Skip to main content
SpringerLink
Log in

Distribution of choline acetyltransferase and NADPH diaphorase in the spinal cord of the pigeon

  • Original Article
  • Published:
Anatomy and Embryology Aims and scope Submit manuscript

Abstract

Acetylcholine is the neurotransmitter of somatic and autonomic motor systems of the spinal cord. However, there are also intrinsic cholinergic systems which have modulatory functions. Modulatory functions have also been assigned to nitric oxide (NO). Acetylcholine is synthesized by choline acetyltransferase and NO by nitric oxide synthase, which is a NADPH diaphorase. The distribution of both enzymes in the mammalian spinal cord is well known. However, there is a lack of comparative data in avian species. Therefore, the distribution of both enzymes in the spinal cord of the pigeon was studied using histochemical and immunohistochemical methods. Aside from somatic motor neurons and autonomic preganglionic neurons choline acetyltransferase-immunoreactivity was found throughout the spinal cord in lamina III of the superficial dorsal horn and near the central canal. The location of choline acetyltransferase-positive preganglionic neurons in the centrally located column of Terni and the lack of an intermediolateral column typical of the mammalian spinal cord can be confirmed. In lumbosacral segments the axons of centrally located cholinergic neurons crossed to the contralateral side to form a tract in the ventral funiculus, which then innervates the contralateral grey substance. A dense band of NADPH diaphorase staining was found in lamina II and in centrally located neurons of all segments. Part of the centrally located neurons double-labelled for choline acetyltransferase and NADPH diaphorase. In contrast to mammals, preganglionic neurons labelled only weakly for NADPH diaphorase. Altogether, despite the divergent evolution of both classes of vertebrate intrinsic modulatory choline acetyltransferase and NADPH diaphorase systems of birds seem to be largely similar to those of the mammalian spinal cord.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1A–D
Fig. 2A, B
Fig. 3A, B
Fig. 4A–C
Fig. 5A–C
Fig. 6A–C
Fig. 7A–C
Fig. 8A, B
Fig. 9
Fig. 10
Fig. 11
Fig. 12
Fig. 13

Similar content being viewed by others

References

  • Aimi Y, Fujimura M, Vincent SR, Kimura H (1991) Localization of NADPH-diaphorase-containing neurons in sensory ganglia of the rat. J Comp Neurol 306:382–392

    CAS  PubMed  Google Scholar 

  • Atoji Y, Yamamoto Y, Suzuki Y (2001) Distribution of NADPH diaphorase-containing neurons in the pigeon central nervous system. J Chem Neuroanat 21:1–22

    Article  CAS  PubMed  Google Scholar 

  • Barber RP, Phelps PE, Houser CR, Crawford GD, Salvaterra PM, Vaughn JE (1984) The morphology and distribution of neurons containing choline acetyltransferase in the adult rat spinal cord: an immunocytochemical study. J Comp Neurol 229:329–346

    CAS  PubMed  Google Scholar 

  • Borges LF, Iversen SD (1986) Topography of choline acetyltransferase immunoreactive neurons and fibers in the rat spinal cord. Brain Res 362:140–148

    CAS  PubMed  Google Scholar 

  • Brinkmann R, Martin AH (1973) A cytoarchitectonic study of the spinal cord of the domestic fowl Gallus gallus domesticus. I. Brachial region. Brain Res 56:43–62

    Article  PubMed  Google Scholar 

  • Brown AG (ed) (1981) Organization in the Spinal Cord. Springer, Berlin Heidelberg New York

  • Brüning G (1992) Localization of NADPH diaphorase, a histochemical marker for nitric oxide synthase, in the mouse spinal cord. Acta Histochem 93:397–401

    PubMed  Google Scholar 

  • Brüning G (1993) Localization of NADPH-diaphorase in the brain of the chicken. J Comp Neurol 334:192–208

    PubMed  Google Scholar 

  • Cabot JB, Bogan N (1987) Light microscopic observations on the morphology of sympathetic preganglionic neurons in the pigeon, Columba livia. Neurosci 20:467–486

    Article  CAS  Google Scholar 

  • De Gennaro LD (1982) The glycogen body. In: Farner DS, King JR, Parkers KC (eds) Avian Biology, vol 4. Academic Press, New York, pp 341–371

  • Doone GV, Pelissier N, Manchester T, Vizzard MA (1999) Distribution of NADPH-d and nNOS-IR in the thoracolumbar and sacrococcygeal spinal cord of the guinea pig. J Autonomic Nerv Syst 77:98–113

    Article  CAS  Google Scholar 

  • Dun NJ, Dun SL, Wu SY, Förstermann U, Schmidt HHHW, Tseng LF (1993) Nitric oxide synthase immunoreactivity in the rat, mouse, cat, and squirrel monkey spinal cord. Neurosci 54:845–857

    CAS  PubMed  Google Scholar 

  • Honda CN (1985) Visceral and somatic afferent convergence onto neurons near the central canal in the sacral spinal cord of the cat. J Neurophysiol 53:1059–1078

    CAS  PubMed  Google Scholar 

  • Hosoya Y, Yaginuma H, Okado N, Kohno K (1992) Morphology of sympathetic preganglionic neurons innervating the superior cervical ganglion in the chicken: an immunohistochemical study using retrograde labeling of cholera toxin subunit B. Exp Brain Res 89:478–483

    CAS  PubMed  Google Scholar 

  • Huber JF (1936) Nerve roots and nuclear groups in the spinal cord of the pigeon. J Comp Neurol 65:43–91

    Google Scholar 

  • Ichikawa T, Shimizu T (1998) Organization of choline acetyltransferase - containing structures in the cranial nerve motor nuclei and spinal cord of the monkey. Brain Res 779:96–103

    Article  CAS  PubMed  Google Scholar 

  • Kluchová D, Rybárová S, Miklošová M, Lovásová K, Schmidtová K, Dorko F (2001) Comparative analysis of NADPH-diaphorase positive neurons in the rat, rabbit and pheasant thoracic spinal cord. A histochemical study. Eur J Histochem 45:239–248

    PubMed  Google Scholar 

  • Kölliker A (1902) Über die oberflächlichen Nervenkerne im Marke der Vögel und Reptilien. Z Wiss Zool 72:126–180

    Google Scholar 

  • Lachi P (1889) Alcune particolarità anatomiche del regonfiamento sacrale nel midollo degli uccelli. Att Soc Tosc Sci Nat 10:268–295

    Google Scholar 

  • Leonard RB, Cohen DH (1975) A cytoarchotectonic analysis of the spinal cord of the pigeon (Columba livia). J Comp Neurol 163:159–180

    CAS  PubMed  Google Scholar 

  • MacDonald RL, Cohen DH (1970) Cells of origin of sympathetic pre- and postganglionic cardioacceleratory fibers in the pigeon. J Comp Neurol 140:343–358

    CAS  PubMed  Google Scholar 

  • Maršala J, Maršala M, Vanický I, Taira Y (1999) Localization of NADPHd-exhibiting neurons in the spinal cord of the rabbit. J Comp Neurol 406:263–284

    Article  PubMed  Google Scholar 

  • Medina L, Reiner A (1994) Distribution of choline acetyltransferase immunoreactivity in the pigeon brain. J Comp Neurol 342:497–537

    CAS  PubMed  Google Scholar 

  • Mesulam M-M, Mufson EJ, Levey AI, Wainer BH (1984) Atlas of cholinergic neurons in the forebrain and upper brainstem of the macaque based on monoclonal choline acetyltransferase immunohistochemistry and acetylcholinesterase histochemistry. Neurosci 12:669–686

    Article  CAS  Google Scholar 

  • Milinski T, Necker R (2001) Histochemical and immunocytochemical investigations of the marginal nuclei in the spinal cord of pigeons (Columba livia). Brain Res Bull 56:15–21

    Article  CAS  PubMed  Google Scholar 

  • Mizukawa K, McGeer PL, Tago H, Peng JH, McGeer EH, Kimura H (1986) The cholinergic system of the human hindbrain studied by choline acetyltransferase immunohistochemistry and acetylcholineesterase histochemistry. Brain Res 379:39–55

    Article  CAS  PubMed  Google Scholar 

  • Nahin RL, Madsen AM, Giesler Jr GJ (1983) Anatomical and physiological studies of the gray matter surrounding the spinal cord central canal. J Comp Neurol 220:321–335

    CAS  PubMed  Google Scholar 

  • Necker R (1985) Projection of a cutaneous nerve to the spinal cord of the pigeon. II. Responses of dorsal horn neurons. Exp Brain Res 59:344–352

    CAS  PubMed  Google Scholar 

  • Necker R (1992) Spinal neurons projecting to anterior or posterior cerebellum in the pigeon. Anat Embryol 185:325–334

    CAS  PubMed  Google Scholar 

  • Necker R (1997) Projections of the marginal nuclei in the spinal cord of the pigeon. J Comp Neurol 377:95–104

    Article  CAS  PubMed  Google Scholar 

  • Necker R (1999) Specializations in the lumbosacral spinal cord of birds: morphological and behavioural evidence for a sense of equilibrium. Eur J Morphol 31:211–214

    Article  Google Scholar 

  • Ness TJ, Gebhart GF (1987) Characterization of neuronal responses to noxious visceral and somatic stimuli in the medial lumbosacral spinal cord of the rat. J Neurophysiol 57:1867–1892

    CAS  PubMed  Google Scholar 

  • Ohmori Y, Watanabe T, Fujioka T (1984) Location of parasympathetic preganglionic neurons in the sacral spinal cord of the domestic fowl. Jap J Zootech Sci 55:792–794

    Google Scholar 

  • Phelps PE, Barber RP, Houser CR, Crawford GD, Salvaterra PM, Vaughn JE (1984) Post-natal development of neurons containing choline acetyltransferase in rat spinal cord: an immunocytochemical study. J Comp Neurol 229:347–361

    CAS  PubMed  Google Scholar 

  • Ribeiro-da-Silva A, Cuello AC (1990) Choline acetyltransferase-immunoreactivity profiles are presynaptic to primary sensory fibers in the rat superficial dorsal horn. J Comp Neurol 295:370–384

    CAS  PubMed  Google Scholar 

  • Scherer-Singler U, Vincent SR, Kimura H, McGeer EG (1983) Demonstration of unique population of neurons with NADPH-diaphorase histochemistry. J Neurosci Methods 9:229–234

    CAS  PubMed  Google Scholar 

  • Sherriff FE, Henderson Z (1994) A cholinergic propriospinal innervation of the rat spinal cord. Brain Res 634:150–154

    PubMed  Google Scholar 

  • Spike RC, Todd AJ, Johnston HM (1993) Coexistence of NADPH diaphorase with GABA, glycine, and acetylcholine in rat spinal cord. J Comp Neurol 335:320–333

    CAS  PubMed  Google Scholar 

  • Tago H, McGeer PL, McGeer EG, Akiyama H, Hersh LB (1989) Distribution of choline acetyltransferase immunopositive structures in the rat brainstem. Brain Res 495:271–297

    Article  CAS  PubMed  Google Scholar 

  • Terni T (1923) Ricerche anatomiche sul sistema nervoso autonomo degli uccelli. Arch Ital die Anat e di Embriol 20:433–510

    Google Scholar 

  • Valtschanoff JG, Weinberg RJ, Rustioni A (1992) NADPH diaphorase in the spinal cord of rats. J Comp Neurol 321:209–222

    CAS  PubMed  Google Scholar 

  • Vincent SR, Kimura H (1992) Histochemical mapping of nitric oxide synthase in the rat brain. Neurosci 46:755–784

    CAS  PubMed  Google Scholar 

  • Vincent SR, Reiner PB (1987) The immunohistochemical localization of choline acetyltransferase in the cat brain. Brain Res Bull 18:371–415

    Article  CAS  PubMed  Google Scholar 

  • Vizzard MA, Erickson K, De Groat WC (1997) Localization of NADPH diaphorase in the thoracolumbar and sacrococcygeal spinal cord of the dog. J Autonomic Nerv Syst 64:128–142

    Article  CAS  Google Scholar 

  • Wall PD, Kerr BJ, Ramer MS (2002) Primary afferent input to and receptive field properties of cells in rat lumbar area X. J Comp Neurol 449:298–306

    Article  PubMed  Google Scholar 

  • Wetts R, Vaughn JE (1994) Choline acetyltransferase and NADPH diaphorase are co-expressed in rat spinal cord neurons. Neurosci 63:1117–1124

    Article  CAS  Google Scholar 

  • Woodbury JC (1992) Physiological studies of cutaneous inputs to dorsal horn laminae I-IV of adult chickens. J Neurophysiol 67:241–254

    CAS  PubMed  Google Scholar 

  • Zhou Y, Mack POP, Ling EA (1998) Localization of nicotinamide adenine dinucleotide phosphate-diaphorase reactivity and nitric oxide synthase immunoreactivity in the lumbosacral dorsal root ganglia in guinea pigs. J Brain Res 39:119–127

    CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by a grant from the Deutsche Forschungsgemeinschaft (grant number Ne 268/5). The excellent technical assistance by Silvia Schweer is gratefully acknowledged. Thanks are also due to Harald Necker for checking the correctness of the English language.

Author information

Authors and Affiliations

  1. Lehrstuhl für Tierphysiologie, Ruhr-Universität Bochum, 44780 , Bochum, Germany

    R. Necker

Authors
  1. R. Necker
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to R. Necker.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Necker, R. Distribution of choline acetyltransferase and NADPH diaphorase in the spinal cord of the pigeon. Anat Embryol 208, 169–181 (2004). https://doi.org/10.1007/s00429-004-0383-4

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00429-004-0383-4

Keywords

Search

Navigation