Abstract
Chronic peripheral nerve injuries produce neural changes at different levels of the somatosensory pathway, but these responses remain poorly defined. We selectively removed cutaneous input from the index finger and thumb in young adult macaque monkeys by lesioning dorsal rootlets to examine both immediate and long-term systemic responses to this deficit. Corresponding digit representations within somatosensory cortex (SI) were initially silenced, but two to seven months later again responded to cutaneous stimulation of the ‘deafferented’ digits. We remapped cutaneous receptive fields (RFs) within adjacent intact dorsal rootlets two to four months after lesioning. RF distributions had greatly expanded, so that rootlets previously innervating adjacent hand regions now responded to stimulation of the index finger and/or thumb. Thus our results demonstrate peripherally mediated central reorganization.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 12 print issues and online access
$209.00 per year
only $17.42 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Buonomano, D. V. & Merzenich, M. M. Cortical plasticity: from synapses to maps. Annu. Rev. Neurosci. 21, 149–186 (1998).
Calford, M. B. & Tweedale, R. Immediate and chronic changes in responses of somatosensory cortex in adult flying-fox after digit amputation. Nature 332, 446–448 (1988).
Kaas, J. H. Plasticity of sensory and motor maps in adult mammals. Annu. Rev. Neurosci. 14, 137–167 (1991).
Kelahan, A. M. & Doetsch, G. S. Time-dependent changes in the functional organization of somatosensory cerebral cortex following digit amputation in adult raccoons. Somatosens. Res. 2, 49–81 (1984).
Merzenich, M. M. et al. Progression of change following median nerve section in the cortical representations of the hand in areas 3b and 1 in adult owl and squirrel monkeys. Neuroscience 10, 639–665 (1983).
Merzenich, M. M. et al. Somatosensory cortical map changes following digital amputation in adult monkeys. J. Comp. Neurol. 224, 591–605 (1984).
Florence, S. L., Garraghty, P. E., Carlson, M. & Kaas, J. H. Sprouting of peripheral nerve axons in the spinal cord of monkeys. Brain Res. 601, 343–348 (1993).
Kaas, J. H. & Florence, S. L. Mechanisms of reorganization in sensory systems of primates after peripheral nerve injury. Adv. Neurol. 73, 147–158 (1997).
Kaas, J. H., Florence, S. L. & Jain, N. Subcortical contributions to massive cortical reorganizations. Neuron 22, 657–660 (1999).
Snow, P. J. & Wilson, P. Progress in Sensory Physiology (Springer, Berlin, 1991).
Florence, S. L. & Kaas, J. H. Large scale reorganization at multiple levels of the somatosensory pathway follows therapeutic amputation of the hand in monkeys. J. Neurosci. 15, 8083–8095 (1995).
Heinen, S. J. & Skavenski, A. A. Recovery of visual responses in foveal V1 neurons following bilateral foveal lesions in adult monkey. Exp. Brain Res. 83, 670–674 (1991).
Darian-Smith, C. & Gilbert, C. D. Topographic reorganization in the striate cortex of the adult cat and monkey is cortically mediated. J. Neurosci. 15, 1631–1647 (1995).
Gilbert C. D. & Darian-Smith, C. in Fifth Conference on the Neurobiology of Learning and Memory 293–301 (Oxford Univ. Press, 1995).
Florence, S. L. et al. Central reorganisation of sensory pathways following peripheral nerve regeneration in fetal monkeys. Nature 381, 69–71 (1996).
Sherrington, C. S. in Textbook of Physiology Vol. II 920–1001 (Pentland, London, 1900).
Willis, W. D. & Coggeshall, R. E. Sensory Mechanisms of the Spinal Cord, 2nd Ed. (Plenum, New York, 1991).
Sunderland, S. Nerve Injuries and Their Repair. A Critical Appraisal (Churchill Livingstone, New York, 1991).
Basbaum, A. I. & Wall, P. D. Chronic changes in the response of cells in adult cat dorsal horn following partial deafferentation: the appearance of responding cells in a previously non-responsive region. Brain Res. 116, 181–204 (1976).
Mendell, L. M., Sassoon, E. M. & Wall, P. D. Properties of synaptic linkage from long ranging afferents onto dorsal horn neurones in normal and deafferented cats. J. Physiol. (Lond.) 285, 299–310 (1978).
Sedivec, M. J., Ovelmen-Levitt, J., Karp, R. & Mendell, L. M. Increase in nociceptive input to spinocervical tract neurons following chronic partial deafferentation. J. Neurosci. 3, 1511–1519 (1983).
Pons, T. P. et al. Massive reorganization of the primary somatosensory cortex after peripheral sensory deafferentation. Science 252, 1857–1860 (1991).
Rausell, E., Cusick, C. G., Taub, E. & Jones, E. G. Chronic deafferentation in monkeys differentially affects nociceptive and nonnociceptive pathways distinguished by calcium-binding proteins and down-regulates λ-aminobutyric acid type A receptors at thalamic levels. Proc. Natl. Acad. Sci. USA 89, 2571–2575 (1992).
Jones, E. G. & Pons, T. P. Thalamic and brainstem contributions to large-scale plasticity of primate somatosensory cortex. Science 282, 1121–1125 (1998).
Nelson, R. J., Sur, M., Felleman, D. J. & Kaas, J. H. Representations of the body surface in postcentral parietal cortex of Macaca fascicularis. J. Comp. Neurol. 192, 611–643 (1980).
Kaas. J. H., Nelson, R. J., Sur, M., Lin, C. S. & Merzenich, M. M. Multiple representations of the body within the primary somatosensory cortex of primates. Science 204, 521–523 (1979).
Jenkins, W. M., Merzenich, M. M., Ochs, M. T., Allard, T. & Guic, R. E. Functional reorganization of primary somatosensory cortex in adult owl monkeys after behaviourally controlled tactile stimulation. J. Neurophysiol. 63, 82–104 (1990).
Edeline, J. M. Learning-induced physiological plasticity in the thalamo-cortical sensory systems: a critical evaluation of receptive field plasticity, map changes and their potential mechanisms. Prog. Neurobiol. 57, 165–224 (1999).
Jain, N., Catania, K. C. & Kaas, J. H. Deactivation and reactivation of somatosensory cortex after dorsal spinal cord injury. Nature 386, 495–498 (1997).
Galea, M. P. & Darian-Smith, I. Corticospinal projection patterns following unilateral section of the cervical spinal cord in the newborn and juvenile macaque monkey. J. Comp. Neurol. 381, 282–306 (1997).
Koerber, H. R., Mirnics, K. & Mendell, M. Properties of regenerated primary afferents and their functional connections. J. Neurophysiol. 73, 693–701 (1995).
Healy, C., LeQuesne, P. M. & Lynn, B. Collateral sprouting of cutaneous nerves in man. Brain 119, 2063–2072 (1996).
Devor, M. & Wall, P. D. Reorganization of spinal cord sensory map after peripheral nerve injury. Nature 276, 75–76 (1978).
Rodin, B. E., Sampogna, S. L. & Kruger, L. An examination of intraspinal sprouting in dorsal root axons with the tracer horseradish peroxidase. J. Comp. Neurol. 215, 187–198 (1983).
LaMotte, C. C. & Kapadia, S. E. Deafferentation-induced terminal field expansion of myelinated saphenous afferents in the adult rat dorsal horn and the nucleus gracilis following pronase injection of the sciatic nerve. J. Comp. Neurol. 330, 83–94 (1993).
McMahon, S. B. & Kett-White, R. Sprouting of peripherally regenerating primary sensory neurones in the adult central nervous system. J. Comp. Neurol. 304, 307–315 (1991).
Woolf, C. J., Shortland, P. & Coggeshall, R. E. Peripheral nerve injury triggers central sprouting of myelinated afferents. Nature 355, 75–78 (1992).
Fitzgerald, M., Woolf, C. J. & Shortland, P. Collateral sprouting of the central terminals of cutaneous primary afferent neurons in the rat spinal cord: pattern, morphology, and influence of targets. J. Comp. Neurol. 300, 370–385 (1990).
Cameron, A. A., Pover, C. M., Willis, W. D. & Coggeshall, R.E. Evidence that fine primary afferent axons innervate a wider territory in the superficial dorsal horn following peripheral axotomy. Brain Res. 575, 151–154 (1992).
Tong, Y.-G. et al. Increased uptake and transport of cholera toxin B-subunit in dorsal root ganglion neurons after peripheral axotomy: possible implications for sensory sprouting. J. Comp. Neurol. 404, 143–158 (1999).
Acknowledgements
This work was supported by Project Grants 960246 and 990097 awarded by the Australian NHMRC. We thank Ken Miller and Tony Goodwin for comments on the manuscript.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Darian-Smith, C., Brown, S. Functional changes at periphery and cortex following dorsal root lesions in adult monkeys. Nat Neurosci 3, 476–481 (2000). https://doi.org/10.1038/74852
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1038/74852
This article is cited by
-
Formation of somatosensory detour circuits mediates functional recovery following dorsal column injury
Scientific Reports (2020)
-
Increased cortical responses to forepaw stimuli immediately after peripheral deafferentation of hindpaw inputs
Scientific Reports (2014)
-
Large-scale reorganization of the somatosensory cortex following spinal cord injuries is due to brainstem plasticity
Nature Communications (2014)
-
Plasticity in Cortical Motor Upper-Limb Representation Following Stroke and Rehabilitation: Two Longitudinal Multi-Joint fMRI Case-Studies
Brain Topography (2012)
-
Neurotrophins: Potential Therapeutic Tools for the Treatment of Spinal Cord Injury
Neurotherapeutics (2011)