Skip to main content
Log in

Propriospinal neurons with ascending collaterals to the dorsal medulla, the thalamus and the tectum: a retrograde fluorescent double-labeling study of the cervical cord of the rat

  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Summary

Branching neurons with descending propriospinal collaterals and ascending collaterals to the dorsal medulla, the thalamus and the tectum were studied in the rat's cervical spinal cord (C1–C8), using the retrograde fluorescent double-labeling technique: Diamidino Yellow Dihydrochloride (DY) was injected in the cord at T2, True Blue (TB) was injected in the brain stem. DY-labeled descending propriospinal neurons were present in all laminae, except lamina IX. They were concentrated in lamina I, laminae IV to VIII, and in the lateral spinal nucleus, LSN. TB-labeled neurons projecting to the dorsal medulla were concentrated in lamina IV and the medial parts of laminae V and VI (probably representing postsynaptic dorsal column — PSDC — neurons), but were also present in lamina I, the LSN, the lateral dorsal horn, and in laminae VII and VIII. DY-TB double-labeled neurons giving rise to both a descending propriospinal collateral and an ascending collateral to the dorsal medulla were intermingled with the TB single-labeled neurons. About 4% of the descending propriospinal neurons gave rise to an ascending collateral to the dorsal column nuclei; these double-labeled cells constitute a sizable fraction (10%) of the PSDC neurons. TB-labeled spinothalamic and spinotectal neurons were located in lamina I, the lateral cervical nucleus (LCN), the LSN, the lateral lamina V, lamina VII and VIII, lamina X and in the spinal extensions of the dorsal column nuclei, predominantly contralateral to the TB injections. DY-TB double-labeled neurons were present throughout C1–C8 in the LSN, lateral lamina V, lamina VIII, ventromedial lamina VII, and lamina X. Only very few were observed in lamina I and the LCN, and none in the spinal extensions of the dorsal column nuclei. The double-labeled neurons constituted only a minor fraction of all labeled neurons; 3–5% of the spinothalamic neurons and about 1–7% of the spinotectal neurons were double-labeled. Conversely, only about 1% of the labeled descending propriospinal neurons gave rise to an ascending spinothalamic collateral, and even fewer (0.1 to 0.6%) to a collateral to the dorsal midbrain. The LSN displayed the highest relative content of branching neurons. Up to 20% of its ascending spinothalamic and spinotectal neurons and up to 8% of its descending propriospinal neurons were found to be branching neurons, indicating that the LSN constitutes an unique cell-group in the rat spinal cord.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Baker ML, Giesler GJ Jr (1984) Anatomical studies of the spinocervical tract of the rat. Somatosens Res 2:1–18

    Google Scholar 

  • Beitz AJ (1982) The organization of afferent projections to the midbrain periaqueductal gray of the rat. Neuroscience 7:133–159

    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 

  • Bentivoglio M, Rustioni A (1986) Corticospinal neurons with branching axons to the dorsal column nuclei in the monkey. J Comp Neurol 253:260–276

    Google Scholar 

  • Brichta AM, Grant G (1985) Cytoarchitectural organization of the spinal cord. In: Paxinos G (ed) The rat nervous system. Academic Press Australia, pp 293–301

    Google Scholar 

  • Brown AG, Fyffe REW (1981) Form and function of dorsal horn neurons with axons ascending the dorsal columns in cat. J Physiol (London) 321:31–47

    Google Scholar 

  • Brown AG, Brown PB, Fyffe REW, Pubols LM (1983) Receptive field organization and response properties of spinal neurones with axons ascending the dorsal columns in the cat. J Physiol (London) 337:575–588

    Google Scholar 

  • Chaouch A, Menétrey D, Binder D, Besson JM (1983) Neurons at the origin of the medial component of the bulbopontine spinoreticular tract in the rat: an anatomical study using horseradish peroxidase retrograde transport. J Comp Neurol 214:309–320

    Google Scholar 

  • Craig AD Jr, Tapper DN (1978) Lateral cervical nucleus in the cat: functional organization and characteristics. J Neurophysiol 41:1511–1534

    Google Scholar 

  • Flink R, Svensson BA (1986) Fluorescent double-labelling study of ascending and descending neurones in the feline lateral cervical nucleus. Exp Brain Res 62:479–485

    Google Scholar 

  • Giesler GJ Jr, Menétrey D, Basbaum AI (1979a) Differential origins of spinothalamic tract projections to medial and lateral thalamus in the rat. J Comp Neurol 184:107–126

    Google Scholar 

  • Giesler GJ Jr, Urea G, Cannon JT, Liebeskind JC (1979b) Response properties of neurons of the lateral cervical nucleus in the rat. J Comp Neurol 186:65–78

    Google Scholar 

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

    Google Scholar 

  • Giesler GJ Jr, Elde RP (1985) Immunocytochemical studies of the peptidergic content of fibers and terminals within the lateral spinal and lateral cervical nuclei. J Neurosci 5:1833–1841

    Google Scholar 

  • Granum SL (1986) The spinothalamic system of the rat. I. Location of cells of origin. J Comp Neurol 247:159–180

    Google Scholar 

  • Gulley RL (1973) Golgi studies of the nucleus gracilis in the rat. Anat Rec 177:325–342

    Google Scholar 

  • Gwyn DG, Waldron HA (1968) A nucleus in the dorsolateral funiculus of the spinal cord of the rat. Brain Res 10:342–351

    Google Scholar 

  • Gwyn DG, Waldron HA (1969) Observations on the morphology of a nucleus in the dorsolateral funiculus of the spinal cord of the guinea-pig, rabbit, ferret and cat. J Comp Neurol 136:233–236

    Google Scholar 

  • Huisman AM, Kuypers HGJM, Verburgh CA (1982) Differences in collateralization of descending spinal pathways from red nucleus and other brain stem cell groups in cat and monkey. In: Kuypers HGJM, Martin GF (eds) Descending pathways to the spinal cord. Progr Brain Res 57:185–217

  • Jankowska E, Rastad J, Zarzecki P (1979) Segmental and supraspinal input to cells of origin of non-primary afferent fibres in the feline dorsal columns. J Physiol (London) 290:185–200

    Google Scholar 

  • Kamogawa H, Bennett GJ (1986) Dorsal column postsynaptic neurons in the cat are excited by myelinated nociceptors. Brain Res 364:386–390

    Google Scholar 

  • Keizer K, Kuypers HGJM, Huisman AM, Dann O (1983) Diamidino Yellow Dihydrochloride (DY.2HCl): a new fluorescent retrograde neuronal tracer which migrates only very slowly out of the cell. Exp Brain Res 51:179–191

    Google Scholar 

  • Kemplay SK, Webster KE (1986) A qualitative and quantitative analysis of the distribution of cells in the spinal cord and spinomedullary junction projecting to the thalamus of the rat. Neuroscience 17:769–789

    Google Scholar 

  • Kevetter GA, Willis WD (1983) Collaterals of spinothalamic cells in the rat. J Comp Neurol 215:453–464

    Google Scholar 

  • Kuypers HGJM, Tuerk JD (1964) The distribution of the cortical fibres in the nuclei cuneatus and gracilis in the cat. J Anat 98:143–162

    Google Scholar 

  • Kuypers HGJM, Huisman AM (1983) Fluorescent neuronal tracers. In: Federoff S (ed) Labeling methods applicable to the study of neuronal pathways: advances in cellular neurobiology, Vol 5. Academic Press, New York

    Google Scholar 

  • Leah J, Menétrey D, Besson JM (1986) Neuropeptides in ascending tract cells in the spinal cord of the rat. Neurosci Lett Suppl 26:8219

    Google Scholar 

  • Liu RPC (1983) Laminar origins of spinal projection neurons to the periaqueductal gray of the rat. Brain Res 264:118–122

    Google Scholar 

  • Liu RPC (1986) Spinal neuronal collaterals to the intralaminar thalamic nuclei and periaqueductal gray. Brain Res 365:145–150

    Google Scholar 

  • Lu G-W, Bennett GJ, Nishikawa N, Hoffert MJ, Dubner R (1983) Extra- and intracellular recording from dorsal column postsynaptic spinomedullary neurons in the cat. Exp Neurol 82:456–477

    Google Scholar 

  • Martin GF, Waltzer RF (1984) A study of overlap and collateralization of the bulbar reticular and raphe neurons which project to the spinal cord and diencephalon of the North American opossum. Brain Behav Evol 24:109–123

    Google Scholar 

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

    Google Scholar 

  • Menétrey D, Chaouch A, Besson JM (1980) Location and properties of dorsal horn neurons at origin of spinoreticular tract in lumbar enlargement of the rat. J Neurophysiol 44:862–877

    Google Scholar 

  • Menétrey D, Chaouch A, Binder D, Besson JM (1982) The origin of the spinomesencephalic tract in the rat: an anatomical study using the retrograde transport of horseradish peroxidase. J Comp Neurol 206:193–207

    Google Scholar 

  • Menétrey D, Roudier F, Besson JM (1983) Spinal neurons reaching the lateral reticular nucleus as studied in the rat by retrograde transport of horseradish peroxidase. J Comp Neurol 220:439–452

    Google Scholar 

  • Morrell JI, Pfaff DW (1983) Retrograde HRP identification of neurons in the rhombencephalon and spinal cord of the rat that project to the dorsal mesencephalon. Am J Anat 167:229–240

    Google Scholar 

  • Paxinos G, Watson C (1982) The rat brain in stereotaxic coordinates. Academic Press, Australia

    Google Scholar 

  • Rexed B (1952) The cytoarchitectonic organization of the spinal cord in the cat. J Comp Neurol 96:415–495

    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 (1974) Non-primary afferents to the cuneate nucleus in the brachial dorsal funiculus of the cat. Brain Res 75:247–259

    Google Scholar 

  • Rustioni A, Kaufmann 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 

  • Rustioni A, Cuénod M (1982) Selective retrograde transport of d-aspartate in spinal interneurons and cortical neurons of rats. Brain Res 236:143–155

    Google Scholar 

  • Schmued LC, Swanson LW, Sawchenko PE (1982) Some fluorescent counterstains for neuroanatomical studies. J Histochem Cytochem 30:123–128

    Google Scholar 

  • Steiner TJ, Turner LM (1972) Cytoarchitecture of the rat spinal cord. J Physiol (London) 222:123–125

    Google Scholar 

  • Svensson BA, Westman J, Rastad J (1985) Light and electron microscopic study of neurons in the feline lateral cervical nucleus with a descending projection. Brain Res 361:114–124

    Google Scholar 

  • Swett JE, McMahon SB, Wall PD (1985) Long ascending projections to the midbrain from cells of lamina I and nucleus of the dorsolateral funiculus of the rat spinal cord. J Comp Neurol 238:401–416

    Google Scholar 

  • Verburgh CA, Kuypers HGJM (1987) Branching neurons in the cervical spinal cord: a retrograde fluorescent double-labeling study in the rat. Exp Brain Res 68:565–578

    Google Scholar 

  • Verburgh CA, Kuypers HGJM, Voogd J, Stevens HPJD (1989) Spinocerebellar neurons and propriospinal neurons in the cervical spinal cord: a fluorescent double-labeling study in the rat and the cat. Exp Brain Res 75:73–82

    Google Scholar 

  • Waltzer R, Martin GF (1984) Collateralization of reticulospinal axons from the nucleus reticularis gigantocellularis to the cerebellum and diencephalon: a double-labeling study in the rat. Brain Res 293:153–158

    Google Scholar 

  • Yamada J, Otani K (1978) The spinoperiventricular fiber system in the rabbit, rat and cat. Exp Neurol 61:395–406

    Google Scholar 

  • Zemlan FP, Leonard CM, Kow LM, Pfaff DW (1978) Ascending tracts of the lateral columns of the rat spinal cord: a study using the silver impregnation and horseradish peroxidase techniques. Exp Neurol 62:298–334

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Verburgh, C.A., Voogd, J., Kuypers, H.G.J.M. et al. Propriospinal neurons with ascending collaterals to the dorsal medulla, the thalamus and the tectum: a retrograde fluorescent double-labeling study of the cervical cord of the rat. Exp Brain Res 80, 577–590 (1990). https://doi.org/10.1007/BF00227997

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00227997

Key words

Navigation