The reactivation of somatosensory cortex and behavioral recovery after sensory loss in mature primates

Frontiers in Systems Neuroscience

Volumn 8, Issue MAY, 2014, Pages

  Qi, Hui Xin ^a   Kaas, Jon H ^a   Reed, Jamie L ^a  

^a VANDERBILT UNIVERSITY   (United States)

Author keywords

Area 3b; Cuneate nucleus; Monkey; Plasticity; Somatosensory system; Spinal cord; Ventroposterior nucleus

Indexed keywords

CHONDROITIN ABC LYASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; BEHAVIOR; CONTROLLED STUDY; HAPLORHINI; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; REVIEW; SENSORY DYSFUNCTION; SOMATOSENSORY CORTEX; SPINAL CORD DORSAL HORN; SPINAL CORD LESION; SYNAPSE; TASK PERFORMANCE;

EID: 84900540740     PISSN: 16625137     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnsys.2014.00084     Document Type: Review

References (156)

1. Aguilar, J., Humanes-Valera, D., Alonso-Calvino, E., Yague, J. G., Moxon, K. A., Oliviero, A., et al. (2010). Spinal cord injury immediately changes the state of the brain. J. Neurosci. 30, 7528-7537.doi: 10.1523/JNEUROSCI.0379-10.2010
2. Anderson, K. D., Gunawan, A., and Steward, O. (2005). Quantitative assessment of forelimb motor function after cervical spinal cord injury in rats: relationship to the corticospinal tract. Exp. Neurol. 194, 161-174.doi: 10.1016/j.expneurol.2005.02.006
3. Azulay, A., and Schwartz, A. S. (1975). The role of the dorsal funiculus of the primate in tactile discrimination. Exp. Neurol. 46, 315-332.doi: 10.1016/0014-4886(75)90138-7
4. Ballermann, M., McKenna, J., and Whishaw, I. Q. (2001). A grasp-related deficit in tactile discrimination following dorsal column lesion in the rat. Brain Res. Bull. 54, 237-242.doi: 10.1016/S0361-9230(01)00431-2
5. Beck, C. (1976). Forelimb performance by squirrel monkeys (Saimiri sciureus) before and after dorsal column lesions. J. Comp. Physiol. Psychol. 90, 353-362.doi: 10.1037/h0077206
6. Bennett, G. J., Seltzer, Z., Lu, G. W., Nishikawa, N., and Dubner, R. (1983). The cells of origin of the dorsal column postsynaptic projection in the lum-bosacral enlargements of cats and monkeys. Somatosens Res. 1, 131-149.doi: 10.3109/07367228309144545
7. Bowes, C., Burish, M., Cerkevich, C., and Kaas, J. (2013). Patterns of cortical reorganization in the adult marmoset after a cervical spinal cord injury. J. Comp. Neurol. 521, 3451-3463.doi: 10.1002/cne.23360
8. Bowes, C., Massey, J. M., Burish, M., Cerkevich, C. M., and Kaas, J. H. (2012). Chondroitinase ABC promotes selective reactivation of somatosensory cortex in squirrel monkeys after a cervical dorsal column lesion. Proc. Natl. Acad. Sci. U.S.A. 109, 2595-2600.doi: 10.1073/pnas.1121604109
9. Bradbury, E. J., and McMahon, S. B. (2006). Spinal cord repair strategies: why do they work? Nat. Rev. Neurosci. 7, 644-653.doi: 10.1038/nrn1964
10. Bradbury, E. J., Moon, L. D., Popat, R. J., King, V. R., Bennett, G. S., Patel, P. N., et al. (2002). Chondroitinase ABC promotes functional recovery after spinal cord injury. Nature 416, 636-640.doi: 10.1038/416636a
11. Brugger, P., Kollias, S. S., Muri, R. M., Crelier, G., Hepp-Reymond, M. C., and Regard, M. (2000). Beyond re-membering: phantom sensations of con-genitally absent limbs. Proc. Natl. Acad. Sci. U.S.A. 97, 6167-6172.doi: 10.1073/pnas.100510697
12. Buchli, A. D., and Schwab, M. E. (2005). Inhibition of Nogo: a key strategy to increase regeneration, plasticity and functional recovery of the lesioned central nervous system. Ann. Med. 37, 556-567.doi: 10.1080/07853890500407520
13. Buonomano, D. V., and Merzenich, M. M. (1998). Cortical plasticity: from synapses to maps. Annu. Rev. Neurosci. 21, 149-186.doi: 10.1146/annurev.neuro.21.1.149
14. Burton, H., Sathian, K., and Shao, D. H. (1990). Altered responses to cutaneous stimuli in the second somatosensory cortex following lesions of the postcen-tral gyrus in infant and juvenile macaques. J. Comp. Neurol. 291, 395-414.doi: 10.1002/cne.902910307
15. Cafferty, W. B., McGee, A. W., and Strittmatter, S. M. (2008). Axonal growth therapeutics: regeneration or sprouting or plasticity? Trends Neurosci. 31, 215-220.doi: 10.1016/j.tins.2008.02.004
16. Calford, M. B., and Tweedale, R. (1988). Immediate and chronic changes in responses of somatosensory cortex in adult flying-fox after digit amputation. Nature 332, 446-448.doi: 10.1038/332446a0
17. Cheetham, C. E., Hammond, M. S., McFarlane, R., and Finnerty, G. T. (2008). Altered sensory experience induces targeted rewiring of local excitatory connections in mature neocortex. J. Neurosci. 28, 9249-9260.doi: 10.1523/JNEUROSCI.2974-08.2008
18. Chen, L. M., Qi, H. X., and Kaas, J. H. (2012). Dynamic reorganization of digit representations in somatosensory cortex of nonhuman primates after spinal cord injury. J. Neurosci. 32, 14649-14663.doi: 10.1523/JNEUROSCI.1841-12.2012
19. Chino, Y., Smith, E. L. 3rd, Zhang, B., Matsuura, K., Mori, T., and Kaas, J. H. (2001). Recovery of binocular responses by cortical neurons after early monocular lesions. Nat. Neurosci. 4, 689-690.doi: 10.1038/89469
20. Chino, Y. M., Smith, E. L. 3rd, Kaas, J. H., Sasaki, Y., and Cheng, H. (1995). Receptive-field properties of deafferentated visual cortical neurons after topographic map reorganization in adult cats. J. Neurosci. 15, 2417-2433.
21. Cooper, B. Y., Glendinning, D. S., and Vierck, C. J. Jr. (1993). Finger movement deficits in the stumptail macaque following lesions of the fasciculus cuneatus. Somatosens Mot. Res. 10, 17-29.doi: 10.3109/08990229309028820
22. Courtine, G., Song, B., Roy, R. R., Zhong, H., Herrmann, J. E., Ao, Y., et al. (2008). Recovery of supraspinal control of stepping via indirect propriospinal relay connections after spinal cord injury. Nat. Med. 14, 69-74.doi: 10.1038/ nm1682
23. Cregg, J. M., Depaul, M. A., Filous, A. R., Lang, B. T., Tran, A., and Silver, J. (2014). Functional regeneration beyond the glial scar. Exp. Neurol. 253C, 197-207.doi: 10.1016/j.expneurol.2013.12.024
24. Crockett, D. P., Maslany, S., Harris, S. L., and Egger, M. D. (1993). Enhanced cytochrome-oxidase staining of the cuneate nucleus in the rat reveals a modifiable somatotopic map. Brain Res. 612, 41-55.doi: 10.1016/0006-8993(93)91642-6
25. Curt, A., Alkadhi, H., Crelier, G. R., Boendermaker, S. H., Hepp-Reymond, M. C., and Kollias, S. S. (2002). Changes of non-affected upper limb cortical representation in paraplegic patients as assessed by fMRI. Brain 125, 2567-2578.doi: 10.1093/brain/awf250
26. Cusick, C. G., and Gould, H. J. 3rd. (1990). Connections between area 3b of the somatosensory cortex and subdivisions of the ventroposterior nuclear complex and the anterior pulvinar nucleus in squirrel monkeys. J. Comp. Neurol. 292, 83-102.doi: 10.1002/cne.902920106
27. D'Amato, C. J., and Hicks, S. P. (1978). Normal development and post-traumatic plasticity of corticospinal neurons in rats. Exp. Neurol. 60, 557-569.doi: 10.1016/0014-4886(78)90010-9
28. Darian-Smith, C. (2004). Primary afferent terminal sprouting after a cervical dorsal rootlet section in the macaque monkey. J. Comp. Neurol. 470, 134-150.doi: 10.1002/cne.11030
29. Darian-Smith, C. (2009). Synaptic plasticity, neurogenesis, and functional recovery after spinal cord injury. Neuroscientist 15, 149-165.doi: 10.1177/ 1073858408331372
30. Darian-Smith, C., and Brown, S. (2000). Functional changes at periphery and cortex following dorsal root lesions in adult monkeys. Nat. Neurosci. 3, 476-481.doi: 10.1038/74852
31. Darian-Smith, C., and Ciferri, M. (2006). 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.doi: 10.1002/cne.21088
32. Darian-Smith, C., and Ciferri, M. M. (2005). Loss and recovery of voluntary hand movements in the macaque following a cervical dorsal rhizotomy. J. Comp. Neurol. 491, 27-45.doi: 10.1002/cne.20686
33. Darian-Smith, C., and Gilbert, C. D. (1994). Axonal sprouting accompanies functional reorganization in adult cat striate cortex. Nature 368, 737-740.doi: 10.1038/368737a0
34. Darian-Smith, C., and Gilbert, C. D. (1995). Topographic reorganization in the striate cortex of the adult cat and monkey is cortically mediated. J. Neurosci. 15, 1631-1647.
35. Darian-Smith, C., Hopkins, S., and Ralston, H. J. 3rd. (2010). Changes in synap-tic populations in the spinal dorsal horn following a dorsal rhizotomy in the monkey. J. Comp. Neurol. 518, 103-117.doi: 10.1002/cne.22216
36. Davis, K. D., Kiss, Z. H., Luo, L., Tasker, R. R., Lozano, A. M., and Dostrovsky, J. O. (1998). Phantom sensations generated by thalamic microstimulation. Nature 391, 385-387.doi: 10.1038/34905
37. Disbrow, E., Litinas, E., Recanzone, G. H., Padberg, J., and Krubitzer, L. (2003). Cortical connections of the second somatosensory area and the parietal ventral area in macaque monkeys. J. Comp. Neurol. 462, 382-399.doi: 10.1002/cne.10731
38. Doetsch, G. S., Harrison, T. A., Macdonald, A. C., and Litaker, M. S. (1996). Short-term plasticity in primary somatosensory cortex of the rat: rapid changes in magnitudes and latencies of neuronal responses following digit denervation. Exp. Brain Res. 112, 505-512.doi: 10.1007/BF00227956
39. Dutta, A., Kambi, N., Raghunathan, P., Khushu, S., and Jain, N. (2013). Large-scale reorganization of the somatosensory cortex of adult macaque monkeys revealed by fMRI. Brain Struct. Funct.doi: 10.1007/s00429-013-0569-8. [Epub ahead of print].
40. Dykes, R. W., and Craig, A. D. (1998). Control of size and excitability of mechanosensory receptive fields in dorsal column nuclei by homolateral dorsal horn neurons. J. Neurophysiol. 80, 120-129.
41. Elbert, T., Sterr, A., Flor, H., Rockstroh, B., Knecht, S., Pantev, C., et al. (1997). Input-increase and input-decrease types of cortical reorganization after upper extremity amputation in humans. Exp. Brain Res. 117, 161-164.doi: 10.1007/s002210050210
42. Faggin, B. M., Nguyen, K. T., and Nicolelis, M. A. (1997). Immediate and simultaneous sensory reorganization at cortical and subcortical levels of the somatosensory system. Proc. Natl. Acad. Sci. U.S.A. 94, 9428-9433.doi: 10.1073/pnas.94.17.9428
43. Fang, P. C., Stepniewska, I., and Kaas, J. H. (2005). Ipsilateral cortical connections of motor, premotor, frontal eye, and posterior parietal fields in a prosimian primate, Otolemur garnetti. J. Comp. Neurol. 490, 305-333.doi: 10.1002/cne.20665
44. Fawcett, J. W., Schwab, M. E., Montani, L., Brazda, N., and Muller, H. W. (2012). Defeating inhibition of regeneration by scar and myelin components. Handb. Clin. Neurol. 109, 503-522.doi: 10.1016/B978-0-444-52137-8.00031-0
45. Flor, H., Elbert, T., Knecht, S., Wienbruch, C., Pantev, C., Birbaumer, N., et al. (1995). Phantom-limb pain as a perceptual correlate of cortical reorganization following arm amputation. Nature 375, 482-484.doi: 10.1038/ 375482a0
46. Flor, H., Elbert, T., Muhlnickel, W., Pantev, C., Wienbruch, C., and Taub, E. (1998). Cortical reorganization and phantom phenomena in congenital and traumatic upper-extremity amputees. Exp. Brain Res. 119, 205-212.doi: 10.1007/s002210050334
47. Florence, S. L., Hackett, T. A., and Strata, F. (2000). Thalamic and cortical contributions to neural plasticity after limb amputation. J. Neurophysiol. 83, 3154-3159.
48. Florence, S. L., and Kaas, J. H. (1995). Large-scale reorganization at multiple levels of the somatosensory pathway follows therapeutic amputation of the hand in monkeys. J. Neurosci. 15, 8083-8095.
49. Florence, S. L., Taub, H. B., and Kaas, J. H. (1998). Large-scale sprouting of cortical connections after peripheral injury in adult macaque monkeys. Science 282, 1117-1121.doi: 10.1126/science.282.5391.1117
50. Garcia-Alias, G., and Fawcett, J. W. (2012). Training and anti-CSPG combination therapy for spinal cord injury. Exp. Neurol. 235, 26-32.doi: 10.1016/j.expneurol.2011.09.009
51. Garraghty, P. E., Arnold, L. L., Wellman, C. L., and Mowery, T. M. (2006). Receptor autoradiographic correlates of deafferentation-induced reorganization in adult primate somatosensory cortex. J. Comp. Neurol. 497, 636-645.doi: 10.1002/cne.21018
52. Garraghty, P. E., Florence, S. L., and Kaas, J. H. (1990a). Ablations of areas 3a and 3b of monkey somatosensory cortex abolish cutaneous responsivity in area 1. Brain Res. 528, 165-169.doi: 10.1016/0006-8993(90)90213-U
53. Garraghty, P. E., Lachica, E. A., and Kaas, J. H. (1991). Injury-induced reorganization of somatosensory cortex is accompanied by reductions in GABA staining. Somatosens Mot. Res. 8, 347-354.doi: 10.3109/08990229109144757
54. Garraghty, P. E., Pons, T. P., and Kaas, J. H. (1990b). Ablations of areas 3b (SI proper) and 3a of somatosensory cortex in marmosets deactivate the second and parietal ventral somatosensory areas. Somatosens Mot. Res. 7, 125-135.doi: 10.3109/08990229009144703
55. Ghosh, A., Sydekum, E., Haiss, F., Peduzzi, S., Zorner, B., Schneider, R., et al. (2009). Functional and anatomical reorganization of the sensory-motor cortex after incomplete spinal cord injury in adult rats. J. Neurosci. 29, 12210-12219.doi: 10.1523/JNEUROSCI.1828-09.2009
56. Giger, R. J., Hollis, E. R. 2nd., and Tuszynski, M. H. (2010). Guidance molecules in axon regeneration. Cold Spring Harb. Perspect. Biol. 2, a001867.doi: 10.1101/cshperspect.a001867
57. Glendinning, D. S., Cooper, B. Y., Vierck, C. J. Jr., and Leonard, C. M. (1992). Altered precision grasping in stumptail macaques after fasciculus cuneatus lesions. Somatosens Mot. Res. 9, 61-73.doi: 10.3109/08990229209144763
58. Graziano, A., Foffani, G., Knudsen, E. B., Shumsky, J., and Moxon, K. A. (2013). Passive exercise of the hind limbs after complete thoracic transection of the spinal cord promotes cortical reorganization. PLoS ONE 8:e54350.doi: 10.1371/journal.pone.0054350
59. Graziano, A., and Jones, E. G. (2009). Early withdrawal of axons from higher centers in response to peripheral somatosensory denervation. J. Neurosci. 29, 3738-3748.doi: 10.1523/JNEUROSCI.5388-08.2009
60. He, Z., and Koprivica, V. (2004). The Nogo signaling pathway for regeneration block. Annu. Rev. Neurosci. 27, 341-368.doi: 10.1146/annurev.neuro.27.070203. 144340
61. Hickmott, P. W., and Steen, P. A. (2005). Large-scale changes in dendritic structure during reorganization of adult somatosensory cortex. Nat. Neurosci. 8, 140-142.doi: 10.1038/nn1384
62. Hicks, S. P., and D'Amato, C. J. (1975). Motor-sensory cortex-corticospinal system and developing locomotion and placing in rats. Am. J. Anat. 143, 1-42.doi: 10.1002/aja.1001430102
63. Humanes-Valera, D., Aguilar, J., and Foffani, G. (2013). Reorganization of the intact somatosensory cortex immediately after spinal cord injury. PLoS ONE 8:e69655.doi: 10.1371/journal.pone.0069655
64. Jain, N., Catania, K. C., and Kaas, J. H. (1997). Deactivation and reactivation of somatosensory cortex after dorsal spinal cord injury. Nature 386, 495-498.doi: 10.1038/386495a0
65. Jain, N., Catania, K. C., and Kaas, J. H. (1998). A histologically visible representation of the fingers and palm in primate area 3b and its immutability following long-term deafferentations. Cereb. Cortex 8, 227-236.doi: 10.1093/cer-cor/8.3.227
66. Jain, N., Florence, S. L., Qi, H. X., and Kaas, J. H. (2000). Growth of new brainstem connections in adult monkeys with massive sensory loss. Proc. Natl. Acad. Sci. U.S.A. 97, 5546-5550.doi: 10.1073/pnas.090572597
67. Jain, N., Qi, H. X., Catania, K. C., and Kaas, J. H. (2001). Anatomic correlates of the face and oral cavity representations in the somatosensory cortical area 3b of monkeys. J. Comp. Neurol. 429, 455-468.doi: 10.1002/1096-9861(20010115)429:3%3C455::AID-CNE7%3E3.0.CO;2-F
68. Jain, N., Qi, H. X., Collins, C. E., and Kaas, J. H. (2008). Large-scale reorganization in the somatosensory cortex and thalamus after sensory loss in macaque monkeys. J. Neurosci. 28, 11042-11060.doi: 10.1523/JNEUROSCI.2334-08.2008
69. Jones, E. G. (2000). Cortical and subcortical contributions to activity-dependent plasticity in primate somatosensory cortex. Annu. Rev. Neurosci. 23, 1-37.doi: 10.1146/annurev.neuro.23.1.1
70. Jones, E. G., Friedman, D. P., and Hendry, S. H. (1982). Thalamic basis of place- and modality-specific columns in monkey somatosensory cortex: a correlative anatomical and physiological study. J. Neurophysiol. 48, 545-568.
71. Jones, E. G., and Pons, T. P. (1998). Thalamic and brainstem contributions to large-scale plasticity of primate somatosensory cortex. Science 282, 1121-1125.doi: 10.1126/science.282.5391.1121
72. Kaas, J. H. (2012). "Somatosensory system," in The Human Nervous System. 3rd Edn, eds J. K. Mai and G. Paxinos. (London: ElsevierAcademic Press), 1064-1099.
73. Kaas, J. H., Nelson, R. J., Sur, M., Dykes, R. W., and Merzenich, M. M. (1984). The somatotopic organization of the ventroposterior thalamus of the squirrel monkey, Saimiri sciureus. J. Comp. Neurol. 226, 111-140.doi: 10.1002/cne.902260109
74. Kaas, J. H., Nelson, R. J., Sur, M., Lin, C. S., and Merzenich, M. M. (1979). Multiple representations of the body within the primary somatosensory cortex of primates. Science 204, 521-523.doi: 10.1126/science.107591
75. Kaas, J. H., Qi, H. X., Burish, M. J., Gharbawie, O. A., Onifer, S. M., and Massey, J. M. (2008). Cortical and subcortical plasticity in the brains of humans, primates, and rats after damage to sensory afferents in the dorsal columns of the spinal cord. Exp. Neurol. 209, 407-416.doi: 10.1016/j.expneurol.2007.06.014
76. Kaas, J. H., Qi, H. X., and Iyengar, S. (2006). Cortical network for representing the teeth and tongue in primates. Anat. Rec. A Discov. Mol. Cell Evol. Biol. 288, 182-190.doi: 10.1002/ar.a.20267
77. Kambi, N., Tandon, S., Mohammed, H., Lazar, L., and Jain, N. (2011). Reorganization of the primary motor cortex of adult macaque monkeys after sensory loss resulting from partial spinal cord injuries. J. Neurosci. 31, 3696-3707.doi: 10.1523/JNEUROSCI.5187-10.2011
78. Kao, T., Shumsky, J. S., Murray, M., and Moxon, K. A. (2009). Exercise induces cortical plasticity after neonatal spinal cord injury in the rat. J. Neurosci. 29, 7549-7557.doi: 10.1523/JNEUROSCI.2474-08.2009
79. Kelahan, A. M., and Doetsch, G. S. (1984). Time-dependent changes in the functional organization of somatosensory cerebral cortex following digit amputation in adult raccoons. Somatosens Res. 2, 49-81.
80. Krajacic, A., Weishaupt, N., Girgis, J., Tetzlaff, W., and Fouad, K. (2010). Training-induced plasticity in rats with cervical spinal cord injury: effects and side effects. Behav. Brain Res. 214, 323-331.doi: 10.1016/j.bbr.2010.05.053
81. Krubitzer, L. A., and Kaas, J. H. (1990). The organization and connections of somatosensory cortex in marmosets. J. Neurosci. 10, 952-974.
82. Krupa, D. J., Ghazanfar, A. A., and Nicolelis, M. A. (1999). Immediate thalamic sensory plasticity depends on corticothalamic feedback. Proc. Natl. Acad. Sci. U.S.A. 96, 8200-8205.doi: 10.1073/pnas.96.14.8200
83. Leonard, C. M., Glendinning, D. S., Wilfong, T., Cooper, B. Y., and Vierck, C. J. Jr. (1992). Alterations of natural hand movements after interruption of fasciculus cuneatus in the macaque. Somatosens Mot. Res. 9, 75-89.doi: 10.3109/08990229209144764
84. Li, C. X., Yang, Q., Vemulapalli, S., and Waters, R. S. (2013). Forelimb amputation-induced reorganization in the cuneate nucleus (CN) is not reflected in large-scale reorganization in rat forepaw barrel subfield cortex (FBS). Brain Res. 1526, 26-43.doi: 10.1016/j.brainres.2013.05.049
85. Liao, C. C., Gharbawie, O. A., Qi, H., and Kaas, J. H. (2013). Cortical connections to single digit representations in area 3b of somatosensory cortex in squirrel monkeys and prosimian galagos. J. Comp. Neurol. 521, 3768-3790.doi: 10.1002/cne.23377
86. Lotze, M., Grodd, W., Birbaumer, N., Erb, M., Huse, E., and Flor, H. (1999). Does use of a myoelectric prosthesis prevent cortical reorganization and phantom limb pain? Nat. Neurosci. 2, 501-502.doi: 10.1038/9145
87. Marik, S. A., Yamahachi, H., McManus, J. N., Szabo, G., and Gilbert, C. D. (2010). Axonal dynamics of excitatory and inhibitory neurons in somatosensory cortex. PLoS Biol. 8:e1000395.doi: 10.1371/journal.pbio.1000395
88. Marik, S. A., Yamahachi, H., Meyer Zum, Alten Borgloh, S., and Gilbert, C. D. (2014). Large-Scale Axonal Reorganization of Inhibitory Neurons following Retinal Lesions. J. Neurosci. 34, 1625-1632.doi: 10.1523/JNEUROSCI.4345-13.2014.
89. Massey, J. M., Hubscher, C. H., Wagoner, M. R., Decker, J. A., Amps, J., Silver, J., et al. (2006). Chondroitinase ABC digestion of the perineuronal net promotes functional collateral sprouting in the cuneate nucleus after cervical spinal cord injury. J. Neurosci. 26, 4406-4414.doi: 10.1523/JNEUROSCI.5467-05.2006
90. McKenna, J. E., and Whishaw, I. Q. (1999). Complete compensation in skilled reaching success with associated impairments in limb synergies, after dorsal column lesion in the rat. J. Neurosci. 19, 1885-1894.
91. Merzenich, M. M., Kaas, J. H., Sur, M., and Lin, C. S. (1978). Double representation of the body surface within cytoarchitectonic areas 3b and 1 in "SI" in the owl monkey (Aotus trivirgatus). J. Comp. Neurol. 181, 41-73.doi: 10.1002/cne.901810104
92. Merzenich, M. M., Kaas, J. H., Wall, J., Nelson, R. J., Sur, M., and Felleman, D. (1983a). Topographic reorganization of somatosensory cortical areas 3b and 1 in adult monkeys following restricted deafferentation. Neuroscience 8, 33-55.doi: 10.1016/0306-4522(83)90024-6
93. Merzenich, M. M., Kaas, J. H., Wall, J. T., Sur, M., Nelson, R. J., and Felleman, D. J. (1983b). Progression of change following median nerve section in the cortical representation of the hand in areas 3b and 1 in adult owl and squirrel monkeys. Neuroscience 10, 639-665.doi: 10.1016/0306-4522(83) 90208-7
94. Moore, C. I., Stern, C. E., Dunbar, C., Kostyk, S. K., Gehi, A., and Corkin, S. (2000). Referred phantom sensations and cortical reorganization after spinal cord injury in humans. Proc. Natl. Acad. Sci. U.S.A. 97, 14703-14708.doi: 10.1073/pnas.250348997
95. Mountcastle, V. B., and Darian-Smith, I. (1968). "Neural mechanisms in somesthe-sia," in Medical Physiology, ed V. B. Mountcastle (St. Louis, MO: C. V. Mosby), 1372-1423.
96. Nathan, P. W., Smith, M. C., and Cook, A. W. (1986). Sensory effects in man of lesions of the posterior columns and of some other afferent pathways. Brain 109(Pt. 5), 1003-1041.
97. Nelson, R. J., and Kaas, J. H. (1981). Connections of the ventroposterior nucleus of the thalamus with the body surface representations in cortical areas 3b and 1 of the cynomolgus macaque, (Macaca fascicularis). J. Comp. Neurol. 199, 29-64.doi: 10.1002/cne.901990104
98. Nelson, R. J., Sur, M., Felleman, D. J., and Kaas, J. H. (1980). Representations of the body surface in postcentral parietal cortex of Macaca fascicularis. J. Comp. Neurol. 192, 611-643.doi: 10.1002/cne.901920402
99. Nout, Y. S., Ferguson, A. R., Strand, S. C., Moseanko, R., Hawbecker, S., Zdunowski, S., et al. (2012b). Methods for functional assessment after C7 spinal cord hemi-section in the rhesus monkey. Neurorehabil. Neural Repair 26, 556-569.doi: 10.1177/1545968311421934
100. Nout, Y. S., Rosenzweig, E. S., Brock, J. H., Strand, S. C., Moseanko, R., Hawbecker, S., et al. (2012a). Animal models of neurologic disorders: a nonhuman primate model of spinal cord injury. Neurotherapeutics 9, 380-392.doi: 10.1007/s13311-012-0114-0
101. Onifer, S. M., Smith, G. M., and Fouad, K. (2011). Plasticity after spinal cord injury: relevance to recovery and approaches to facilitate it. Neurotherapeutics 8, 283-293.doi: 10.1007/s13311-011-0034-4
102. Paxino, G., and Watson, C. (2007). The Rat Brain in Stereotaxic Coordinates. Amsterdam: Elsevier.
103. Pei, Y. C., Denchev, P. V., Hsiao, S. S., Craig, J. C., and Bensmaia, S. J. (2009). Convergence of submodality-specific input onto neurons in primary somatosensory cortex. J. Neurophysiol. 102, 1843-1853.doi: 10.1152/jn. 00235.2009
104. Perl, E. R., Whitlock, D. G., and Gentry, J. R. (1962). Cutaneous projection to second-order neurons of the dorsal column system. J. Neurophysiol. 25, 337-358.
105. Pons, T. P., Garraghty, P. E., Friedman, D. P., and Mishkin, M. (1987). Physiological evidence for serial processing in somatosensory cortex. Science 237, 417-420.doi: 10.1126/science.3603028
106. Pons, T. P., Garraghty, P. E., and Mishkin, M. (1992). Serial and parallel processing of tactual information in somatosensory cortex of rhesus monkeys. J. Neurophysiol. 68, 518-527.
107. Pons, T. P., Garraghty, P. E., Ommaya, A. K., Kaas, J. H., Taub, E., and Mishkin, M. (1991). Massive cortical reorganization after sensory deafferentation in adult macaques. Science 252, 1857-1860.doi: 10.1126/science.1843843
108. Qi, H. X., Chen, L. M., and Kaas, J. H. (2011a). Reorganization of somatosen-sory cortical areas 3b and 1 after unilateral section of dorsal columns of the spinal cord in squirrel monkeys. J. Neurosci. 31, 13662-13675.doi: 10.1523/JNEUROSCI.2366-11.2011
109. Qi, H. X., Gharbawie, O. A., Wong, P., and Kaas, J. H. (2011b). Cell-poor septa separate representations of digits in the ventroposterior nucleus of the thala-mus in monkeys and prosimian galagos. J. Comp. Neurol. 519, 738-758.doi: 10.1002/cne.22545
110. Qi, H. X., Gharbawie, O. A., Wynne, K. W., and Kaas, J. H. (2013). Impairment and recovery of hand use after unilateral section of the dorsal columns of the spinal cord in squirrel monkeys. Behav. Brain Res. 252, 363-376.doi: 10.1016/j.bbr.2013.05.058
111. Qi, H. X., Jain, N., Collins, C. E., Lyon, D. C., and Kaas, J. H. (2010). Functional organization of motor cortex of adult macaque monkeys is altered by sensory loss in infancy. Proc. Natl. Acad. Sci. U.S.A. 107, 3192-3197.doi: 10.1073/pnas. 0914962107
112. Qi, H. X., and Kaas, J. H. (2004). Myelin stains reveal an anatomical framework for the representation of the digits in somatosensory area 3b of macaque monkeys. J. Comp. Neurol. 477, 172-187.doi: 10.1002/cne.20247
113. Qi, H. X., Reed, J. L., Bui, T., Chen, L. M., and Kaas, J. H. (2012). Longitudinal fMRI and behavioral recovery after sensory loss from the hand of adult monkeys. Fed. Euro. Neurosci. Soc. Forum Abstr. A-471-0142-02394.
114. Qi, H. X., Reed, J. L., Gharbawie, O. A., Burish, M. J., and Kaas, J. H. (2014). Cortical neuron response properties are related to lesion extent and behavioral recovery after sensory loss from spinal cord injury in monkeys. J. Neurosci. 34, 4345-4363.doi: 10.1523/JNEUROSCI.4954-13.2014
115. Ramachandran, V. S. (1993). Behavioral and magnetoencephalographic correlates of plasticity in the adult human brain. Proc. Natl. Acad. Sci. U.S.A. 90, 10413-10420.doi: 10.1073/pnas.90.22.10413
116. Ramachandran, V. S., and Rogers-Ramachandran, D. (2000). Phantom limbs and neural plasticity. Arch. Neurol. 57, 317-320.doi: 10.1001/archneur.5 7.3.317
117. Rasmusson, D. D. (1996). Changes in the response properties of neurons in the ventroposterior lateral thalamic nucleus of the raccoon after peripheral deafferentation. J. Neurophysiol. 75, 2441-2450.
118. Rasmusson, D. D., and Northgrave, S. A. (1997). Reorganization of the raccoon cuneate nucleus after peripheral denervation. J. Neurophysiol. 78, 2924-2936.
119. Reed, J. L., Qi, H. X., and Kaas, J. H. (2012). Ipsilateral responses and interhemi-spheric interactions in area 3b after dorsal column spinal cord injury in New World m o n k e y s Soc. Neurosci. Abstr. 42.
120. Reed, J. L., Qi, H. X., Zhou, Z., Bernard, M. R., Burish, M. J., Bonds, A. B., et al. (2010). Response properties of neurons in primary somatosensory cortex of owl monkeys reflect widespread spatiotemporal integration. J. Neurophysiol. 103, 2139-2157.doi: 10.1152/jn.00709.2009
121. Rose, J. E., and Mountcastle, V. B. (1959). "Touch and kinesthesis," in Handbook of Physilogy, ed H. W. Magoun (Washington, DC: American Physiology Society), 387-429.
122. Rustioni, A., Hayes, N. L., and O'Neill, S. (1979). Dorsal column nuclei and ascending spinal afferents in macaques. Brain 102, 95-125.doi: 10.1093/brain/102.1.95
123. Schmidlin, E., Kaeser, M., Gindrat, A. D., Savidan, J., Chatagny, P., Badoud, S., et al. (2011). Behavioral assessment of manual dexterity in non-human primates. J. Vis. Exp. 57, 3258-3270.doi: 10.3791/3258
124. Schnell, L., Schneider, R., Kolbeck, R., Barde, Y. A., and Schwab, M. E. (1994). Neurotrophin-3 enhances sprouting of corticospinal tract during development and after adult spinal cord lesion. Nature 367, 170-173.doi: 10.1038/ 367170a0
125. Sengelaub, D. R., Muja, N., Mills, A. C., Myers, W. A., Churchill, J. D., and Garraghty, P. E. (1997). Denervation-induced sprouting of intact peripheral afferents into the cuneate nucleus of adult rats. Brain Res. 769, 256-262.doi: 10.1016/S0006-8993(97)00708-7
126. Silva, A. C., Rasey, S. K., Wu, X., and Wall, J. T. (1996). Initial cortical reactions to injury of the median and radial nerves to the hands of adult primates. J. Comp. Neurol. 366, 700-716.doi: 10.1002/(SICI)1096-9861(19960318)366:4<700::AID-CNE9>3.0.CO;2-8
127. Silva, N. A., Sousa, N., Reis, R. L., and Salgado, A. J. (2014). From basics to clinical: a comprehensive review on spinal cord injury. Prog. Neurobiol. 114, 25-57.doi: 10.1016/j.pneurobio.2013.11.002
128. Stepniewska, I., Preuss, T. M., and Kaas, J. H. (1993). Architectonics, soma-totopic organization, and ipsilateral cortical connections of the primary motor area (M1) of owl monkeys. J. Comp. Neurol. 330, 238-271.doi: 10.1002/cne.903300207
129. Sur, M., Nelson, R. J., and Kaas, J. H. (1982). Representations of the body surface in cortical areas 3b and 1 of squirrel monkeys: comparisons with other primates. J. Comp. Neurol. 211, 177-192.doi: 10.1002/cne.902110207
130. Sur, M., Wall, J. T., and Kaas, J. H. (1984). Modular distribution of neurons with slowly adapting and rapidly adapting responses in area 3b of somatosensory cortex in monkeys. J. Neurophysiol. 51, 724-744.
131. Tandon, S., Kambi, N., Lazar, L., Mohammed, H., and Jain, N. (2009). Large-scale expansion of the face representation in somatosensory areas of the lateral sul-cus after spinal cord injuries in monkeys. J. Neurosci. 29, 12009-12019.doi: 10.1523/JNEUROSCI.2118-09.2009
132. Tetzlaff, W., Fouad, K., and Kwon, B. (2009). Be careful what you train for. Nat. Neurosci. 12, 1077-1079.doi: 10.1038/nn0909-1077
133. Tommerdahl, M., Whitsel, B. L., Vierck, C. J. Jr., Favorov, O., Juliano, S., Cooper, B., et al. (1996). Effects of spinal dorsal column transection on the response of monkey anterior parietal cortex to repetitive skin stimulation. Cereb. Cortex 6, 131-155.doi: 10.1093/cercor/6.2.131
134. Turrigiano, G. G. (1999). Homeostatic plasticity in neuronal networks: the more things change, the more they stay the same. Trends Neurosci. 22, 221-227.doi: 10.1016/S0166-2236(98)01341-1
135. Vahlsing, H. L., and Feringa, E. R. (1980). A ventral uncrossed corticospinal tract in the rat. Exp. Neurol. 70, 282-287.doi: 10.1016/0014-4886(80)90027-8
136. Vierck, C. J. Jr. (1973). Alterations of spatio-tactile discrimination after lesions of primate spinal cord. Brain Res. 58, 69-79.doi: 10.1016/0006-8993(73)90824-X
137. Vierck, C. J. Jr. (1974). Tactile movement detection and discrimination following dorsal column lesions in monkeys. Exp. Brain Res. 20, 331-346.doi: 10.1007/BF00237379
138. Vierck, C. J. Jr. (1998). Impaired detection of repetitive stimulation following interruption of the dorsal spinal column in primates. Somatosens Mot. Res. 15, 157-163.doi: 10.1080/08990229870880
139. Vierck, C. J. Jr., and Cooper, B. Y. (1998). Cutaneous texture discrimination following transection of the dorsal spinal column in monkeys. Somatosens Mot. Res. 15, 309-315.doi: 10.1080/08990229870718
140. Wall, J. T., Xu, J., and Wang, X. (2002). Human brain plasticity: an emerging view of the multiple substrates and mechanisms that cause cortical changes and related sensory dysfunctions after injuries of sensory inputs from the body. Brain Res. Brain Res. Rev. 39, 181-215.doi: 10.1016/S0165-0173(02)00192-3
141. Wall, P. D. (1970). The sensory and motor role of impulses travelling in the dorsal columns towards cerebral cortex. Brain 93, 505-524.doi: 10.1093/brain/93.3.505
142. Wall, P. D. (1977). The presence of ineffective synapses and the circumstances which unmask them. Philos. Trans. R. Soc. Lond. B Biol. Sci. 278, 361-372.doi: 10.1098/rstb.1977.0048
143. Wang, Z., Qi, H. X., Kaas, J. H., Roe, A. W., and Chen, L. M. (2013). Functional signature of recovering cortex: dissociation of local field potentials and spiking activity in somatosensory cortices of spinal cord injured monkeys. Exp. Neurol. 249, 132-143.doi: 10.1016/j.expneurol.2013.08.013
144. Welker, W. I. (1973). Principles of organization of the ventrobasal complex in mammals. Brain Behav. Evol. 7, 253-336.doi: 10.1159/000124417
145. Wellman, C. L., Arnold, L. L., Garman, E. E., and Garraghty, P. E. (2002). Acute reductions in GABAA receptor binding in layer IV of adult primate somatosensory cortex after peripheral nerve injury. Brain Res. 954, 68-72.doi: 10.1016/S0006-8993(02)03343-7
146. Weng, H. R., Lenz, F. A., Vierck, C., and Dougherty, P. M. (2003). Physiological changes in primate somatosensory thalamus induced by deafferentation are dependent on the spinal funiculi that are sectioned and time following injury. Neuroscience 116, 1149-1160.doi: 10.1016/S0306-4522(02)00796-0
147. rd Edn, eds W. D. Willis and R. E. Coggeshall (New York, NY: Kluwer Academy/Plenum Publisher), 597-664.doi: 10.1007/978-1-4615-0035-3_9
148. Wise, S. P., Boussaoud, D., Johnson, P. B., and Caminiti, R. (1997). Premotor and parietal cortex: corticocortical connectivity and combinatorial computations. Annu. Rev. Neurosci. 20, 25-42.doi: 10.1146/annurev.neuro.20.1.25
149. Witham, C. L., and Baker, S. N. (2011). Modulation and transmission of peripheral inputs in monkey cuneate and external cuneate nuclei. J. Neurophysiol. 106, 2764-2775.doi: 10.1152/jn.00449.2011
150. Wu, C. W., and Kaas, J. H. (1999). Reorganization in primary motor cortex of primates with long-standing therapeutic amputations. J. Neurosci. 19, 7679-7697.
151. Xerri, C. (2012). Plasticity of cortical maps: multiple triggers for adaptive reorganization following brain damage and spinal cord injury. Neuroscientist 18, 133-148.doi: 10.1177/1073858410397894
152. Xu, J., and Wall, J. T. (1997). Rapid changes in brainstem maps of adult primates after peripheral injury. Brain Res. 774, 211-215.doi: 10.1016/S0006-8993(97)81706-4
153. Xu, J., and Wall, J. T. (1999). Evidence for brainstem and supra-brainstem contributions to rapid cortical plasticity in adult monkeys. J. Neurosci. 19, 7578-7590.
154. Yamahachi, H., Marik, S. A., McManus, J. N., Denk, W., and Gilbert, C. D. (2009). Rapid axonal sprouting and pruning accompany functional reorganization in primary visual cortex. Neuron 64, 719-729.doi: 10.1016/j.neuron.2009.11.026
155. Zhao, R. R., Andrews, M. R., Wang, D., Warren, P., Gullo, M., Schnell, L., et al. (2013). Combination treatment with anti-Nogo-A and chondroitinase ABC is more effective than single treatments at enhancing functional recovery after spinal cord injury. Eur. J. Neurosci. 38, 2946-2961.doi: 10.1111/ejn.12276
156. Zorner, B., Filli, L., Starkey, M. L., Gonzenbach, R., Kasper, H., Rothlisberger, M., et al. (2010). Profiling locomotor recovery: comprehensive quantification of impairments after CNS damage in rodents. Nat. Methods 7, 701-708.doi: 10.1038/nmeth.1484