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An electron microscopic examination of the corticospinal projection to the cervical spinal cord in the rat: lack of evidence for cortico-motoneuronal synapses

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Abstract

We investigated whether direct, cortico-motoneuronal connections are present in the rat, using both light microscopic and electron microscopic techniques. Corticospinal fibres were labelled using the anterograde tracer, biotinylated dextran-amine (BDA), which was injected into forelimb sensorimotor cortex. Motoneurons were retrogradely labelled after injection of cholera toxin subunit B (CTB) into forelimb muscles, contralateral to the injected hemisphere. Terminals of peripheral afferent fibres, which were also labelled by CTB, were easily distinguishable from, and much larger than, BDA-labelled corticospinal terminals. At the light microscope level, corticospinal terminals were found in all laminae contralateral to the injection site, most extensively in laminae VI and VII of cervical segments C5–C8. Although labelling in the ventral horn (lamina IX) was present, it was extremely sparse. A total of 47 corticospinal synapses were studied at the electron microscope level; most of these were in lamina VII and the majority (35/47; 74%) made axo-dendritic contacts with asymmetrical synapses; one made an axo-somatic synapse, and in the remaining 11 cases no postsynaptic structure could be identified. All corticospinal terminals contained spherical boutons. Serial sectioning of eight BDA-labelled corticospinal boutons in lamina IX revealed that most (seven out of eight) did not make synaptic contacts with any neuronal structure, and none made any contact with adjacent dendrites of CTB-labelled motoneurons. Thus these results provide no positive ultrastructural evidence for direct cortico-motoneuronal synaptic connections within lamina IX between corticospinal axon boutons and the proximal dendrites of forelimb motoneurons. The results confirm other lines of evidence suggesting that such connections are not present in the rat.

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References

  • Babalian A, Liang F, Rouiller EM (1993) Cortical influences on cervical motoneurons in the rat: recordings of synaptic responses from motoneurons and compound action potential from corticospinal axons. Neurosci Res 16:301–310

    CAS  PubMed  Google Scholar 

  • Bannister CM, Porter R (1967) Effects of limited direct stimulation of the medullary pyramidal tract on spinal motoneurons in the rat. Exp Neurol 17:265–275

    CAS  PubMed  Google Scholar 

  • Bareyre FM, Haudenschild B, Schwab ME (2002) Long-lasting and gene expression changes induced by the monoclonal antibody IN-1 in the adult spinal cord. J Neurosci 22:7097–7110

    CAS  PubMed  Google Scholar 

  • Bodian D (1975) Origin of specific types in the motoneuron neuropil of the monkey. J Comp Neurol 159:225–244

    CAS  PubMed  Google Scholar 

  • Bortoff GA, Strick PL (1993) Corticospinal terminations in two New-World primates: further evidence that corticomotoneuronal connections provide part of the neural substrate for manual dexterity. J Neurosci 13:5105–5118

    CAS  PubMed  Google Scholar 

  • Brandt HM, Apkarian AV (1992) Biotin-dextran: a sensitive anterograde tracer for neuroanatomic studies in rat and monkey. J Neurosci Methods 45:35–40

    CAS  PubMed  Google Scholar 

  • Brosamle C, Schwab ME (1997) Cells of origin, course, and termination patterns of the ventral, uncrossed component of the mature rat corticospinal tract. J Comp Neurol 386:293–303

    CAS  PubMed  Google Scholar 

  • Brown LT (1971) Projections and termination of the corticospinal tract in rodents. Exp Brain Res 13:432–450

    PubMed  Google Scholar 

  • Brown AG, Fyffe REW (1981) Direct observations on the contacts made between Ia afferent fibres and þ-motoneurones in the cat's lumbosacral spinal cord. J Physiol (Lond) 313:121–140

    Google Scholar 

  • Conradi S (1969) Ultrastructure of dorsal root boutons on lumbosacral motoneurons of the adult cats as revealed by dorsal root section. Acta Physiol Scand Suppl 332:85–115

    CAS  PubMed  Google Scholar 

  • Conradi S, Cullheim S, Gollvik L, Kellerth JO (1983) Electron microscopic observations on the synaptic contacts of group Ia muscle spindle afferents in the cat lumbosacral cord. Brain Res 265:31–39

    CAS  PubMed  Google Scholar 

  • Curfs MHJM, Gribnau AAM, Dederen PJWC (1994) Selective elimination of transient corticospinal projections in the rat cervical spinal cord gray matter. Dev Brain Res 78:182–190

    CAS  Google Scholar 

  • Curfs MHJM, Gribnau AAM, Dederen PJWC (1996) Direct cortico-motoneuronal synaptic contacts are present in the adult rat cervical spinal cord and are first established at postnatal day 7. Neurosci Lett 205:123–126

    Article  CAS  PubMed  Google Scholar 

  • Donoghue JP, Wise SP (1982) The motor cortex of the rat: cytoarchitecture and microstimulation mapping. J Comp Neurol 212:76–88

    Google Scholar 

  • Elger CE, Speckmann E-J, Caspers H, Janzen RWC (1977) Cortico-spinal connections in the rat. I. Monosynaptic and polysynaptic responses of cervical motor neurons to epicortical stimulation. Exp Brain Res 28:385–404

    CAS  PubMed  Google Scholar 

  • Ericson H, Blomqvist A (1988) Tracing of neuronal connections with cholera toxin subunit B: light and electron microscopic immunohistochemistry using monoclonal antibodies. J Neurosci Methods 24:225–235

    CAS  PubMed  Google Scholar 

  • Gemma M, Perego GB, Pizzini G, Tredici G (1987) Distribution of the cortico-spinal fibres in the cervical and lumbar enlargements of the rat spinal cord. J Hirnforsch 28:457–462

    CAS  PubMed  Google Scholar 

  • Gibson CL, Clowry GJ (1999) Retraction of muscle afferents from the rat ventral horn during development. Neuroreport 10:231–235

    CAS  PubMed  Google Scholar 

  • Gorgels TGMF, de Kort EM, van Aanholt HTH, Nieuwenjuys R (1989) A quantitative analysis of the development of the pyramidal tract in the cervical spinal cord in the rat. Anat Embryol (Berl) 179:377–383

    Google Scholar 

  • Gribnau AAM, de Kort EJM, Dederen PJWC, Nieuwenjuys R (1986) On the development of the pyramidal tract in the rat. II. An anterograde tracer study of the outgrowth of the corticospinal fibers. Anat Embryol (Berl) 175:101–110

    Google Scholar 

  • Gugino LD, Rowinski MJ, Stoney SD (1990) Motor outflow to cervical motoneurons from racoon motorsensory cortex. Brain Res Bull 24:833–837

    CAS  PubMed  Google Scholar 

  • Hall RD, Lindholm EP (1974) Organization of motor and somatosensory neocortex in the albino rat. Brain Res 6:23–38

    Google Scholar 

  • Hirakawa M, McCabe JT, Kawata M (1992) Time-related changes in the labelling pattern of motor and sensory neurons innervating the gastrocnemius muscle, as revealed by the retrograde transport of the cholera toxin B subunit. Cell Tissue Res 267:419–427

    CAS  PubMed  Google Scholar 

  • Holstege G (1995) The basic, somatic, and emotional components of the motor system in mammals. In: Paxinos G (ed) The rat nervous system. Academic, New York, pp 137–154

  • Illert M, Lundberg A, Tanaka R (1976) Integration in descending motor pathways controlling the forelimb in the cat. 1. Pyramidal effects on motoneurones. Exp Brain Res 26:509–519

    CAS  PubMed  Google Scholar 

  • Ivanco TL, Pellis SM, Whishaw IQ (1996) Skilled forelimb movements in prey catching and in reaching by rats (Rattus norvegicus) and opossums (Monodelphis domestica): relations to anatomical differences in motor systems. Behav Brain Res 79:163–181

    Article  CAS  PubMed  Google Scholar 

  • Iwaniuk AN, Whishaw IQ (2000) On the origin of skilled forelimb movements. Trends Neurosci 23:372–376

    CAS  PubMed  Google Scholar 

  • Iwaniuk AN, Pellis SM, Whishaw IQ (1999) Is digital dexterity really related to corticospinal projections?: a re-analysis of the Heffner and Masterton data set using modern comparative statistics. Behav Brain Res 101:173–187

    Article  CAS  PubMed  Google Scholar 

  • Kamida T, Fujiki M, Hori S, Isono M (1998) Conduction pathways of motor evoked potentials following transcranial magnetic stimulation: a rodent study using a "figure-8" coil. Muscle Nerve June:722–731

    Article  Google Scholar 

  • Kuang RZ, Kalil K (1990) Branching patterns of corticospinal axon arbors in the rodent. J Comp Neurol 292:585–598

    CAS  PubMed  Google Scholar 

  • Küchler M, Fouad K, Weinmann O, Schwab ME, Raineteau O (2002) Red nucleus projections to distinct motor neuron pools in the rat spinal cord. J Comp Neurol 448:349–359

    Article  PubMed  Google Scholar 

  • Kuypers HGJM (1981) Anatomy of the descending pathways. In: Brookhart JM, Mountcastle VB (eds) Handbook of physiology—the nervous system II. American Physiological Society, Bethesda, MD, pp 597–666

  • Lawrence DG, Hopkins DA (1976) The development of motor control in the rhesus monkey: evidence concerning the role of corticomotoneuronal connections. Brain 99:235–254

    CAS  PubMed  Google Scholar 

  • Lawrence DG, Kuypers HGJM (1968) The functional organization of the motor system in the monkey. I. The effects of bilateral pyramidal lesions. Brain 91:1–14

    CAS  PubMed  Google Scholar 

  • Lawrence DG, Porter R, Redman SJ (1985) Corticomotoneuronal synapses in the monkey: light microscopic localization upon motoneurons of intrinsic muscles of the hand. J Comp Neurol 232:499–510

    CAS  PubMed  Google Scholar 

  • Lemon RN (1993) Cortical control of the primate hand. The 1992 G.L. Brown Prize Lecture. Exp Physiol 78:263–301

    CAS  PubMed  Google Scholar 

  • Lemon RN, Kirkwood PA, Maier MA, Nakajima K, Nathan P (2002) Direct and indirect pathways for corticospinal control of upper limb motoneurones in the primate. In: Mori S (Ed) Brain mechanisms for the integration of posture and movement. Progress in brain research. Elsevier, Amsterdam (in press)

  • Liang F, Moret M, Wiesendanger M, Rouiller EM (1991) Corticomotoneuronal connections in the rat: evidence from double-labeling of motoneurons and corticospinal axon arborizations. J Comp Neurol 311:356–366

    CAS  PubMed  Google Scholar 

  • Llewellyn-Smith IJ, Minson JB (1992) Complete penetration of antibodies into vitratome sections after glutaraldehyde fixation and ethanol treatment: light and electron microscopy for neuropeptides. J Histochem Cytochem 40:1741–1749

    CAS  PubMed  Google Scholar 

  • Luppi PH, Sakai K, Salvert D, Fort P, Jouvet M (1987) Peptidergic hypothalamic afferents to the cat nucleus raphe pallidus as revealed by a double immunostaining technique using unconjugated cholera toxin as a retrograde tracer. Brain Res 402:339–345

    CAS  PubMed  Google Scholar 

  • Maier MA, Olivier E, Baker SN, Kirkwood PA, Morris T, Lemon RN (1997) Direct and indirect corticospinal control of arm and hand motoneurons in the squirrel monkey (Saimiri sciureus). J Neurophysiol 78:721–733

    CAS  PubMed  Google Scholar 

  • McKenna JE, Whishaw IQ (1999) Complete compensation in skilled reaching success with associated impairments in limb synergies, after dorsal column lesion in the rat. J Neurosci 19:1885–1894

    CAS  PubMed  Google Scholar 

  • McLaughlin BJ (1972) Dorsal root projections to the motor nuclei in the cat spinal cord. J Comp Neurol 144:461–474

    Google Scholar 

  • Molander C, Grant G (1995) Spinal cord cytoarchitecture. In: Paxinos G (ed) The rat nervous system. Academic, New York, pp 39–45

  • Nakajima K, Maier MA, Kirkwood PA, Lemon RN (2000) Striking differences in the transmission of corticospinal excitation to upper limb motoneurons in two primate species. J Neurophysiol 84:698–709

    CAS  PubMed  Google Scholar 

  • Neafsey EJ, Bold EL, Haas G, Hurley-Gius KM, Quirk G, Sievert CF, Terreberry RR (1986) The organization of the rat motor cortex: a microstimulation mapping study. Brain Res Brain Res Rev 11:77–96

    Google Scholar 

  • Nielsen JB, Aimonetti J-M, Marchand-Pauvert V, Enriquez-Denton M (2001) The effect of pyramidal tract stimulation on cervical motoneurones in the rat. International Union of Physiological Sciences Meeting, 2001, Abstr No. 2245

  • O'Donoghue DL, Kartje-Tillotson G, Neafsey EJ, Castro AJ (1986) A study of forelimb movements evoked by intracortical microstimulation after hemicerebellectomy in newborn, young and adult rats. Brain Res 385:311–320

    CAS  PubMed  Google Scholar 

  • Ornung G, Ragnarson B, Grant G, Ottersen OP, Storm-Mathisen J, Ulfhake B (1995) la boutons to CCN neurones and motoneurones are enriched with glutamate-like immunoreactivity. Neuroreport 6:1975–1980

    CAS  PubMed  Google Scholar 

  • Petras JM, Lehman RAW (1966) Corticospinal fibers in the racoon. Brain Res 3:195–197

    CAS  PubMed  Google Scholar 

  • Porter R, Lemon RN (1993) Corticospinal function and voluntary movement. Oxford University Press, Oxford

  • Porter R, Sanderson JH (1964) Antidromic cortical responses to pyramidal tract stimulation in the rat. J Physiol (Lond) 170:355–370

    Google Scholar 

  • Rose PK, Richmond ER (1981) White matter dendrites in the upper cervical spinal cord of the adult cat: a light and electron microscopic study. J Comp Neurol 199:191–203

    CAS  PubMed  Google Scholar 

  • Schwartzman RJ (1978) A behavioural analysis of complete unilateral section of the pyramid tract at the medullary level in Macaca mulatta. Ann Neurol 4:234–244

    CAS  PubMed  Google Scholar 

  • Valtschanoff JG, Weinberg RJ, Rustioni A (1993) Amino acid immunoreactivity in corticospinal terminals. Exp Brain Res 93:95–103

    CAS  PubMed  Google Scholar 

  • Valverde F (1966) The pyramidal tract in rodents. A study of its relations with the posterior column nuclei, dorsolateral reticular formation of the medulla oblongata, and cervical spinal cord. Z Zellforsch 71:297–363

    Google Scholar 

  • Whishaw IQ, Gorny B, Sarna J (1998a) Paw and limb use in skilled and spontaneous reaching after pyramidal tract, red nucleus and combined lesions in the rat: behavioral and anatomical dissociations. Behav Brain Res 93:167–183

    Article  CAS  PubMed  Google Scholar 

  • Whishaw IQ, Sarna JR, Pellis SM (1998b) Evidence for rodent—common and species—typical limb and digit use in eating, derived from a comparative analysis of ten rodent species. Behav Brain Res 96:79–97

    Article  CAS  PubMed  Google Scholar 

  • Wirth FP, O'Leary JL, Smith JM, Jenny AB (1974) Monosynaptic corticospinal motoneuron path in the raccoon. Brain Res 77:344–348

    CAS  PubMed  Google Scholar 

  • Wouterlood FG, Jorritsma-Byham B (1993) The anterograde neuroanatomical tracer biotinylated dextran-amine: comparison with the tracer Phaseolus vulgaris-leucoagglutinin in preparations for electron microscopy. J Neurosci Methods 48:75–87

    CAS  PubMed  Google Scholar 

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Acknowledgements

This work was supported by the Wellcome Trust. We wish to thank Dr. Jean Armand for advice and to Peter Kirkwood and Jens Nielsen for commenting on the manuscript. We thank Kully Sunner and Dr. Chris Seers for expert technical assistance.

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  1. H.-W. Yang

    Present address: Department of Life Sciences, Chung Shan Medical University, 402, Taichung, Taiwan

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  1. Sobell Department of Motor Neuroscience and Movement Disorders, Institute of Neurology, University College London, Queen Square, London, WC1N 3BG, UK

    H.-W. Yang & R. N. Lemon

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Correspondence to R. N. Lemon.

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Yang, HW., Lemon, R.N. An electron microscopic examination of the corticospinal projection to the cervical spinal cord in the rat: lack of evidence for cortico-motoneuronal synapses. Exp Brain Res 149, 458–469 (2003). https://doi.org/10.1007/s00221-003-1393-9

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