SpringerLink
Log in

The calcium binding proteins calbindin, parvalbumin, and calretinin have specific patterns of expression in the gray matter of cat spinal cord

  • Published:
Journal of Neurocytology

Abstract

Calcium binding proteins (CBPs) regulate intracellular levels of calcium (Ca2+) ions. CBPs are particularly interesting from a morphological standpoint, because they are differentially expressed in certain sub-populations of cells in the nervous system of various species of vertebrate animals. However, knowledge on the cellular regulation governing such cell-specific CBP expression is still incomplete. In this work on the L7 segment of the cat spinal cord, we analyzed the localization and morphology of neurons expressing the CBPs calbindin-28 KD (CB), parvalbumin (PV), and calretinin (CR), and co-expressing CB and PV, CB and CR, and PV and CR. Single CBP-positive (+) neurons showed specific distributions: (1) CB was present in small neurons localized in laminae I, II, III and X, in small to medium size neurons in laminae III–VI, and in medium to large neurons in laminae VI–VIII; (2) PV was present in small size neurons in laminae III and IV and in medial portions of laminae V and VI, medium neurons and in lamina X at the border with lamina VII, in medium to large neurons in laminae VII and VIII; (3) CR labeling was detected in small size neurons in laminae I, II, III and VIII, in medium to large size neurons in laminae I and III–VII, and in small to medium size neurons in lamina X. Double labeled neurons were a small minority of the CBP+ cells. Co-expression of CB and PV was seen in 1 to 2% of the CBP+ cells, and they were detected in the ventral and intermediate portions of lamina VII and in lamina X. Co-localization of CB and CR was present in 0.3% of the cells and these cells were localized in lamina II. Double labeling for PV and CR occurred in 6% of the cells, and the cells were localized in ventral part of lamina VII and in lamina VIII. Overall, these results revealed distinct and reproducible patterns of localization of the neurons expressing single CBPs and co-expressing two of them. Distinct differences of CBP expression between cat and other species are discussed. Possible relations between the cat L7 neurons expressing different CBPs with the neurons previously analyzed in cat and other animals are suggested.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

  • ALVAREZ., F. J., DEWEY, D. E, HARRINGTON, D. A. & FYFFE, R. E. (1997) Cell-type specific organization of glycine receptor clusters in the mammalian spinal cord. Journal of Comparative Neurology 379, 150–170.

    Article  PubMed  CAS  Google Scholar 

  • ALVAREZ, F. J., DEWEY, D. E., MCMILLIN, P. & FYFFE, R. E. (1999) Distribution of cholinergic contacts on Renshaw cells in the rat spinal cord: A light microscopic study. Journal of Physiology 515, 787–797.

    Article  PubMed  CAS  Google Scholar 

  • ANDRESSEN, C., BLUMCKE, I. & CELIO, M. R. (1993) Calcium-binding proteins: Selective markers of nerve cells. Cell and Tissue Research 271, 181–208.

    Article  PubMed  CAS  Google Scholar 

  • ANELLI, R., DUNN, M. E. & MUGNAINI, E. (2000) Unipolar brush cells develop a set of characteristic features in primary cerebellar cultures. Journal of Neurocytology 29, 129–144.

    Article  PubMed  CAS  Google Scholar 

  • ANELLI, R. & MUGNAINI, E. (2001) Enrichment of unipolar brush cell-like neurons in primary rat cerebellar cultures. Anatomy and Embryology (Berl) 203, 283–292.

    Article  CAS  Google Scholar 

  • ANTAL, M., FREUND, T. F. & POLGAR, E. (1990) Calcium-binding proteins, parvalbumin- and calbindin-D 28k-immunoreactive neurons in the rat spinal cord and dorsal root ganglia: A light and electron microscopic study. Journal of Comparative Neurology 295, 467–484.

    Article  PubMed  CAS  Google Scholar 

  • ANTAL, M., POLGAR, E., CHALMERS, J., MINSON, J. B., LLEWELLYN-SMITH, I., HEIZMANN, C. W. & SOMOGYI, P. (1991) Different populations of parvalbumin- and calbindin-D28k-immunoreactive neurons contain GABA and accumulate 3H-D-aspartate in the dorsal horn of the rat spinal cord. Journal of Comparative Neurology 314, 114–124.

    Article  PubMed  CAS  Google Scholar 

  • AOKI, E., SEMBA, R., SETO-OHSHIMA, A., HEIZMANN, C. W. & KASHIWAMATA, S. (1990) Coexistence of parvalbumin and glycine in the rat brainstem. Brain Research 525, 140–143.

    Article  PubMed  CAS  Google Scholar 

  • ARMSTRONG, D. M. & SCHILD, R. F. (1979) Spino-olivary neurones in the lumbo-sacral cord of the cat demonstrated by retrograde transport of horseradish peroxidase. Brain Research 168, 176–179.

    Article  PubMed  CAS  Google Scholar 

  • ARVANITOGIANNIS, A., ROBINSON, B., BEAULE, C. & AMIR, S. (2000) Calbindin-D28k immunoreactivity in the suprachiasmatic nucleus and the circadian response to constant light in the rat. Neuroscience 99, 397–401.

    Article  PubMed  CAS  Google Scholar 

  • ARVIDSSON, U., ULFHAKE, B., CULLHEIM, S., RAMIREZ, V., SHUPLIAKOV, O. & HOKFELT, T. (1992) Distribution of calbindin D28k-like immunoreactivity (LI) in the monkey ventral horn: Do Renshaw cells contain calbindin D28k-LI? Journal of Neuroscience 12, 718–728.

    PubMed  CAS  Google Scholar 

  • BAIMBRIDGE, K. G., CELIO, M. R. & ROGERS, J. H. (1992) Calcium-binding proteins in the nervous system. Trends in Neuroscience 15, 303–308.

    Article  CAS  Google Scholar 

  • BARAKAT-WALTER, I., KRAFTSIK, R., KUNTZER, T., BOGOUSSLAVSKY, J. & MAGISTRETTI, P. (2000) Differential effect of thyroid hormone deficiency on the growth of calretinin-expressing neurons in rat spinal cord and dorsal root ganglia. Journal of Comparative Neurology 426, 519–533.

    Article  PubMed  CAS  Google Scholar 

  • BRAS, H., CAVALLARI, P., JANKOWSKA, E. & KUBIN, L. (1989) Morphology of midlumbar interneurones relaying information from group II muscle afferents in the cat spinal cord. Journal of Comparative Neurology 290, 1–15.

    Article  PubMed  CAS  Google Scholar 

  • CAO, C. Q., DJOUHRI, L. & BROWN, A. G. (1993) Lumbosacral spinal neurons in the cat that are candidates for being activated by collaterals from the spinocervical tract. Neuroscience 57, 153–165.

    Article  PubMed  CAS  Google Scholar 

  • CARR, P. A., ALVAREZ, F. J., LEMAN, E. A. & FYFFE, R. E. (1998) Calbindin D28k expression in immunohistochemically identified Renshaw cells. Neuroreport 9, 2657–2661.

    Article  PubMed  CAS  Google Scholar 

  • CARSTENS, E. & TREVINO, D. L. (1978) Laminar origins of spinothalamic projections in the cat as determined by the retrograde transport of horseradish peroxidase. Journal of Comparative Neurology 182, 161–165.

    PubMed  CAS  Google Scholar 

  • CELIO, M. R. (1986) Parvalbumin in most gamma-aminobutyric acid-containing neurons of the rat cerebral cortex. Science 231, 995–997.

    PubMed  CAS  Google Scholar 

  • CLOWRY, G. J., ARNOTT, G. A., CLEMENT-JONES, M., FALLAH, Z., GOULD, S. & WRIGHT, C. (2000) Changing pattern of expression of parvalbumin immunoreactivity during human fetal spinal cord development. Journal of Comparative Neurology 423, 727–735.

    Article  PubMed  CAS  Google Scholar 

  • CZARKOWSKA, J., JANKOWSKA, E. & SYBIRSKA, E. (1981) Common interneurones in reflex pathways from group 1a and 1b afferents of knee flexors and extensors in the cat. Journal of Physiology 310, 367–380.

    PubMed  CAS  Google Scholar 

  • EDGLEY, S. A. (2001) Organisation of inputs to spinal interneurone populations. Journal of Physiology 533, 51–56.

    Article  PubMed  CAS  Google Scholar 

  • ENEVOLDSON, T. P. & GORDON, G. (1989) Postsynaptic dorsal column neurons in the cat: A study with retrograde transport of horseradish peroxidase. Experimental Brain Research 75, 611–620.

    CAS  Google Scholar 

  • ERTEL, S. I. & ERTEL, E. A. (1997) Low-voltage-activated T-type Ca2+ channels. Trends in Pharmacogical Sciences 18, 37–42.

    Article  CAS  Google Scholar 

  • FIELDS, H. L., CLANTON, C. H. & ANDERSON, S. D. (1977) Somatosensory properties of spinoreticular neurons in the cat. Brain Research 120, 49–66.

    Article  PubMed  CAS  Google Scholar 

  • FOURNET, N., GARCIA-SEGURA, L. M., NORMAN, A. W. & ORCI, L. (1986) Selective localization of calcium-binding protein in human brainstem, cerebellum and spinal cord. Brain Research 399, 310–316.

    Article  PubMed  CAS  Google Scholar 

  • FYFFE, R. E. (1990) Evidence for separate morphological classes of Renshaw cells in the cat's spinal cord. Brain Research 536, 301–304.

    Article  PubMed  CAS  Google Scholar 

  • GALHARDO, V. & LIMA, D. (1999) Structural characterization of marginal (lamina I) spinal cord neurons in the cat: AA Golgi study. Journal of Comparative Neurology 414, 315–333.

    Article  PubMed  CAS  Google Scholar 

  • GEIMAN, E. J., KNOX, M. C. & ALVAREZ, F. J. (2000) Postnatal maturation of gephyrin/glycine receptor clusters on develo** Renshaw cells. Journal of Comparative Neurology 426, 130–142.

    Article  PubMed  CAS  Google Scholar 

  • GEIMAN, E. J., ZHENG, W., FRITSCHY, J. M. & ALVAREZ, F. J. (2002) Glycine and GABA(A) receptor subunits on Renshaw cells: Relationship with presynaptic neurotransmitters and postsynaptic gephyrin clusters. Journal of Comparative Neurology 444, 275–289.

    Article  PubMed  CAS  Google Scholar 

  • GRANT, G., WIKSTEN, B., BERKLEY, K. J. & ALDSKOGIUS, H. (1982) The location of cerebellar-projecting neurons within the lumbosacral spinal cord in the cat. An anatomical study with HRP and retrograde chromatolysis. Journal of Comparative Neurology 204, 336–348.

    Article  PubMed  CAS  Google Scholar 

  • GUGLIELMONE, R. & CORVETTI, G. (2000) First appearance and distribution of calretinin-immunoreactive neurons in the early development of the chick central nervous system. Cell Tissue Research 300, 21–28.

    PubMed  CAS  Google Scholar 

  • HAN, Z. S., ZHANG, E. T. & CRAIG, A. D. (1998) Nociceptive and thermoreceptive lamina I neurons are anatomically distinct. Nature Neuroscience 1, 218–225.

    Article  PubMed  CAS  Google Scholar 

  • HARRISON, P. J., JANKOWSKA, E. & ZYTNICKI, D. (1986) Lamina VIII interneurones interposed in crossed reflex pathways in the cat. Journal of Physiology 371, 147–166.

    PubMed  CAS  Google Scholar 

  • HEIZMANN, C. W. & BRAUN, K. (1992) Changes in Ca(2+)-binding proteins in human neurodegenerative disorders. Trends in Neuroscience 15, 259–264.

    Article  CAS  Google Scholar 

  • HONGO, T., JANKOWSKA, E., OHNO, T., SASAKI, S., YAMASHITA, M. & YOSHIDA, K. (1983) Inhibition of dorsal spinocerebellar tract cells by interneurones in upper and lower lumbar segments in the cat. Journal of Physiology 342, 145–159.

    PubMed  CAS  Google Scholar 

  • HOOVER, J. E. & DURKOVIC, R. G. (1992) Retrograde labeling of lumbosacral interneurons following injections of red and green fluorescent microspheres into hindlimb motor nuclei of the cat. Somatosensory Motor Research 9, 211–226.

    PubMed  CAS  Google Scholar 

  • HUANG, A., NOGA, B. R., CARR, P. A., FEDIRCHUK, B. & JORDAN, L. M. (2000) Spinal cholinergic neurons activated during locomotion: Localization and electrophysiological characterization. Journal of Neurophysiology 83, 3537–3547.

    PubMed  CAS  Google Scholar 

  • HULTBORN, H., JANKOWSKA, E. & LINDSTROM, S. (1971) Recurrent inhibition of interneurones monosynaptically activated from group Ia afferents. Journal of Physiology 215, 613–636.

    PubMed  CAS  Google Scholar 

  • INCE, P., STOUT, N., SHAW, P., SLADE, J., HUNZIKER, W., HEIZMANN, C. W. & BAIMBRIDGE, K. G. (1993) Parvalbumin and calbindin D-28k in the human motor system and in motor neuron disease. Neuropathology and Applied Neurobiology 19, 291–299.

    PubMed  CAS  Google Scholar 

  • JANKOWSKA, E. & LINDSTROM, S. (1972) Morphology of interneurones mediating Ia reciprocal inhibition of motoneurones in the spinal cord of the cat. Journal of Physiology 226, 805–823.

    PubMed  CAS  Google Scholar 

  • JANKOWSKA, E. (1992) Interneuronal relay in spinal pathways from proprioceptors. Progress in Neurobiology 38, 335–378.

    Article  PubMed  CAS  Google Scholar 

  • JANKOWSKA, E., RIDDELL, J. S., SZABO-LACKBERG, Z. & HAMMAR, I. (1993) Morphology of interneurones in pathways from group II muscle afferents in sacral segments of the cat spinal cord. Journal of Comparative Neurology 337, 518–528.

    Article  PubMed  CAS  Google Scholar 

  • JANKOWSKA, E. & RIDDELL, J. S. (1994) Interneurones in pathways from group II muscle afferents in sacral segments of the feline spinal cord. Journal of Physiology 475, 455–468.

    PubMed  CAS  Google Scholar 

  • JANKOWSKA, E. (2001) Spinal interneuronal systems: Identification, multifunctional character and reconfigurations in mammals. Journal of Physiology 533, 31–40.

    Article  PubMed  CAS  Google Scholar 

  • JO, Y. H., STOECKEL, M. E. & SCHLICHTER, R. (1998) Electrophysiological properties of cultured neonatal rat dorsal horn neurons containing GABA and met-enkephalin-like immunoreactivity. Journal of Neurophysiology 79, 1583–1586.

    PubMed  CAS  Google Scholar 

  • KAWAGUCHI, Y., KATSUMARU, H., KOSAKA, T., HEIZMANN, C. W. & HAMA, K. (1987) Fast spiking cells in rat hippocampus (CA1 region) contain the calcium- binding protein parvalbumin. Brain Research 416, 369–374.

    Article  PubMed  CAS  Google Scholar 

  • KNIRSCH, U., STURM, S., REUTER, A., BACHUS, R., GOSZTONYI, G., VOELKEL, H. & LUDOLPH, A. C. (2001) Calcineurin A and calbindin immunoreactivity in the spinal cord of G93A superoxide dismutase transgenic mice. Brain Research 889, 234–238.

    Article  PubMed  CAS  Google Scholar 

  • KUZE, B., MATSUYAMA, K., MATSUI, T., MIYATA, H. & MORI, S. (1999) Segment-specific branching patterns of single vestibulospinal tract axons arising from the lateral vestibular nucleus in the cat: A PHA-L tracing study. Journal of Comparative Neurology 414, 80–96.

    Article  PubMed  CAS  Google Scholar 

  • LEE, R. H. & HECKMAN, C. J. (1998a) Bistability in spinal motoneurons in vivo: Systematic variations in persistent inward currents. Journal of Neurophysiology 80, 583–593.

    CAS  Google Scholar 

  • LEE, R. H. & HECKMAN, C. J. (1998b) Bistability in spinal motoneurons in vivo: systematic variations in rhythmic firing patterns. Journal of Neurophysiology 80, 572–582.

    CAS  Google Scholar 

  • LEE, R. H. & HECKMAN, C. J. (2000) Adjustable amplification of synaptic input in the dendrites of spinal motoneurons in vivo. Journal of Neuroscience 20, 6734–6740.

    PubMed  CAS  Google Scholar 

  • LEE, R. H. & HECKMAN, C. J. (2001) Essential role of a fast persistent inward current in action potential initiation and control of rhythmic firing. Journal of Neurophysiology 85, 472–475.

    PubMed  CAS  Google Scholar 

  • LEE, S. H., ROSENMUND, C., SCHWALLER, B. & NEHER, E. (2000) Differences in Ca2+ buffering properties between excitatory and inhibitory hippocampal neurons from the rat. Journal of Physiology 525 Pt 2, 405–418.

    Article  PubMed  CAS  Google Scholar 

  • LIMA, D. & COIMBRA, A. (1990). Structural types of marginal (lamina I) neurons projecting to the dorsal reticular nucleus of the medulla oblongata. Neuroscience 34, 591–606.

    Article  PubMed  CAS  Google Scholar 

  • LIMA, D., AVELINO, A. & COIMBRA, A. (1993) Morphological characterization of marginal (lamina I) neurons immunoreactive for substance P, enkephalin, dynorphin and gamma-aminobutyric acid in the rat spinal cord. Journal of Chemical Neuroanatomy 6, 43–52.

    Article  PubMed  CAS  Google Scholar 

  • MALER, L., JANDE, S. & LAWSON, E. M. (1984) Localization of vitamin D-dependent calcium binding protein in the electrosensory and electromotor system of high frequency gymnotid fish. Brain Research 301, 166–170.

    Article  PubMed  CAS  Google Scholar 

  • MARTINA, M., SCHULTZ, J. H., EHMKE, H., MONYER, H. & JONAS, P. (1998) Functional and molecular differences between voltage-gated K+ channels of fast-spiking interneurons and pyramidal neurons of rat hippocampus. Journal of Neuroscience 18, 8111–8125.

    PubMed  CAS  Google Scholar 

  • MAUNZ, R. A., PITTS, N. G. & PETERSON, B. W. (1978) Cat spinoreticular neurons: Locations, responses and changes in responses during repetitive stimulation. Brain Research 148, 365–379.

    Article  PubMed  CAS  Google Scholar 

  • MAXWELL, D. J., KERR, R., JANKOWSKA, E. & RIDDELL, J. S. (1997) Synaptic connections of dorsal horn group II spinal interneurons: synapses formed with the interneurons and by their axon collaterals. Journal of Comparative Neurology 380, 51–69.

    Article  PubMed  CAS  Google Scholar 

  • MENETREY, D., ROUDIER, F. & BESSON, J. M. (1983) Spinal neurons reaching the lateral reticular nucleus as studied in the rat by retrograde transport of horseradish peroxidase. Journal of Comparative Neurology 220, 439–452.

    Article  PubMed  CAS  Google Scholar 

  • MENETREY, D. & BASBAUM, A. I. (1987) Spinal and trigeminal projections to the nucleus of the solitary tract: A possible substrate for somatovisceral and viscerovisceral reflex activation. Journal of Comparative Neurology 255, 439–450.

    Article  PubMed  CAS  Google Scholar 

  • MENETREY, D., DE POMMERY, J., THOMASSET, M. & BAIMBRIDGE, K. G. (1992) Calbindin-D28K (CaBP28k)-like Immunoreactivity in Ascending Projections. European Journal of Neuroscience 4, 70–76.

    Article  PubMed  Google Scholar 

  • MEYERS, D. E. & SNOW, P. J. (1982) The morphology of physiologically identified deep spinothalamic tract cells in the lumbar spinal cord of the cat. Journal of Physiology 329, 373–388.

    PubMed  CAS  Google Scholar 

  • MOSCHOVAKIS, A. K., SOLODKIN, M. & BURKE, R. E. (1992) Anatomical and physiological study of interneurons in an oligosynaptic cutaneous reflex pathway in the cat hindlimb. Brain Research 586, 311–318.

    Article  PubMed  CAS  Google Scholar 

  • MOUTON, L. J. & HOLSTEGE, G. (1994) The periaqueductal gray in the cat projects to lamina VIII and the medial part of lamina VII throughout the length of the spinal cord. Experimental Brain Research 101, 253–264.

    Article  CAS  Google Scholar 

  • MOUTON, L. J. & HOLSTEGE, G. (1998) Three times as many lamina I neurons project to the periaqueductal gray than to the thalamus: A retrograde tracing study in the cat. Neuroscience Letters 255, 107–110.

    Article  PubMed  CAS  Google Scholar 

  • NAHIN, R. L., MADSEN, A. M. & GIESLER, G. J., JR. (1983) Anatomical and physiological studies of the gray matter surrounding the spinal cord central canal. Journal of Comparative Neurology 220, 321–335.

    Article  PubMed  CAS  Google Scholar 

  • NOGA, B. R., KETTLER, J. & JORDAN, L. M. (1988) Locomotion produced in mesencephalic cats by injections of putative transmitter substances and antagonists into the medial reticular formation and the pontomedullary locomotor strip. Journal of Neuroscience 8, 2074–2086.

    PubMed  CAS  Google Scholar 

  • NOGA, B. R., FORTIER, P. A., KRIELLAARS, D. J., DAI, X., DETILLIEUX, G. R. & JORDAN, L. M. (1995) Field potential map** of neurons in the lumbar spinal cord activated following stimulation of the mesencephalic locomotor region. Journal of Neuroscience 15, 2203–2217.

    PubMed  CAS  Google Scholar 

  • PEZET, S., ONT NIENTE, B., GRANNEC, G. & CALVINO, B. (1999) Chronic pain is associated with increased TrkA immunoreactivity in spinoreticular neurons. Journal of Neuroscience 19, 5482–5492.

    PubMed  CAS  Google Scholar 

  • POPPELE, R. E., BOSCO, G. & RANKIN, A. M. (2002) Independent representations of limb axis length and orientation in spinocerebellar response components. Journal of Neurophysiology 87, 409–422.

    PubMed  CAS  Google Scholar 

  • PRESCOTT, S. A. & KONINCK, Y. D. (2002) Four cell types with distinctive membrane properties and morphologies in lamina I of the spinal dorsal horn of the adult rat. Journal of Physiology 539, 817–836.

    Article  PubMed  CAS  Google Scholar 

  • PUSKAR, Z. & ANTAL, M. (1997) Localization of last-order premotor interneurons in the lumbar spinal cord of rats. Journal of Comparative Neurology 389, 377–389.

    Article  PubMed  CAS  Google Scholar 

  • RABOISSON, P., DALLEL, R., BERNARD, J. F., LE BARS, D. & VILLANUEVA, L. (1996) Organization of efferent projections from the spinal cervical enlargement to the medullary subnucleus reticularis dorsalis and the adjacent cuneate nucleus: a PHA-L study in the rat. Journal of Comparative Neurology 367, 503–517.

    Article  PubMed  CAS  Google Scholar 

  • RASTAD, J., JANKOWSKA, E. & WESTMAN, J. (1977) Arborization of initial axon collaterals of spinocervical tract cells stained intracellularly with horseradish peroxidase. Brain Research 135, 1–10.

    Article  PubMed  CAS  Google Scholar 

  • RASTAD, J., GAD, P., JANKOWSKA, E., MCCREA, D. & WESTMAN, J. (1990) Light microscopical study of dendrites and perikarya of interneurones mediating la reciprocal inhibition of cat lumbar alpha-motoneurones. Anatomy and Embryology 181, 381–388.

    Article  PubMed  CAS  Google Scholar 

  • REN, K. & RUDA, M. A. (1994) A comparative study of the calcium-binding proteins calbindin-D28K, calretinin, calmodulin and parvalbumin in the rat spinal cord. Brain Research 19, 163–179.

    Article  CAS  Google Scholar 

  • REXED, B. (1952) The cytoarchitectonic organization of the spinal cord in the cat. Journal of Comparative Neurology 96, 415–466.

    Article  Google Scholar 

  • REYNOLDS, G. P. & BEASLEY, C. L. (2001) GABAergic neuronal subtypes in the human frontal cortex-Development and deficits in schizophrenia. Journal of Chemical Neuroanatomy 22, 95–100.

    Article  PubMed  CAS  Google Scholar 

  • RIDDELL, J. S. & HADIAN, M. (2000) Interneurones in pathways from group II muscle afferents in the lower- lumbar segments of the feline spinal cord. Journal of Physiology 522 Pt 1, 109–123.

    Article  PubMed  CAS  Google Scholar 

  • ROGERS, J., KHAN, M. & ELLIS, J. (1990) Calretinin and other CaBPs in the nervous system. Advances Experimental in Medical Biology 269, 195–203.

    CAS  Google Scholar 

  • RUDOMIN, P. & SCHMIDT, R. F. (1999) Presynaptic inhibition in the vertebrate spinal cord revisited. Experimental Brain Research 129, 1–37.

    Article  CAS  Google Scholar 

  • SANDKUHLER, J., CHEN, J. G., CHENG, G. & RANDIC, M. (1997) Low-frequency stimulation of afferent Adelta-fibers induces long-term depression at primary afferent synapses with substantia gelatinosa neurons in the rat. Journal of Neuroscience 17, 6483–6491.

    PubMed  CAS  Google Scholar 

  • SCHNEIDER, S. P. & FYFFE, R. E. (1992) Involvement of GABA and glycine in recurrent inhibition of spinal motoneurons. Journal of Neurophysiology 68, 397–406.

    PubMed  CAS  Google Scholar 

  • SCHWALLER, B., MEYER, M. & SCHIFFMANN, S. (2002) ‘New’ functions for ‘old’ proteins: The role of the calcium-binding proteins calbindin D-28k, calretinin and parvalbumin, in cerebellar physiology. Studies with knockout mice. Cerebellum 1, 241–258.

    Article  PubMed  CAS  Google Scholar 

  • SNOW, P. J., ROSE, P. K. & BROWN, A. G. (1976) Tracing axons and axon collaterals of spinal neurons using intracellular injection of horseradish peroxidase. Science 191, 312–313.

    PubMed  CAS  Google Scholar 

  • SOLBACH, S. & CELIO, M. R. (1991) Ontogeny of the calcium binding protein parvalbumin in the rat nervous system. Anatomy and Embryology 184, 103–124.

    Article  PubMed  CAS  Google Scholar 

  • TOLEDO-RODRIGUEZ, M., BLUMENFELD, B., WU, C., LUO, J., ATTALI, B., GOODMAN, P. & MARKRAM, H. (2004) Correlation Maps Allow Neuronal Electrical Properties to be Predicted from Single-cell Gene Expression Profiles in Rat Neocortex. Cerebral Cortex. (Advance Access published) June 10.

  • VANDERHORST, V. G., MOUTON, L. J., BLOK, B. F. & HOLSTEGE, G. (1996) Distinct cell groups in the lumbosacral cord of the cat project to different areas in the periaqueductal gray. Journal of Comparative Neurology 376, 361–385.

    Article  PubMed  CAS  Google Scholar 

  • VERGARA, C., LATORRE, R., MARRION, N. V. & ADELMAN, J. P. (1998) Calcium-activated potassium channels. Current Opinion in Neurobiogy 8, 321–329.

    Article  CAS  Google Scholar 

  • VILLANUEVA, L., DE POMMERY, J., MENETREY, D. & LE BARS, D. (1991) Spinal afferent projections to subnucleus reticularis dorsalis in the rat. Neuroscience Letters 134, 98–102.

    Article  PubMed  CAS  Google Scholar 

  • WIBERG, M. & BLOMQVIST, A. (1984) The spinomesencephalic tract in the cat: Its cells of origin and termination pattern as demonstrated by the intraaxonal transport method. Brain Research 291, 1–18.

    Article  PubMed  CAS  Google Scholar 

  • WILLIS, W. D. & WILLIS, J. C. (1964) Location of Renshaw Cells. Nature 204, 1214–1215.

    Article  PubMed  CAS  Google Scholar 

  • WILLIS, W. D. (1995) Pain. In The Rat Nervous System (edited by ACADEMIC PRESS), pp. 725–750. Sydney.

  • WOODS, T. M., CUSICK, C. G., PONS, T. P., TAUB, E. & JONES, E. G. (2000) Progressive transneuronal changes in the brainstem and thalamus after long-term dorsal rhizotomies in adult macaque monkeys. Journal of Neuroscience 20, 3884–3899.

    PubMed  CAS  Google Scholar 

  • YOSHIDA, S., SENBA, E., KUBOTA, Y., HAGIHIRA, S., YOSHIYA, I., EMSON, P. C. & TOHYAMA, M. (1990) Calcium-binding proteins calbindin and parvalbumin in the superficial dorsal horn of the rat spinal cord. Neuroscience 37, 839–848.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Physiology, Northwestern Feinberg School of Medicine, Chicago, Illinois

    Roberta Anelli

  2. Physical Medicine and Rehabilitation, Northwestern Feinberg School of Medicine, Chicago, Illinois

    C. J. Heckman

Authors
  1. Roberta Anelli
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. C. J. Heckman
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Roberta Anelli.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Anelli, R., Heckman, C.J. The calcium binding proteins calbindin, parvalbumin, and calretinin have specific patterns of expression in the gray matter of cat spinal cord. J Neurocytol 34, 369–385 (2005). https://doi.org/10.1007/s11068-006-8724-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11068-006-8724-2

Keywords

Search

Navigation