Large-scale reorganization of the somatosensory cortex following spinal cord injuries is due to brainstem plasticity

Nature Communications

Volumn 5, Issue , 2014, Pages

  Kambi, Niranjan ^a   Halder, Priyabrata ^a   Rajan, Radhika ^a   Arora, Vasav ^a   Chand, Prem ^a   Arora, Manika ^a   Jain, Neeraj ^a  

^a NATIONAL BRAIN RESEARCH CENTRE   (India)

Author keywords

[No Author keywords available]

Indexed keywords

LIDOCAINE;

BRAIN; INJURY; MAMMAL; SENSORY SYSTEM;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN STEM; CAPILLARY TUBE; CHIN; CUNEATE NUCLEUS; DEAFFERENTATION; EVOKED RESPONSE; MACACA RADIATA; MALE; MANDIBULAR NERVE; MICROELECTRODE; NERVE CELL PLASTICITY; NONHUMAN; PRIMARY SOMATOSENSORY CORTEX; RECEPTIVE FIELD; RHESUS MONKEY; SPINAL CORD INJURY; TACTILE STIMULATION; THALAMUS; TRIGEMINAL NERVE; TRIGEMINAL NUCLEUS; ANIMAL; FACE; HAND; INNERVATION; MEDULLA OBLONGATA; PATHOPHYSIOLOGY; PHYSIOLOGY; SOMATOSENSORY CORTEX;

MAMMALIA;

ANIMALS; BRAIN STEM; FACE; HAND; MACACA MULATTA; MACACA RADIATA; MALE; MEDULLA OBLONGATA; NEURONAL PLASTICITY; SOMATOSENSORY CORTEX; SPINAL CORD INJURIES;

EID: 84911943871     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms4602     Document Type: Article

References (50)

1. Jain, N., Catania, K. C. & Kaas, J. H. Deactivation and reactivation of somatosensory cortex after dorsal spinal cord injury. Nature 386, 495-498 (1997).
2. Jain, N., Qi, H. X., Collins, C. E. & Kaas, J. H. Large-scale reorganization in the somatosensory cortex and thalamus after sensory loss in macaque monkeys. J. Neurosci. 28, 11042-11060 (2008).
3. Tandon, S., Kambi, N., Lazar, L., Mohammed, H. & Jain, N. Large-scale expansion of the face representation in somatosensory areas of the lateral sulcus after spinal cord injuries in monkeys. J. Neurosci. 29, 12009-12019 (2009).
4. Pollin, B. & Albe-Fessard, D. Organization of somatic thalamus in monkeys with and without section of dorsal spinal tracts. Brain Res. 173, 431-449 (1979).
5. Pons, T. P. et al. Massive cortical reorganization after sensory deafferentation in adult macaques. Science 252, 1857-1860 (1991).
6. Gustin, S. M. et al. Pain and plasticity: is chronic pain always associated with somatosensory cortex activity and reorganization? J. Neurosci. 32, 14874-14884 (2012).
7. Ramachandran, V. S. Behavioral and magnetoencephalographic correlates of plasticity in the adult human brain. Proc. Natl Acad. Sci. USA 90, 10413-10420 (1993).
8. Flor, H. et al. Phantom-limb pain as a perceptual correlate of cortical reorganization following arm amputation. Nature 375, 482-484 (1995).
9. Lotze, M., Flor, H., Grodd, W., Larbig, W. & Birbaumer, N. Phantom movements and pain. An fMRI study in upper limb amputees. Brain 124, 2268-2277 (2001).
10. Cramer, S. C. et al. Harnessing neuroplasticity for clinical applications. Brain 134, 1591-1609 (2011).
11. Fang, P. C., Jain, N. & Kaas, J. H. Few intrinsic connections cross the hand-face border of area 3b of New World monkeys. J. Comp. Neurol. 454, 310-319 (2002).
12. Padberg, J. et al. Thalamocortical connections of parietal somatosensory cortical fields in macaque monkeys are highly divergent and convergent. Cereb. Cortex 19, 2038-2064 (2009).
13. Kaas, J. H., Florence, S. L. & Jain, N. Subcortical contributions to massive cortical reorganizations. Neuron 22, 657-660 (1999).
14. Manger, P. R., Woods, T. M., Munoz, A. & Jones, E. G. Hand/face border as a limiting boundary in the body representation in monkey somatosensory cortex. J. Neurosci. 17, 6338-6351 (1997).
15. Pettit, M. J. & Schwark, H. D. Receptive field reorganization in dorsal column nuclei during temporary denervation. Science 262, 2054-2056 (1993).
16. Schroeder, C. E., Seto, S., Arezzo, J. C. & Garraghty, P. E. Electrophysiological evidence for overlapping dominant and latent inputs to somatosensory cortex in squirrel monkeys. J. Neurophysiol. 74, 722-732 (1995).
17. Jones, E. G. Cortical and subcortical contributions to activity-dependent plasticity in primate somatosensory cortex. Annu. Rev. Neurosci. 23, 1-37 (2000).
18. Buonomano, D. V. & Merzenich, M. M. Cortical plasticity: from synapses to maps. Annu. Rev. Neurosci. 21, 149-186 (1998).
19. Henderson, L. A., Gustin, S. M., Macey, P. M., Wrigley, P. J. & Siddall, P. J. Functional reorganization of the brain in humans following spinal cord injury: evidence for underlying changes in cortical anatomy. J. Neurosci. 31, 2630-2637 (2011).
20. Jones, E. G. & Pons, T. P. Thalamic and brainstem contributions to large-scale plasticity of primate somatosensory cortex. Science 282, 1121-1125 (1998).
21. Kaas, J. H. & Florence, S. L. Mechanisms of reorganization in sensory systems of primates after peripheral nerve injury. Adv. Neurol. 73, 147-158 (1997).
22. Jain, N., Florence, S. L., Qi, H. X. & Kaas, J. H. Growth of new brainstem connections in adult monkeys with massive sensory loss. Proc. Natl Acad. Sci. USA 97, 5546-5550 (2000).
23. Calford, M. B., Wright, L. L., Metha, A. B. & Taglianetti, V. Topographic plasticity in primary visual cortex is mediated by local corticocortical connections. J. Neurosci. 23, 6434-6442 (2003).
24. Darian-Smith, C. & Gilbert, C. D. Axonal sprouting accompanies functional reorganization in adult cat striate cortex. Nature 368, 737-740 (1994).
25. Florence, S. L., Taub, H. B. & Kaas, J. H. Large-scale sprouting of cortical connections after peripheral injury in adult macaque monkeys. Science 282, 1117-1121 (1998).
26. Dancause, N. et al. Extensive cortical rewiring after brain injury. J. Neurosci. 25, 10167-10179 (2005).
27. Graziano, A. & Jones, E. G. Early withdrawal of axons from higher centers in response to peripheral somatosensory denervation. J. Neurosci. 29, 3738-3748 (2009).
28. Sherrington, C. & Denny-Brown, D. On distribution of sensory nerve roots. In Selected writings of Sir Charles Sherrington 31-93 (Hamish Hamilton, 1939).
29. Xu, J. & Wall, J. T. Functional organization of tactile inputs from the hand in the cuneate nucleus and its relationship to organization in the somatosensory cortex. J. Comp. Neurol. 411, 369-389 (1999).
30. Xu, J. & Wall, J. T. Evidence for brainstem and supra-brainstem contributions to rapid cortical plasticity in adult monkeys. J. Neurosci. 19, 7578-7590 (1999).
31. Darian-Smith, C. & Ciferri, M. Cuneate nucleus reorganization following cervical dorsal rhizotomy in the macaque monkey: its role in the recovery of manual dexterity. J. Comp. Neurol. 498, 552-565 (2006).
32. Kambi, N., Tandon, S., Mohammed, H., Lazar, L. & Jain, N. Reorganization of the primary motor cortex of adult macaque monkeys after sensory loss resulting from partial spinal cord injuries. J. Neurosci. 31, 3696-3707 (2011).
33. Price, D. D., Dubner, R. & Hu, J. W. Trigeminothalamic neurons in nucleus caudalis responsive to tactile, thermal, and nociceptive stimulation of monkey's face. J. Neurophysiol. 39, 936-953 (1976).
34. Kerr, F. W., Kruger, L., Schwassmann, H. O. & Stern, R. Somatotopic organization of mechanoreceptor units in the trigeminal nuclear complex of the macaque. J. Comp. Neurol. 134, 127-144 (1968).
35. Jain, N., Florence, S. L. & Kaas, J. H. Reorganization of Somatosensory Cortex After Nerve and Spinal Cord Injury. News Physiol. Sci. 13, 143-149 (1998).
36. Darian-Smith, C. & Brown, S. Functional changes at periphery and cortex following dorsal root lesions in adult monkeys. Nat. Neurosci. 3, 476-481 (2000).
37. Florence, S. L., Hackett, T. A. & Strata, F. Thalamic and cortical contributions to neural plasticity after limb amputation. J. Neurophysiol. 83, 3154-3159 (2000).
38. Garraghty, P. E. & Kaas, J. H. Functional reorganization in adult monkey thalamus after peripheral nerve injury. Neuroreport 2, 747-750 (1991).
39. 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).
40. Darian-Smith, C. Primary afferent terminal sprouting after a cervical dorsal rootlet section in the macaque monkey. J. Comp. Neurol. 470, 134-150 (2004).
41. Darian-Smith, C. & Gilbert, C. D. Topographic reorganization in the striate cortex of the adult cant and monkey is cortically mediated. J. Neurosci. 15, 1631-1647 (1995).
42. Ralston, 3rd H. J., Ohara, P. T., Meng, X. W., Wells, J. & Ralston, D. D. Transneuronal changes of the inhibitory circuitry in the macaque somatosensory thalamus following lesions of the dorsal column nuclei. J. Comp. Neurol. 371, 325-335 (1996).
43. Ergenzinger, E. R., Glasier, M. M., Hahm, J. O. & Pons, T. P. Cortically induced thalamic plasticity in the primate somatosensory system. Nat. Neurosci. 1, 226-229 (1998).
44. Pluto, C. P., Lane, R. D. & Rhoades, R. W. Local GABA receptor blockade reveals hindlimb responses in the SI forelimb-stump representation of neonatally amputated rats. J. Neurophysiol. 92, 372-379 (2004).
45. Dutta, A., Kambi, N., Raghunathan, P., Khushu, S. & Jain, N. Large-scale reorganization of the somatosensory cortex of adult macaque monkeys revealed by fMRI. Brain Struct. Funct. doi:10.1007/s00429-013-0569-8 (2013).
46. Martin, J. H. Autoradiographic estimation of the extent of reversible inactivation produced by microinjection of lidocaine and muscimol in the rat. Neurosci. Lett. 127, 160-164 (1991).
47. Pluto, C. P., Chiaia, N. L., Rhoades, R. W. & Lane, R. D. Reducing contralateral SI activity reveals hindlimb receptive fields in the SI forelimb-stump representation of neonatally amputated rats. J. Neurophysiol. 94, 1727-1732 (2005).
48. Wong-Riley, M. Changes in the visual system of monocularly sutured or enucleated cats demonstrable with cytochrome oxidase histochemistry. Brain Res. 171, 11-28 (1979).
49. Geneser-Jensen, F. A. & Blackstad, T. W. Distribution of acetyl cholinesterase in the hippocampal region of the guinea pig. I. Entorhinal area, parasubiculum, and presubiculum. Z Zellforsch. Mikrosk. Anat. 114, 460-481 (1971).
50. Tandon, S., Kambi, N. & Jain, N. Complete reorganization of the motor cortex of adult rats following long-term spinal cord injuries. Eur. J. Neurosci. 38, 2271-2279 (2013).