis and anatomical relationships. J Morphol 85:337–389CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  1. 1.Lehrstuhl für TierphysiologieRuhr-Universität BochumBochumGermany

Personalised recommendations