Elsevier

Brain Research

Volume 586, Issue 2, 24 July 1992, Pages 208-218
Brain Research

Research report
Origins and collateralization of corticospinal, corticopontine, corticorubral and corticostriatal tracts: a multiple retrograde fluorescent tracing study

https://doi.org/10.1016/0006-8993(92)91629-SGet rights and content

Abstract

Cerebral cells of origin for the corticospinal (CST), corticopontine (CP), corticorubral (CR) and corticostriatal (CS) fibers in the rat were identified following the simultaneous retrograde transport of propidium iodide (PI), fast blue (FB), fluorogold (FG) and diamidino yellow (DY). PI was injected into the contralateral C4 spinal cord segment while FB, FG and DY were injected into the ipsilateral medial pontine nuclei, red nucleus and striatum, respectively. Labeled pyramidal neurons projecting corticospinal axons were contralateral to injection in lamina V and ranged in size from small to large. These CST neurons occupied two distinct cortical areas. The cortical neurons of origin for the corticopontine, corticorubral and corticostriatal fibers were ipsilateral to injections. Labeled neurons were localized in cortical lamina V for the corticopontine and corticorubral fibers while corticostriate neurons were located in laminae III, V and VI. The CP, CR and CS labeled cells occupied one large cortical area which topographically included parts of the medial (AGm) and lateral (AGI) agranular cortices and the primary (SI) somatosensory cortex. Considerable overlapping of the cortical neurons of origin for the four motor fiber systems was apparent. More than 98% of the labeled cells were single labeled while less than 2% were double labeled. No triple or quadruple labeled neurons were observed. Hence, morphological evidence is presented that cortical motor neurons project mainly individual, rather than collateral, axons to each of the four motor associated nuclei investigated in this study. However, only a few cortical neurons projected axons simultaneously to a maximum of two nuclei involved in the motor pathways.

References (55)

  • A. Akintunde et al.

    Differential sites of origin and collateralization of the corticospinal tract in the rat: a multiple retrograde fluorescent tracer study

    Brain Res.

    (1992)
  • G.I. Allen et al.

    Cerebrocerebellar communication systems

    Physiol. Rev.

    (1974)
  • G.I. Allen et al.

    The mode of synaptic linkage in the cerebro-ponto-cerebellar pathway of the cat. II. Responses of single cells in the pontine nuclei

    Exp. Brain Res.

    (1975)
  • M. Bentivoglio et al.

    Retrograde neuronal labeling by means of bisbenzimide and nuclear yellow (Hoeschst S-769121). Measures to prevent diffusion of the tracers out of retrogradely labeled neurons

    Neurosci. Lett.

    (1980)
  • M. Bentivoglio et al.

    Two new fluorescent retrograde neuronal tracers which are transported over long distances

    Neurosci. Lett.

    (1980)
  • M. Bentivoglio et al.

    The cortical projections of the thalamic intralaminar nuclei, as studied in cat and rat with the multiple fluorescent retrograde tracing technique

    Neurosci. Lett.

    (1981)
  • M. Bentivoglio et al.

    Fluorescent retrograde triple labeling of brain stem reticular neurons

    Neurosci. Lett.

    (1984)
  • D. Blake et al.

    Electrophysiological study of cortico-caudate projections in the cat

    J. Neurobiol.

    (1976)
  • P. Brodal

    The corticopontine projection in the cat. I. Demonstration of a somatotopically organized projection from the primary sensorimotor cortex

    Exp. Brain Res.

    (1968)
  • L.T. Brown

    Corticorubral projections in the rat

    J. Comp. Neurol.

    (1974)
  • R.J. Dado et al.

    Evidence that Fluoro-Gold can be transported avidly through fibers of passage

    Brain Res.

    (1990)
  • C. Darian-Smith et al.

    Thalamic projections to sensorimotor cortex in the Macaque monkey: use of multiple retrograde fluorescent tracers

    J. Comp. Neurol.

    (1990)
  • J. De Olmos et al.

    Double and triple labeling of neurons with fluorescent substances; the study of collateral pathways in the ascending raphe system

    Neurosci. Lett.

    (1980)
  • D. Denny-Brown et al.

    The role of the basal ganglia in the initiation of movement

  • J.P. Donoghue et al.

    A collateral pathway to the neostriatum from corticofugal neurons of the rat sensory-motor cortex: an intracellular HRP study

    J. Comp. Neurol.

    (1981)
  • J.P. Donoghue et al.

    The motor cortex of the rat: cytoarchitecture and microstimulation mapping

    J. Comp. Neurol.

    (1982)
  • J.C. Eccles

    Circuits in the cerebellar control of movement

  • K. Endo et al.

    The distribution and pattern of axon branching of pyramidal tract cells

    Brain Res.

    (1973)
  • R.S. Fisher et al.

    Interhemispheric organization of corticocaudate projections in the cat: a retrograde double-labeling study

    Neurosci. Lett.

    (1984)
  • E. Garcia-Rill

    The basal ganglia and the locomotor regions

    Brain Res. Rev.

    (1986)
  • R.D. Hall et al.

    Organization of motor and somatosensory neocortex in the albino rat

    Brain Res.

    (1974)
  • S.P. Hicks et al.

    Locating corticospinal neurons by retrograde axonal transport of horseradish peroxidase

    Exp. Neurol.

    (1977)
  • T. Hongo et al.

    Effects from the sensorimotor cortex on the spinal cord in cats with transected pyramids

    Exp. Brain Res.

    (1967)
  • A.M. Huisman et al.

    Quantitative differences in collateralization of the descending spinal pathways from red nucleus and other brain stem cell groups in rat as demonstrated with the multiple fluorescent retrograde tracer technique

    Brain Res.

    (1981)
  • D.R. Humphrey et al.

    Properties of pyramidal tract neuron system within a functionally defined subregion of primate motor cortex

    J. Neurophysiol.

    (1978)
  • D.R. Humphrey et al.

    Sizes, laminar and topographic origins of cortical projections to the major divisions of the red nucleus in the monkey

    J. Comp. Neurol.

    (1984)
  • D.R. Humphrey et al.

    Cells of origin of corticorubral projections from the arm area of primate motor cortex and their synaptic actions in the red nucleus

    Brain Res.

    (1976)
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