Home LiteratureArticle Details
PMID: 10024372 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Complete compensation in skilled reaching success with associated impairments in limb synergies, after dorsal column lesion in the rat.

The Journal of neuroscience : the official journal of the Society for Neuroscience ·Vol. 19 ·No. 5 ·1999-03-01 ·Pages 1885-94

McKenna JE, Whishaw IQ

Abstract

Each of the dorsal columns of the rat spinal cord conveys primary sensory information, by way of the medullary dorsal column nucleus, to the ventrobasal thalamus on the contralateral side; thus the dorsal columns are an important source of neural input to the sensorimotor cortex. Damage to the dorsal columns causes impairments in synergistic proximal or whole-body movements in cats and distal limb impairments in primates, particularly in multiarticulated finger movements and tactile foviation while handling objects, but the behavioral effects of afferent fiber lesions in the dorsal columns of rodents have not been described. Female Long-Evans rats were trained to reach with a forelimb for food pellets and subsequently received lesions of the dorsomedial spinal cord at the C2 level, ipsilateral to their preferred limb. Reaching success completely recovered within a few days of dorsal column lesion. Nevertheless, a detailed analysis of high-speed video recordings revealed that rotatory limb movements (aiming, pronation, supination, etc.) were irreversibly impaired. Compensation was achieved with whole-body and alternate limb movements. These results indicate the following: (1) in the absence of the dorsal columns, other sensorimotor pathways support endpoint success in reaching; (2) sensory input conveyed by the dorsal columns is important for both proximal and distal limb movements used for skilled reaching; and (3) detailed behavioral analyses in addition to endpoint measures are necessary to completely describe the effects of dorsal column lesions.

MeSH Terms
Animals Behavior, Animal/physiology Female Forelimb/physiology Movement/physiology Psychomotor Performance/physiology Rats Rats, Long-Evans Recovery of Function/physiology Spinal Cord/pathology,physiology Spinal Cord Injuries/physiopathology Video Recording
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
McKenna J E
Department of Psychology and Neuroscience, University of Lethbridge, Alberta, Canada, T1K 3M4.
Whishaw I Q
References (62)
62 references, click to expand
  1. Differential origins of spinothalamic tract projections to medial and lateral thalamus in the rat.
    J Comp Neurol. 1979 Mar 1;184(1):107-26 PMID: 84002
  2. Remodeling of dorsal column nuclear efferents to the basilar pontine gray after cortical ablations in newborn rats.
    Brain Res. 1987 Mar 17;406(1-2):302-7 PMID: 3567629
  3. Fetal cortical transplants into neonatal rats respond to thalamic and peripheral stimulation in the adult. An electrophysiological study of single-unit activity.
    Brain Res. 1989 Jul 24;493(1):33-40 PMID: 2776008
  4. Olfaction directs skilled forelimb reaching in the rat.
    Behav Brain Res. 1989 Feb 1;32(1):11-21 PMID: 2930630
  5. Adaptive behavioral reactions of reaching in rats following discrete somatosensorimotor cortex lesions.
    Physiol Behav. 1996 Feb;59(2):255-63 PMID: 8838603
  6. The impairments in reaching and the movements of compensation in rats with motor cortex lesions: an endpoint, videorecording, and movement notation analysis.
    Behav Brain Res. 1991 Jan 31;42(1):77-91 PMID: 2029348
  7. A behavioral study of the contributions of cells and fibers of passage in the red nucleus of the rat to postural righting, skilled movements, and learning.
    Behav Brain Res. 1992 Nov 30;52(1):29-44 PMID: 1472285
  8. Deficient influence of peripheral stimuli on precentral neurones in monkeys with dorsal column lesions.
    J Physiol. 1978 Mar;276:27-48 PMID: 418170
  9. Regeneration of lesioned corticospinal tract fibers in the adult rat spinal cord under experimental conditions.
    Spinal Cord. 1997 Jul;35(7):469-73 PMID: 9232753
  10. Fetal spinal cord transplants support the development of target reaching and coordinated postural adjustments after neonatal cervical spinal cord injury.
    J Neurosci. 1998 Jan 15;18(2):763-78 PMID: 9425018
  11. Effects of a dorsal column lesion on temporal processing within the somatosensory system of primates.
    Exp Brain Res. 1996 Nov;112(2):253-67 PMID: 8951394
  12. Fetal spinal cord transplants support growth of supraspinal and segmental projections after cervical spinal cord hemisection in the neonatal rat.
    J Neurosci. 1998 Jan 15;18(2):779-93 PMID: 9425019
  13. Motor recovery after serial spinal cord lesions of defined descending pathways in cats.
    Neurosci Res. 1987 Oct;5(1):68-73 PMID: 3431751
  14. Topographic organization of convergent projections to the thalamus from the inferior colliculus and spinal cord in the rat.
    J Comp Neurol. 1987 Oct 1;264(1):123-46 PMID: 2445791
  15. Collaterals of spinothalamic cells in the rat.
    J Comp Neurol. 1983 Apr 20;215(4):453-64 PMID: 6863593
  16. The reaching reaction in the rat: a part of the digging pattern?
    Behav Brain Res. 1990 Jan 1;36(1-2):53-64 PMID: 2302321
  17. Impairments of reaching movements in patients without proprioception. I. Spatial errors.
    J Neurophysiol. 1995 Jan;73(1):347-60 PMID: 7714577
  18. Proximal and distal impairments in rat forelimb use in reaching follow unilateral pyramidal tract lesions.
    Behav Brain Res. 1993 Jul 30;56(1):59-76 PMID: 7691077
  19. The effects of cortical ablations on digital usage in the rat.
    Brain Res. 1972 Feb 25;37(2):173-85 PMID: 5061111
  20. The structure of skilled forelimb reaching in the rat: a proximally driven movement with a single distal rotatory component.
    Behav Brain Res. 1990 Dec 7;41(1):49-59 PMID: 2073355
  21. Lack of a proprioceptive deficit after dorsal column lesions in monkeys.
    Neurology. 1993 Feb;43(2):363-6 PMID: 8437703
  22. The effect of fasciculus cuneatus lesions on finger positioning and long-latency reflexes in monkeys.
    Exp Brain Res. 1993;93(1):104-16 PMID: 8467880
  23. Heterotopic neocortical transplants. An anatomical and electrophysiological analysis of host projections to occipital cortical grafts placed into sensorimotor cortical lesions made in newborn rats.
    Brain Res Dev Brain Res. 1991 Feb 22;58(2):231-6 PMID: 1851470
  24. Manual dexterity and corticospinal connectivity following unilateral section of the cervical spinal cord in the macaque monkey.
    J Comp Neurol. 1997 May 12;381(3):307-19 PMID: 9133570
  25. Anatomical studies of the spinocervical tract of the rat.
    Somatosens Res. 1984;2(1):1-18 PMID: 6505460
  26. Repair of adult rat corticospinal tract by transplants of olfactory ensheathing cells.
    Science. 1997 Sep 26;277(5334):2000-2 PMID: 9302296
  27. Schwann cells induce sprouting in motor and sensory axons in the adult rat spinal cord.
    J Neurosci. 1994 Jul;14(7):4050-63 PMID: 8027762
  28. Functional recovery and enhanced corticofugal plasticity after unilateral pyramidal tract lesion and blockade of myelin-associated neurite growth inhibitors in adult rats.
    J Neurosci. 1998 Jun 15;18(12):4744-57 PMID: 9614248
  29. Comparison of forelimb and hindlimb motor deficits following dorsal column section in monkeys.
    Brain Res. 1978 May 12;146(2):279-94 PMID: 417758
  30. Effects of spinal tractotomy on spatial sequence recognition in macaques.
    J Neurosci. 1983 Feb;3(2):280-90 PMID: 6822864
  31. Implantation of stimulated homologous macrophages results in partial recovery of paraplegic rats.
    Nat Med. 1998 Jul;4(7):814-21 PMID: 9662373
  32. Neurotrophic factors increase axonal growth after spinal cord injury and transplantation in the adult rat.
    Exp Neurol. 1997 Dec;148(2):475-94 PMID: 9417827
  33. Thalamic afferents from the spinal cord and trigeminal nuclei. An experimental anatomical study in the rat.
    J Comp Neurol. 1967 Aug;130(4):313-28 PMID: 6059371
  34. Central projections of C4-C8 dorsal root ganglia in the rat studied by anterograde transport of WGA-HRP.
    J Comp Neurol. 1990 Feb 15;292(3):349-62 PMID: 1692849
  35. The contributions of motor cortex, nigrostriatal dopamine and caudate-putamen to skilled forelimb use in the rat.
    Brain. 1986 Oct;109 ( Pt 5):805-43 PMID: 3779371
  36. 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 Jan;74(1-2):79-90 PMID: 8851917
  37. Altered precision grasping in stumptail macaques after fasciculus cuneatus lesions.
    Somatosens Mot Res. 1992;9(1):61-73 PMID: 1595322
  38. Alterations of natural hand movements after interruption of fasciculus cuneatus in the macaque.
    Somatosens Mot Res. 1992;9(1):75-89 PMID: 1595323
  39. The role of dorsal columns in serial order acts.
    Exp Neurol. 1971 Oct;33(1):93-102 PMID: 5287034
  40. 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 Jun;93(1-2):167-83 PMID: 9659998
  41. A comparative topographical analysis of dorsal column nuclear and cerebral cortical projections to the basilar pontine gray in rats.
    J Comp Neurol. 1986 Feb 8;244(2):163-73 PMID: 2419371
  42. Arpeggio and fractionated digit movements used in prehension by rats.
    Behav Brain Res. 1994 Jan 31;60(1):15-24 PMID: 8185848
  43. Forelimb motor performance following cervical spinal cord contusion injury in the rat.
    Exp Neurol. 1992 Sep;117(3):287-98 PMID: 1397165
  44. Reaching behavior in the rat: absence of forelimb peripheral input.
    Physiol Behav. 1992 Jun;51(6):1151-6 PMID: 1641415
  45. Spontaneous forelimb grasping in free feeding by rats: motor cortex aids limb and digit positioning.
    Behav Brain Res. 1992 Jun 8;48(2):113-25 PMID: 1616602
  46. Effects of spinal lesions on temporal resolution of cutaneous sensations.
    Somatosens Res. 1985;3(1):45-56 PMID: 4070892
  47. Integration in descending motor pathways controlling the forelimb in the cat. 9. Differential behavioural defects after spinal cord lesions interrupting defined pathways from higher centres to motoneurones.
    Exp Brain Res. 1981;42(3-4):299-318 PMID: 7238672
  48. 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. (Golgi and electron microscopic observations).
    Z Zellforsch Mikrosk Anat. 1966;71(3):298-363 PMID: 6011377
  49. Sprouts from cut corticospinal axons persist in the presence of astrocytic scarring in long-term lesions of the adult rat spinal cord.
    Exp Neurol. 1995 Jul;134(1):102-11 PMID: 7672031
  50. Absolute and differential sensitivities to touch stimuli after spinal cord lesions in monkeys.
    Brain Res. 1977 Oct 14;134(3):529-39 PMID: 409453
  51. Manual motor performance in a deafferented man.
    Brain. 1982 Sep;105 (Pt 3):515-42 PMID: 6286035
  52. Rescuing neurons from trans-synaptic degeneration after brain damage: helpful, harmful, or neutral in recovery of function?
    Can J Psychol. 1990 Jun;44(2):276-92 PMID: 2166618
  53. Finger movement deficits in the stumptail macaque following lesions of the fasciculus cuneatus.
    Somatosens Mot Res. 1993;10(1):17-29 PMID: 8484293
  54. Forelimb motor performance following dorsal column, dorsolateral funiculi, or ventrolateral funiculi lesions of the cervical spinal cord in the rat.
    Exp Neurol. 1993 Apr;120(2):264-76 PMID: 8491282
  55. Spinal cord repair in adult paraplegic rats: partial restoration of hind limb function.
    Science. 1996 Jul 26;273(5274):510-3 PMID: 8662542
  56. Spinal cord injury and anti-NGF treatment results in changes in CGRP density and distribution in the dorsal horn in the rat.
    Exp Neurol. 1997 Oct;147(2):463-75 PMID: 9344570
  57. Organization of spinothalamic tract axons within the rat spinal cord.
    J Comp Neurol. 1981 Jan 10;195(2):243-52 PMID: 6788822
  58. Spinal afferents to the ventrobasal thalamic complex in the rat: an anatomical study using wheat-germ agglutinin conjugated to horseradish peroxidase.
    Brain Res. 1983 Nov 14;278(1-2):240-4 PMID: 6315154
  59. Motor control in humans with large-fiber sensory neuropathy.
    Hum Neurobiol. 1985;4(2):101-14 PMID: 2993208
  60. A quantifiable model of axonal regeneration in the demyelinated adult rat spinal cord.
    Exp Neurol. 1998 Jun;151(2):303-13 PMID: 9628765
  61. Sensory effects in man of lesions of the posterior columns and of some other afferent pathways.
    Brain. 1986 Oct;109 ( Pt 5):1003-41 PMID: 3096488
  62. Ascending spinal influences on rubrospinal cells in the cat.
    Exp Brain Res. 1997 Sep;116(2):326-40 PMID: 9348131
Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
0270-6474
Published
1999-03-01
Pages
1885-94
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC6782168
Subset
IM
External Links
PubMed source PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2