Elsevier

Neuroscience

Volume 200, 3 January 2012, Pages 19-30
Neuroscience

Cognitive, Behavioral, and Systems Neuroscience
Research Paper
Spatial characterization of the motor neuron columns supplying the rat forelimb

https://doi.org/10.1016/j.neuroscience.2011.10.054Get rights and content

Abstract

Rats can generate a rich array of forepaw and forelimb movements that are similar, although not as complex, to those produced by human and non-human primates. When reaching for food for instance, rats display skilled movements of the forelimb and the paw, therefore, making them attractive models to validate strategies aimed at the recovery of fine motor control. Surprisingly however, few anatomical studies have been performed on the central control of forelimb movements in the rat. The current series of experiments examined the details of the segmental arrangement of motor neurons that supply the rat forelimb. The distribution of motor end plates across the rat forelimb was first visualized by means of acetylcholinesterase histochemistry, and this information was used to create a motor end plate map of the forelimb muscles. This map was subsequently used as a guide for multiple injections of retrograde tracers along the motor end plate regions of 11 forelimb muscles. The entire cervical region of the spinal cord was subsequently analyzed under epifluorescence. This tract-tracing analysis confirmed that motor neurons innervating the rat forelimb are arranged in columns within the cervical segments of the spinal cord. This anatomical investigation also supports the previous observation that, although discrete, some of the motor neuron columns lying in the cervical aspect of the rat spinal cord are inter-mingled. The length of these columns, and hence the overlap between them, appears to be greater than previously reported, particularly within the uppermost segments of the brachial plexus.

Highlights

▶In this study we provided a map of the motor end plates for 11 rat forelimb muscles. ▶We characterized the spatial distribution of the motor columns supplying these muscles. ▶The length and the overlap between some motor neuron columns is greater than previously described. ▶The upper cervical enlargement contains more motor neuron columns than previously reported. ▶This provides a greater understanding of the organization of the motor columns for the rat forelimb.

Section snippets

Animals

All experimental procedures complied with the Animal Care and Ethics Committee of the University of New South Wales and were performed in accordance with the National Health and Medical Research Council of Australia regulations for animal experimentation. A total of 27 adult female hooded rats (Rattus norvegicus; Long-Evans) (Monash University, Victoria, Australia) weighing approximately 250 g at the time of surgery were used in this study. The rats were housed in groups of four in an animal

Localization of the motor end plates in the rat forelimb

The location of the motor end plates in each muscle under investigation is shown in Fig. 1, Fig. 2. Fig. 1 is a photograph of the lateral view of a rat forelimb processed with an aceytlcholinesterase reaction that reveals the motor end plate regions. On this photograph, the motor end plates appear as black speckles aligned on the brown muscle fibres. Moreover, Fig. 1 also shows the direction of the muscle fibres in situ. Analysis of the lateral, ventral, and dorsal views of the forelimbs used

Discussion

The aim of this research was to characterize the details of the spatial organization of the columns of motor neurons that supply the musculature of the rat forelimb. Particular attention was given to identify the degree of overlap between these motor columns that lie in the cervical segments of the spinal cord and that has been incidentally reported (McKenna et al., 2000). Special emphasis was also placed on the number of motor neuron columns spanning the cervical enlargement. The results of

Conclusion

This anatomical investigation supports previous observations that, although discrete, some of the motor neuron columns lying in the cervical aspect of the rat spinal cord are inter-digitized. The length of these columns, and hence the overlap between them, appears to be greater than previously reported, particularly within the uppermost segments of the cervical enlargement. This map constitutes a valuable guide for the selection of appropriate muscle(s) for the delivery of therapeutic genes

Acknowledgments

The research was supported by the Christopher and Dana Reeve Foundation (Renée Morris) and by a University of New South Wales Faculty of Medicine Research Grant (Renée Morris).

References (80)

  • A.R. Iliya et al.

    Somatotopic relations between the motor nucleus and its innervated muscle fibres in the cat tibialis anterior

    Exp Neurol

    (1984)
  • A.N. Iwaniuk et al.

    On the origin of skilled forelimb movements

    Trends Neurosci

    (2000)
  • S.G. Kanagal et al.

    Task-dependent compensation after pyramidal tract and dorsolateral spinal lesions in rats

    Exp Neurol

    (2009)
  • Y. Liu et al.

    Grafts of BDNF-producing fibroblasts rescue axotomised rubrospinal neurons and prevent their atrophy

    Exp Neurol

    (2002)
  • M. Mutai et al.

    Somatotopic organization of motoneurons innervating the pronators, carpal and digital flexors and forepaw muscles in the dog: a retrograde horseradish peroxidase study

    Brain Res

    (1986)
  • B. Rexed

    Some aspects of the cytoarchitecture and synaptology of the spinal cord

  • G.J. Romanes

    The motor pools of the spinal cord

  • L.-A.R. Sacrey et al.

    Rodent model of human skilled reaching

    Behav Brain Res

    (2009)
  • G.W. Schrimsher et al.

    Forelimb motor performance following dorsal column, dorsolateral funiculi, or ventrolateral funiculi lesions of the cervical spinal cord in the rat

    Exp Neurol

    (1993)
  • I.Q. Whishaw et al.

    Varieties of paw and digit movement during spontaneous food handling in rats: postures, bimanual co-ordination, preferences, and the effect of forelimb cortex lesions

    Behav Brain Res

    (1996)
  • I.Q. Whishaw et al.

    Arpeggio and fractionated digit movements used in prehension by rats

    Behav Brain Res

    (1994)
  • I.Q. Whishaw et al.

    Does the red nucleus provide the tonic support against which fractionated movements occur?A study on forepaw movements used in skilled reaching by the rat

    Behav Brain Res

    (1996)
  • I.Q. Whishaw et al.

    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

    (1998)
  • I.Q. Whishaw et al.

    Red nucleus lesions do not affect limb preference or use, but exacerbate the effects of motor cortex lesions on grasping in the rat

    Behav Brain Res

    (1990)
  • M. Xiao et al.

    Human adult olfactory neural progenitors rescue axotomized rodent rubrospinal neurons and promote functional recovery

    Exp Neurol

    (2005)
  • M. Xiao et al.

    Human adult olfactory neural progenitors promote axotomised rubrospinal tract axonal reinnervation and locomotor recovery

    Neurol Dis

    (2007)
  • B.J. Baumgartner et al.

    Neuroprotection of CNS neuron by retrograde transport of adenoviral vectors carrying neurotrophic genes

    J Neurosci

    (1997)
  • B.J. Baumgartner et al.

    Permanent rescue of lesioned motoneurons and enhanced axonal regeneration by adenovirus mediated expression of glial cell·line derived neurotrophic factor

    J Neurosci Res

    (1998)
  • D.H. Beerman et al.

    A combined silver and acetylcholinesterase method for staining intramuscular innervation

    Stain Technol

    (1976)
  • M.R. Bennet et al.

    Death of motorneurons during the postnatal loss of polyneuronal innervation of rat muscles

    J Comp Neurol

    (1983)
  • J.A. Bertelli et al.

    The rat brachial plexus and its terminal branches: an experimental model for the study of peripheral nerve regeneration

    Microsurgery

    (1995)
  • N.M. Boulis et al.

    Intraneural colchicine inhibition of adenoviral and adeno-associated viral vector remote spinal cord gene delivery

    Neurosurgery

    (2003)
  • A.M. Brichta et al.

    Quantitative analysis of cervical musculature in rats: histochemical composition and motor pool organizationI. Muscles of the spinal accessory complex

    J Comp Neurol

    (1987)
  • R.J. Callister et al.

    Quantitative analysis of cervical musculature in rats: histochemical composition and motor pool organizationII. Deep dorsal muscles

    J Comp Neurol

    (1987)
  • M.A. Cenci et al.

    Animal models of neurological deficits: how relevant is the rat?

    Nat Rev Neurosci

    (2002)
  • J.R. Coonan et al.

    Role of EphA4 in defining the position of a motoneurons pool within the spinal cord

    J Comp Neurol

    (2003)
  • O.A. Gharbawie et al.

    Recovery of skilled reaching following motor cortex stroke: do residual corticofugal fibres mediate compensatory recovery?

    Eur J Neurosci

    (2007)
  • E.C. Greene

    Anatomy of the ratTransactions of the American Philosophical Society

    (1935)
  • E.C. Greene
    (1955)
  • R. Hebel et al.

    Anatomy of the laboratory rat

    (1976)
  • Cited by (63)

    View all citing articles on Scopus
    View full text