Skip to main content
SpringerLink
Log in

Observations on the development of ascending spinal pathways in the clawed toad, Xenopus laevis

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

Summary

The development of ascending spinal pathways has been studied in the clawed toad, Xenopus laevis. From stage 35 (hatching) on, HRP was applied at the spinomedullary border or to the area of the developing dorsal column nucleus, to analyze the development of ascending spinal pathways to the brain stem, and the onset and development of spinal projections to the dorsal column nucleus, respectively. Several populations of spinal neurons with ascending projections at least as far as the spinomedullary border were successively labeled. In early stages ascending spinal projections arise from Rohon-Beard cells and ascending interneuron populations located at the margin of the gray and white matter, i.e., marginal neurons. The ascending interneuron populations could be characterized as dorsolateral commissural and commissural interneurons projecting contralaterally, and as ipsilaterally projecting ascending interneurons and distinguished by Roberts and co-workers. Such a subdivision could be made until about stage 57. Then these ascending and commissural interneuron populations become intermingled with other populations of ascending tract neurons. Rohon-Beard cells could be labeled, more or less shrunken, until stage 55. Around stage 48 (at the time of the appearance of the limb buds) spinal ganglion cells could be labeled from the spinomedullary border and the developing dorsal column nucleus. At stage 48 such ascending primary spinal afferents were found to arise only from non-limbbud-innervating dorsal root ganglia. Gradually also the limb-bud-innervating ganglia give rise to ascending collaterals, so that by stage 53 all spinal ganglia send ascending collaterals to the brain stem. The number of cells of origin of secondary spinal afferents to the brain stem increases during development, and their distribution becomes more extensive. Particularly impressive is a large population of neurons in the dorsal horn projecting ipsilaterally to the dorsal column nucleus. Part of the latter population represents non-primary spinal afferents to the dorsal column nucleus.

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

Similar content being viewed by others

References

  • Adams JC (1981) Heavy metal intensification of DAB-based HRP reaction product. J Histochem Cytochem 29:775

    Google Scholar 

  • Altman J, Bayer SA (1984) The development of the rat spinal cord. Adv Anat Embryol Cell Biol, vol 85. Springer, Berlin Heidelberg

    Google Scholar 

  • Altman JS, Dawes EA (1983) A cobalt study of medullary sensory projections from the lateral line nerves, associated cutaneous nerves, and the VIIIth nerve in Xenopus laevis. J Comp Neurol 213:310–326

    Google Scholar 

  • Angaut-Petit D (1975a) The dorsal column system. I. Existence of long ascending postsynaptic fibres in the cat's fasciculus gracilis. Exp Brain Res 22:457–470

    Google Scholar 

  • Angaut-Petit D (1975b) The dorsal column system. II. Functional properties and bulbar relay of the postsynaptic fibres of the cat's fasciculus gracilis. Exp Brain Res 22:471–493

    Google Scholar 

  • Antal M, Tornai I, Székely G (1980) Longitudinal extent of dorsal root fibres in the spinal cord and brain stem of the frog. Neuroscience 5:1311–1322

    Google Scholar 

  • Asanuma C, Ohkawa R, Stanfield BB, Cowan WM (1988) Observations on the development of certain ascending inputs to the thalamus in rats. I. Postnatal development. Dev Brain Res 41:159–170

    Google Scholar 

  • Barron DH (1944) The early development of the sensory and internuncial cells in the spinal cord of the sheep. J Comp Neurol 81:193–225

    Google Scholar 

  • Bennett GJ, Nishikawa N, Lu G-W, Hoffert MJ, Dubner R (1984) The morphology of dorsal column postsynaptic spinomedullary neurons in the cat. J Comp Neurol 224:568–578

    Google Scholar 

  • de Boer-van Huizen R (1989) Polyacrylamide als inbedmedium voor vries- of vibratoomcoupes. Histotechniek 8:148–152

    Google Scholar 

  • Burstein R, Cliffer KD, Giesler Jr GJ (1987) Direct somatosensory projections from the spinal cord to the hypothalamus and telencephalon. J Neurosci 7:4159–4164

    Google Scholar 

  • Clarke JDW, Hayes BP, Hunt SP, Roberts A (1984) Sensory physiology, anatomy and immunohistochemistry of Rohon-Beard neurones in embryos of Xenopus laevis. J Physiol 348:511–525

    Google Scholar 

  • Clarke JDW, Tonge D, Holder N (1986) Stage dependent restoration of sensory dorsal columns following spinal cord transection in anuran tadpoles. Proc R Soc Lond [Biol] 227:67–82

    Google Scholar 

  • Cliffer KD, Giesler Jr GJ (1989) Postsynaptic dorsal column pathway of the rat. III. Distribution of ascending afferent fibers. J Neurosci 9:3146–3168

    Google Scholar 

  • Dale N, Ottersen OP, Roberts A, Storm-Mathisen J (1986) Inhibitory neurones of a motor pattern generator in Xenopus revealed by antibodies to glycine. Nature 324:255–257

    Google Scholar 

  • Dale N, Roberts A, Ottersen OP, Storm-Mathisen J (1987a) The morphology and distribution of ‘Kolmer-Agduhr cells’, a class of cerebrospinal-fluid contacting neurons revealed in the frog embryo spinal cord by GABA immunocytochemistry. Proc R Soc Lond [Biol] 232:193–203

    Google Scholar 

  • Dale N, Roberts A, Ottersen OP, Storm-Mathisen J (1987b) The development of a population of spinal neurons and their axonal projections revealed by GABA immunocytochemistry in frog embryos. Proc R Soc Lond [Biol] 232:205–215

    Google Scholar 

  • Deuchar EM (1975) Xenopus: the South African clawed frog. Wiley, London New York

    Google Scholar 

  • Ebbesson SOE (1969) Brain stem afferents from the spinal cord in a sample of reptilian and amphibian species. Ann NY Acad Sci 167:80–102

    Google Scholar 

  • Ebbesson SOE (1976) Morphology of the spinal cord. In: Llinás R, Precht W (eds) Frog Neurobiology. Springer, New York, pp 679–706

    Google Scholar 

  • Funke K (1988) Spinal projections to the dorsal column nuclei in pigeons. Neurosci Lett 91:295–300

    Google Scholar 

  • Funke K, Necker R (1986) Cells of origin of ascending pathways in the spinal cord of the pigeon. Neurosci Lett 71:25–30

    Google Scholar 

  • Forehand CJ, Farel PB (1982a) Spinal cord development in anuran larvae. I. Primary and secondary neurons. J Comp Neurol 209:386–394

    Google Scholar 

  • Forehand CJ, Farel PB (1982b) Spinal cord development in anural larvae. II. Ascending and descending pathways. J Comp Neurol 209:395–408

    Google Scholar 

  • Frank E, Westerfield M (1983) Development of sensory-motor synapses in the spinal cord of the frog. J Physiol (Lond) 343:593–610

    Google Scholar 

  • Gaupp E (1896) A Ecker's und R Wiedersheim's Anatomie des Frosches. Vieweg, Braunschweig

    Google Scholar 

  • Giesler Jr, GJ, Nahin RL, Madsen AM (1984) Postsynaptic dorsal column pathway of the rat. I. Anatomical studies. J Neurophysiol 51:260–275

    Google Scholar 

  • Hausen P, Dreyer C (1981) The use of polyacrylamide as an embedding medium for immunohistochemical studies of embryonic tissues. Stain Technol 56:287–293

    Google Scholar 

  • Holder N, Clarke JDW, Tonge D (1987) Pathfinding by dorsal column axons in the spinal cord of the frog tadpole. Development 99:577–587

    Google Scholar 

  • Honig MG (1982) The development of sensory projection patterns in embryonic chick hind limb. J Physiol (Lond) 330:175–202

    Google Scholar 

  • Hughes A (1957) The development of the primary sensory system in Xenopus laevis (Daudin). J Anat 91:323–338

    Google Scholar 

  • Hughes A, Tschumi PA (1958) The factors controlling the development of the dorsal root ganglia and ventral horn in Xenopus laevis (Daud.). J Anat 92:498–527

    Google Scholar 

  • Jacobson M, Huang S (1985) Neurite outgrowth traced by means of horseradish peroxidase inherited from neuronal ancestral cells in frog embryos. Dev Biol 110:102–113

    Google Scholar 

  • Johnson JI, Hamilton TC, Hsung JC, Ulinski PS (1972) Gracile nucleus absent in adult opossums after leg removal in infancy. Brain Res 38:421–424

    Google Scholar 

  • Killackey HP, Dawson DR (1989) Expansion of the central hindpaw representation following fetal forelimb removal in the rat. Eur J Neurosci 1:210–221

    Google Scholar 

  • Lamborghini JE (1980) Rohon-Beard cells and other large neurons in Xenopus embryos originate during gastrulation. J Comp Neurol 189:329–333

    Google Scholar 

  • Lamborghini JE (1987) Disappearance of Rohon-Beard neurons from the spinal cord of larval Xenopus laevis. J Comp Neurol 264:47–55

    Google Scholar 

  • van der Linden JAM, ten Donkelaar HJ (1987) Observations on the development of cerebellar afferents in Xenopus laevis. Anat Embryol 176:431–439

    Google Scholar 

  • van der Linden JAM, ten Donkelaar HJ, de Boer-van Huizen R (1988) Development of spinocerebellar afferents in the clawed toad, Xenopus laevis. J Comp Neurol 277:41–52

    Google Scholar 

  • Liuzzi FJ, Beattie MS, Bresnahan JC (1985) The development of the relationship between dorsal root afferents and motoneurons in the larval bullfrog spinal cord. Brain Res Bull 14:377–392

    Google Scholar 

  • Lowe DA, Russell IJ (1982) The central projections of lateral line and cutaneous sensory fibres (VII and X) in Xenopus laevis. Proc R Soc Lond [Biol] 216:279–297

    Google Scholar 

  • Martin GF, Culberson JL, Hazlett JC (1983) Observations on the early development of ascending spinal pathways-studies using the North American opossum. Anat Embryol 166:191–207

    Google Scholar 

  • Martin GF, Cabana T, Hazlett JC, Ho R, Waltzer R (1987) Development of brain stem and cerebellar projections to the diencephalon with notes on thalamocortical projections: studies in the North American opossum. J Comp Neurol 260:186–200

    Google Scholar 

  • Matesz C, Székely G (1978) The motor column and sensory projections of the branchial cranial nerves in the frog. J Comp Neurol 178:157–176

    Google Scholar 

  • Mehler WR (1969) Some neurological species differences — a posterori. Ann NY Acad Sci 167:424–468

    Google Scholar 

  • Mesdag TM (1909) Bijdrage tot de ontwikkelingsgeschiedenis van de structuur der hersenen bij de kip. Thesis, University of Groningen

  • van Mier P, ten Donkelaar HJ (1984) Early development of descending pathways from the brain stem to the spinal cord in Xenopus laevis. Anat Embryol 170:295–306

    Google Scholar 

  • van Mier P, ten Donkelaar HJ (1988) The development of primary afferents to the lumbar spinal cord in Xenopus laevis. Neurosci Lett 84:35–40

    Google Scholar 

  • Millard N, Robinson JT (1955) Dissection of the spiny dogfish and the platanna. Maskew Miller, Cape Town

    Google Scholar 

  • Muntz L (1964) Neuromuscular foundations of behaviour in early stages of Xenopus. PhD thesis, Bristol University

  • Neary TJ, Wilczynski W (1977) Ascending thalamic projections from the obex region in ranid frogs. Brain Res 138:529–533

    Google Scholar 

  • Nieuwkoop PD, Faber J (1967) Normal table of Xenopus laevis (Daudin). North-Holland, Amsterdam

    Google Scholar 

  • Nikundiwe AM, de Boer-van Huizen R, ten Donkelaar HJ (1982) Dorsal root projections in the clawed toad (Xenopus laevis) as demonstrated by anterograde labeling with horseradish peroxidase. Neuroscience 7:2089–2103

    Google Scholar 

  • Nishikawa K, Wasserzug R (1988) Morphology of the caudal spinal cord in Rana (Ranidae) and Xenopus (Pipidae) tadpoles. J Comp Neurol 269:193–202

    Google Scholar 

  • Nordlander RH (1984) Developing descending neurons of the early Xenopus tail spinal cord. J Comp Neurol 228:117–127

    Google Scholar 

  • Nordlander RH (1987) Axonal growth cones in the developing amphibian spinal cord. J Comp Neurol 263:485–496

    Google Scholar 

  • Nordlander RH, Awwiller DM, Cook H (1988) Dorsal roots are absent from the tail of larval Xenopus. Brain Res 440:391–395

    Google Scholar 

  • Petit D (1972) Postsynaptic fibres in the dorsal columns and their relay in the nucleus gracilis. Brain Res 48:380–384

    Google Scholar 

  • Ramón y Cajal S (1911) Histologie du système nerveux de l'homme et des vertébrés. Maloine, Paris

    Google Scholar 

  • Retzius G (1898) Zur Frage von der Endigungsweise der peripherischen sensiblen Nerven. Biol Untersuch 8:114

    Google Scholar 

  • Roberts A (1988) The early development of neurons in Xenopus embryos revealed by transmitter immunocytochemistry for serotonin, GABA and glycine. In: Pollack ED, Bibb HD (eds) Developmental Neurobiology of the Frog. Liss, New York, pp 191–205

    Google Scholar 

  • Roberts A (1989) The neurons that control axial movements in a frog embryo. Am Zool 29:53–63

    Google Scholar 

  • Roberts A, Clarke JDW (1982) The neuroanatomy of an amphibian embryo spinal cord. Philos Trans R Soc Lond [Biol] 296:195–212

    Google Scholar 

  • Roberts A, Hayes BP (1977) The anatomy and function of ‘free’ nerve endings in an amphibian skin sensory system. Proc R Soc Lond [Biol] 196:415–429

    Google Scholar 

  • Roberts A, Sillar KT (1990) Characterization and function of spinal excitatory interneurons with commissural projections in Xenopus laevis embryos. Eur J Neurosci 2:1051–1062

    Google Scholar 

  • Roberts A, Smyth D (1974) The development of a dual touch sensory system in embryos of the amphibian Xenopus laevis. J Comp Physiol 88:31–42

    Google Scholar 

  • Roberts A, Dale N, Ottersen OP, Storm-Mathisen J (1987) The early development of neurons with GABA immunoreactivity in the CNS of Xenopus laevis embryos. J Comp Neurol 261:435–449

    Google Scholar 

  • Roberts A, Dale N, Ottersen OP, Storm-Mathisen J (1988) Development and characterization of commissural interneurons in the spinal cord of Xenopus laevis embryos revealed by antibodies to glycine. Development 103:447–461

    Google Scholar 

  • Rustioni A (1973) Non-primary afferents to the nucleus gracilis from the lumbar cord of the cat. Brain Res 51:81–95

    Google Scholar 

  • Rustioni A, Kaufman AB (1977) Identification of cells of origin of non-primary afferents to the dorsal column nuclei of the cat. Exp Brain Res 27:1–14

    Google Scholar 

  • Rustioni A, Hayes NL, O'Neill S (1979) Dorsal column nuclei and ascending spinal afferents in macaques. Brain 102:95–125

    Google Scholar 

  • Smith CL (1983) The development and postnatal organization of primary afferent projections to the rat thoracic spinal cord. J Comp Neurol 220:29–43

    Google Scholar 

  • Smith CL, Frank E (1988a) Specificity of sensory projections to the spinal cord during development in bullfrogs. J Comp Neurol 269:96–108

    Google Scholar 

  • Smith CL, Frank E (1988b) Peripheral specification of sensory connections in the spinal cord. Brain Behav Evol 31:227–242

    Google Scholar 

  • Taylor AC, Kollros JJ (1946) Stages in the normal development of Rana pipiens larvae. Anat Rec 94:7–23

    Google Scholar 

  • Tosney KW, Landmesser LT (1985) Development of the major pathways for neurite outgrowth in the chick hindlimb. Dev Biol 109:193–214

    Google Scholar 

  • Uddenberg N (1968) Functional organization of long, second-order afferents in the dorsal funiculus. Exp Brain Res 4:377–382

    Google Scholar 

  • Urbán L, Székely G (1982) The dorsal column nuclei of the frog. Neuroscience 7:1187–1196

    Google Scholar 

  • Vaughn JE, Grieshaber JA (1973) Morphological investigation of an early reflex pathway in developing rat spinal cord. J Comp Neurol 148:177–210

    Google Scholar 

  • Wentworth LE (1984) The development of the cervical spinal cord of the mouse embryo. II. A Golgi analysis of sensory, commissural, and association cell differentiation. J Comp Neurol 222:96–115

    Google Scholar 

  • Willis WD, Coggeshall RE (1978) Sensory mechanisms of the spinal cord. Wiley, Chichester New York

    Google Scholar 

  • Windle WF (1932) The neurofibrillar structure of the five-and-one-half millimeter cat embryo. J Comp Neurol 55:315–331

    Google Scholar 

  • Windle WF, Baxter RE (1936) Development of reflex mechanisms in the spinal cord of albino rat embryos. Correlation between structure and function and comparisons with the cat and the chick. J Comp Neurol 63:189–209

    Google Scholar 

  • Windle WF, Orr DW (1934) The development of behavior in chick embryos: spinal cord structure correlated with early somatic mobility. J Comp Neurol 60:287–307

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Anatomy and Embryology, University of Nijmegen, NL-6500, HB Nijmegen, The Netherlands

    H. J. ten Donkelaar & R. de Boer-van Huizen

Authors
  1. H. J. ten Donkelaar
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. R. de Boer-van Huizen
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

ten Donkelaar, H.J., de Boer-van Huizen, R. Observations on the development of ascending spinal pathways in the clawed toad, Xenopus laevis . Anat Embryol 183, 589–603 (1991). https://doi.org/10.1007/BF00187908

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00187908

Key words

Search

Navigation