Chronic electrical stimulation of transected peripheral nerves preserves anatomy and function in the primary somatosensory cortex

European Journal of Neuroscience

Volumn 36, Issue 12, 2012, Pages 3679-3690

  Herrera Rincon, Celia ^a   Torets, Carlos ^a   Sanchez Jimenez, Abel ^a   Avendaño, Carlos ^b   Panetsos, Fivos ^a  

^a UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^b UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

Author keywords

Calbindin D28k; Cytochrome oxidase CyO; Parvalbumin PV; Plasticity; Rat; Trigeminal nerve implant

Indexed keywords

CALBINDIN; CYTOCHROME C OXIDASE; PARVALBUMIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BRAIN REGION; CENTRAL NERVOUS SYSTEM FUNCTION; CONTROLLED STUDY; ELECTRIC PERIPHERAL NERVE STIMULATOR; ELECTRODE; ELECTROPHYSIOLOGY; ELECTROSTIMULATION; EVOKED CORTICAL RESPONSE; INFRAORBITAL NERVE; INTERNEURON; LATENT PERIOD; MINIMUM INHIBITORY CONCENTRATION; NEUROPROSTHESIS; NEUROPROTECTION; NONHUMAN; PRIMARY SOMATOSENSORY CORTEX; PRIORITY JOURNAL; RAT; SENSORY STIMULATION; SOMATOSENSORY CORTEX; TRIGEMINAL NERVE;

ANIMALS; CALCIUM-BINDING PROTEIN, VITAMIN D-DEPENDENT; DENERVATION; ELECTRIC STIMULATION; ELECTRON TRANSPORT COMPLEX IV; EVOKED POTENTIALS; FEMALE; INTERNEURONS; PARVALBUMINS; RATS; RATS, WISTAR; SOMATOSENSORY CORTEX; TRIGEMINAL NERVE;

EID: 84871335282     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/ejn.12000     Document Type: Article

References (97)

1. Aldskogius, H. & Arvidsson, J. (1978) Nerve cell degeneration and death in the trigeminal ganglion of the adult rat following peripheral nerve transection. J. Neurocytol., 7, 229-250.
2. Armstrong-James, M., Fox, K. & Das-Gupta, A. (1992) Flow of excitation within rat barrel cortex on striking a single vibrissa. J. Neurophysiol., 68, 1345-1358.
3. Avendano, C. (2006) Stereology of neural connections. An overview. In Záborszky, L., Wouterlood, F.G. & Lanciego, J.L. (Eds), Neuroanatomical Tract Tracing: Molecules, Neurons, & Systems. Springer Science & Business Media, New York, NY, pp. 477-529.
4. Bao, S., Chang, E.F., Woods, J. & Merzenich, M.M. (2004) Temporal plasticity in the primary auditory cortex induced by operant perceptual learning. Nat. Neurosci., 7, 974-981.
5. Blumcke, I., Weruaga, E., Kasas, S., Hendrickson, A.E. & Celio, M.R. (1994) Discrete reduction patterns of parvalbumin and calbindin D-28k immunoreactivity in the dorsal lateral geniculate nucleus and the striate cortex of adult macaque monkeys after monocular enucleation. Vis. Neurosci., 11, 1-11.
6. Bruchey, A.K. & Gonzalez-Lima, F. (2008) Enhanced metabolic capacity of the frontal cerebral cortex after Pavlovian conditioning. Neuroscience, 152, 299-307.
7. Buonomano, D.V. & Merzenich, M.M. (1998) Cortical plasticity: from synapses to maps. Annu. Rev. Neurosci., 21, 149-186.
8. Calford, M.B. (2002) Dynamic representational plasticity in sensory cortex. Neuroscience, 111, 709-738.
9. Carder, R.K., Leclerc, S.S. & Hendry, S.H. (1996) Regulation of calcium-binding protein immunoreactivity in GABA neurons of macaque primary visual cortex. Cereb. Cortex, 6, 271-287.
10. Cellerino, A., Siciliano, R., Domenici, L. & Maffei, L. (1992) Parvalbumin immunoreactivity: a reliable marker for the effects of monocular deprivation in the rat visual cortex. Neuroscience, 51, 749-753.
11. Chakrabarti, S. & Alloway, K.D. (2006) Differential origin of projections from SI barrel cortex to the whisker representations in SII and MI. J. Comp. Neurol., 498, 624-636.
12. Chapin, J.K. & Lin, C.S. (1984) Mapping the body representation in the SI cortex of anesthetized and awake rats. J. Comp. Neurol., 229, 199-213.
13. Chouard, C.H., Meyer, B., Josset, P. & Buche, J.F. (1983) The effect of the acoustic nerve chronic electric stimulation upon the guinea pig cochlear nucleus development. Acta Otolaryngol., 95, 639-645.
14. Churchill, J.D., Tharp, J.A., Wellman, C.L., Sengelaub, D.R. & Garraghty, P.E. (2004) Morphological correlates of injury-induced reorganization in primate somatosensory cortex. BMC Neurosci., 5, 43.
15. Cruz-Orive, L.M. (1999) Precision of Cavalieri sections and slices with local errors. J. Microsc., 193, 182-198.
16. DeFelipe, J. (1997) Types of neurons, synaptic connections and chemical characteristics of cells immunoreactive for calbindin-D28K, parvalbumin and calretinin in the neocortex. J. Chem. Neuroanat., 14, 1-19.
17. Desgent, S., Boire, D. & Ptito, M. (2010) Altered expression of parvalbumin and calbindin in interneurons within the primary visual cortex of neonatal enucleated hamsters. Neuroscience, 171, 1326-1340.
18. Di Pino, G., Guglielmelli, E. & Rossini, P.M. (2009) Neuroplasticity in amputees: main implications on bidirectional interfacing of cybernetic hand prostheses. Prog. Neurobiol., 88, 114-126.
19. Diamond, M.E., von, H.M., Knutsen, P.M., Kleinfeld, D. & Ahissar, E. (2008) 'Where' and 'what' in the whisker sensorimotor system. Nat. Rev. Neurosci., 9, 601-612.
20. Dostrovsky, J.O., Millar, J. & Wall, P.D. (1976) The immediate shift of afferent drive to dorsal column nucleus cells following deafferentation: a comparison of acute and chronic deafferentation in gracile nucleus and spinal cord. Exp. Neurol., 52, 480-495.
21. Druga, R. (2009) Neocortical inhibitory system. Folia Biol. (Praha), 55, 201-217.
22. Dykes, R.W., Avendaño, C. & Leclerc, S.S. (1995) Evolution of cortical responsiveness subsequent to multiple forelimb nerve transections: an electrophysiological study in adult cat somatosensory cortex. J. Comp. Neurol., 354, 333-344.
23. Erzurumlu, R.S. (2003) Somatosensory cortical plasticity: recruiting silenced barrels by active whiskers. Exp. Neurol., 184, 565-569.
24. Fallon, J.B., Irvine, D.R. & Shepherd, R.K. (2008) Cochlear implants and brain plasticity. Hear. Res., 238, 110-117.
25. Farahvar, A., Darwish, N.H., Sladek, S. & Meisami, E. (2007) Marked recovery of functional metabolic activity and laminar volumes in the rat hippocampus and dentate gyrus following postnatal hypothyroid growth retardation: a quantitative cytochrome oxidase study. Exp. Neurol., 204, 556-568.
26. Feldman, D.E. & Brecht, M. (2005) Map plasticity in somatosensory cortex. Science, 310, 810-815.
27. Florence, S.L. & 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.
28. Garraghty, P.E. & Kaas, J.H. (1991) Functional reorganization in adult monkey thalamus after peripheral nerve injury. NeuroReport, 2, 747-750.
29. Gierdalski, M., Jablonska, B., Smith, A., Skangiel-Kramska, J. & Kossut, M. (1999) Deafferentation induced changes in GAD67 and GluR2 mRNA expression in mouse somatosensory cortex. Brain Res. Mol. Brain Res., 71, 111-119.
30. Gonchar, Y. & Burkhalter, A. (1997) Three distinct families of GABAergic neurons in rat visual cortex. Cereb. Cortex, 7, 347-358.
31. Gonzalez Andino, S.L., Herrera-Rincon, C., Panetsos, F. & Grave, de.P.R. (2011) Combining BMI stimulation and mathematical modeling for acute stroke recovery and neural repair. Front. Neurosci., 5, 87.
32. Gulyas, A.I., Buzsaki, G., Freund, T.F. & Hirase, H. (2006) Populations of hippocampal inhibitory neurons express different levels of cytochrome c. Eur. J. Neurosci., 23, 2581-2594.
33. Gundersen, H.J., Bagger, P., Bendtsen, T.F., Evans, S.M., Korbo, L., Marcussen, N., Moller, A., Nielsen, K., Nyengaard, J.R. & Pakkenberg, B. (1988) The new stereological tools: disector, fractionator, nucleator and point sampled intercepts and their use in pathological research and diagnosis. APMIS, 96, 857-881.
34. Hevner, R.F. & Wong-Riley, M.T. (1989) Brain cytochrome oxidase: purification, antibody production, and immunohistochemical/histochemical correlations in the CNS. J. Neurosci., 9, 3884-3898.
35. Hevner, R.F., Liu, S. & Wong-Riley, M.T. (1995) A metabolic map of cytochrome oxidase in the rat brain: histochemical, densitometric and biochemical studies. Neuroscience, 65, 313-342.
36. Hickmott, P.W. & Steen, P.A. (2005) Large-scale changes in dendritic structure during reorganization of adult somatosensory cortex. Nat. Neurosci., 8, 140-142.
37. Hoeflinger, B.F., nett-Clarke, C.A., Chiaia, N.L., Killackey, H.P. & Rhoades, R.W. (1995) Patterning of local intracortical projections within the vibrissae representation of rat primary somatosensory cortex. J. Comp. Neurol., 354, 551-563.
38. Holtmaat, A. & Svoboda, K. (2009) Experience-dependent structural synaptic plasticity in the mammalian brain. Nat. Rev. Neurosci., 10, 647-658.
39. House, D.R., Elstrott, J., Koh, E., Chung, J. & Feldman, D.E. (2011) Parallel regulation of feedforward inhibition and excitation during whisker map plasticity. Neuron, 72, 819-831.
40. Jackson, M.E. & Cauller, L.J. (1998) Neural activity in SII modifies sensory evoked potentials in SI in awake rats. NeuroReport, 9, 3379-3382.
41. Jain, N., Florence, S.L. & Kaas, J.H. (1998) Reorganization of somatosensory cortex after nerve and spinal cord injury. News Physiol. Sci., 13, 143-149.
42. Jiao, Y., Zhang, C., Yanagawa, Y. & Sun, Q.Q. (2006) Major effects of sensory experiences on the neocortical inhibitory circuits. J. Neurosci., 26, 8691-8701.
43. Kaas, J.H. & Collins, C.E. (2003) Anatomic and functional reorganization of somatosensory cortex in mature primates after peripheral nerve and spinal cord injury. Adv. Neurol., 93, 87-95.
44. Kawaguchi, Y. & Kubota, Y. (1997) GABAergic cell subtypes and their synaptic connections in rat frontal cortex. Cereb. Cortex, 7, 476-486.
45. Kis, Z., Farkas, T., Rabl, K., Kis, E., Korodi, K., Simon, L., Marusin, I., Rojik, I. & Toldi, J. (1999) Comparative study of the neuronal plasticity along the neuraxis of the vibrissal sensory system of adult rat following unilateral infraorbital nerve damage and subsequent regeneration. Exp. Brain Res., 126, 259-269.
46. Kossut, M. (1992) Plasticity of the barrel cortex neurons. Prog. Neurobiol., 39, 389-422.
47. Kossut, M. (1998) Experience-dependent changes in function and anatomy of adult barrel cortex. Exp. Brain Res., 123, 110-116.
48. Kublik, E., Musial, P. & Wrobel, A. (2001) Identification of principal components in cortical evoked potentials by brief surface cooling. Clin. Neurophysiol., 112, 1720-1725.
49. Kubota, Y., Hattori, R. & Yui, Y. (1994) Three distinct subpopulations of GABAergic neurons in rat frontal agranular cortex. Brain Res., 649, 159-173.
50. LaManna, J.C., Kutina- Nelson, K.L., Hritz, M.A., Huang, Z. & Wong-Riley, M.T. (1996) Decreased rat brain cytochrome oxidase activity after prolonged hypoxia. Brain Res., 720, 1-6.
51. Land, P.W. & Akhtar, N.D. (1987) Chronic sensory deprivation affects cytochrome oxidase staining and glutamic acid decarboxylase immunoreactivity in adult rat ventrobasal thalamus. Brain Res., 425, 178-181.
52. Land, P.W., Buffer, S.A.Jr. & Yaskosky, J.D. (1995) Barreloids in adult rat thalamus: three-dimensional architecture and relationship to somatosensory cortical barrels. J. Comp. Neurol., 355, 573-588.
53. Liu, Q. & Wong-Riley, M.T. (2003) Postnatal changes in cytochrome oxidase expressions in brain stem nuclei of rats: implications for sensitive periods. J. Appl. Physiol., 95, 2285-2291.
54. Machin, R., Blasco, B., Bjugn, R. & Avendano, C. (2004) The size of the whisker barrel field in adult rats: minimal nondirectional asymmetry and limited modifiability by chronic changes of the sensory input. Brain Res., 1025, 130-138.
55. Machin, R., Perez- Cejuela, C.G., Bjugn, R. & Avendano, C. (2006) Effects of long-term sensory deprivation on asymmetric synapses in the whisker barrel field of the adult rat. Brain Res., 1107, 104-110.
56. Maier, D.L., Grieb, G.M., Stelzner, D.J. & McCasland, J.S. (2003) Large-scale plasticity in barrel cortex following repeated whisker trimming in young adult hamsters. Exp. Neurol., 184, 737-745.
57. Marasco, P.D. & Kuiken, T.A. (2010) Amputation with median nerve redirection (targeted reinnervation) reactivates forepaw barrel subfield in rats. J. Neurosci., 30, 16008-16014.
58. Matsushima, J.I., Shepherd, R.K., Seldon, H.L., Xu, S.A. & Clark, G.M. (1991) Electrical stimulation of the auditory nerve in deaf kittens: effects on cochlear nucleus morphology. Hear. Res., 56, 133-142.
59. Merzenich, M.M., Kaas, J.H., Wall, J., Nelson, R.J., Sur, M. & Felleman, D. (1983a) Topographic reorganization of somatosensory cortical areas 3b and 1 in adult monkeys following restricted deafferentation. Neuroscience, 8, 33-55.
60. Merzenich, M.M., Kaas, J.H., Wall, J.T., Sur, M., Nelson, R.J. & 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.
61. Mountcastle, V. (2005). The Sensory Hand: Neural Mechanisms of Somatic Sensation. Harvard University Press, Cambridge, MA.
62. Mowery, T.M. & Garraghty, P.E. (2009) Nerve-injury induced changes to GluR1 and GluR2/3 sub-unit expression in area 3b of adult squirrel monkeys: developmental recapitulation? Front. Syst. Neurosci., 3, 1.
63. Mowery, T.M., Elliott, K.S. & Garraghty, P.E. (2009) The cortical response to sensory deprivation in adult rats is affected by gonadectomy. Exp. Brain Res., 195, 27-33.
64. Mowery, T.M., Sarin, R.M., Elliott, K.S. & Garraghty, P.E. (2011) Nerve injury-induced changes in GABA(A) and GABA(B) sub-unit expression in area 3b and cuneate nucleus of adult squirrel monkeys: further evidence of developmental recapitulation. Brain Res., 1415, 63-75.
65. Murphy, T.H. & Corbett, D. (2009) Plasticity during stroke recovery: from synapse to behaviour. Nat. Rev. Neurosci., 10, 861-872.
66. Negredo, P., Martin, Y.B., Lagares, A., Castro, J., Villacorta, J.A. & Avendano, C. (2009) Trigeminothalamic barrelette neurons: natural structural side asymmetries and sensory input-dependent plasticity in adult rats. Neuroscience, 163, 1242-1254.
67. Nie, F. & Wong-Riley, M.T. (1996) Metabolic and neurochemical plasticity of gamma-aminobutyric acid-immunoreactive neurons in the adult macaque striate cortex following monocular impulse blockade: quantitative electron microscopic analysis. J. Comp. Neurol., 370, 350-366.
68. Nowicka, D., Soulsby, S., Skangiel-Kramska, J. & Glazewski, S. (2009) Parvalbumin-containing neurons, perineuronal nets and experience-dependent plasticity in murine barrel cortex. Eur. J. Neurosci., 30, 2053-2063.
69. Panetsos, F. & Sanchez-Jimenez, A. (2010) Single unit oscillations in rat trigeminal nuclei and their control by the sensorimotor cortex. Neuroscience, 169, 893-905.
70. Panetsos, F., Avendano, C., Negredo, P., Castro, J. & Bonacasa, V. (2008) Neural prostheses: electrophysiological and histological evaluation of central nervous system alterations due to long-term implants of sieve electrodes to peripheral nerves in cats. IEEE Trans. Neural Syst. Rehabil. Eng., 16, 223-232.
71. Pasic, T.R., Moore, D.R. & Rubel, E.W. (1994) Effect of altered neuronal activity on cell size in the medial nucleus of the trapezoid body and ventral cochlear nucleus of the gerbil. J. Comp. Neurol., 348, 111-120.
72. Pons, T.P., Garraghty, P.E., Ommaya, A.K., Kaas, J.H., Taub, E. & Mishkin, M. (1991) Massive cortical reorganization after sensory deafferentation in adult macaques. Science, 252, 1857-1860.
73. Rasmusson, D.D., Webster, H.H. & Dykes, R.W. (1992) Neuronal response properties within subregions of raccoon somatosensory cortex 1 week after digit amputation. Somatosens. Mot. Res., 9, 279-289.
74. Rosier, A.M., Arckens, L., Demeulemeester, H., Orban, G.A., Eysel, U.T., Wu, Y.J. & Vandesande, F. (1995) Effect of sensory deafferentation on immunoreactivity of GABAergic cells and on GABA receptors in the adult cat visual cortex. J. Comp. Neurol., 359, 476-489.
75. Sanchez-Jimenez, A., Panetsos, F. & Murciano, A. (2009) Early frequency-dependent information processing and cortical control in the whisker pathway of the rat: electrophysiological study of brainstem nuclei principalis and interpolaris. Neuroscience, 160, 212-226.
76. Schroeder, C.E., Seto, S. & Garraghty, P.E. (1997) Emergence of radial nerve dominance in median nerve cortex after median nerve transection in an adult squirrel monkey. J. Neurophysiol., 77, 522-526.
77. Schwartz, D.R., Schacht, J., Miller, J.M., Frey, K. & Altschuler, R.A. (1993) Chronic electrical stimulation reverses deafness-related depression of electrically evoked 2-deoxyglucose activity in the guinea pig inferior colliculus. Hear. Res., 70, 243-249.
78. Shepherd, R.K. & Hardie, N.A. (2001) Deafness-induced changes in the auditory pathway: implications for cochlear implants. Audiol. Neurootol., 6, 305-318.
79. Shimegi, S., Ichikawa, T., Akasaki, T. & Sato, H. (1999) Temporal characteristics of response integration evoked by multiple whisker stimulations in the barrel cortex of rats. J. Neurosci., 19, 10164-10175.
80. Skangiel-Kramska, J., Glazewski, S., Jablonska, B., Siucinska, E. & Kossut, M. (1994) Reduction of GABAA receptor binding of [3H]muscimol in the barrel field of mice after peripheral denervation: transient and long-lasting effects. Exp. Brain Res., 100, 39-46.
81. Skibinska, A., Glazewski, S., Fox, K. & Kossut, M. (2000) Age-dependent response of the mouse barrel cortex to sensory deprivation: a 2-deoxyglucose study. Exp. Brain Res., 132, 134-138.
82. Sun, Q.Q. (2009) Experience-dependent intrinsic plasticity in interneurons of barrel cortex layer IV. J. Neurophysiol., 102, 2955-2973.
83. Terayama, Y., Kaneko, Y., Kawamoto, K. & Sakai, N. (1977) Ultrastructural changes of the nerve elements following disruption of the organ of Corti. I. Nerve elements in the organ of Corti. Acta Otolaryngol., 83, 291-302.
84. Tropea, D., Kreiman, G., Lyckman, A., Mukherjee, S., Yu, H., Horng, S. & Sur, M. (2006) Gene expression changes and molecular pathways mediating activity-dependent plasticity in visual cortex. Nat. Neurosci., 9, 660-668.
85. Turnbull, B.G. & Rasmusson, D.D. (1991) Chronic effects of total or partial digit denervation on raccoon somatosensory cortex. Somatosens. Mot. Res., 8, 201-213.
86. Valla, J., Berndt, J.D. & Gonzalez-Lima, F. (2001) Energy hypometabolism in posterior cingulate cortex of Alzheimer's patients: superficial laminar cytochrome oxidase associated with disease duration. J. Neurosci., 21, 4923-4930.
87. Waite, P.M.E. & Tracey, D.J. (1995) Trigeminal sensory system. In Paxinos, G. (Ed.), The Rat Nervous System. Academic Press, San Diego, CA, pp. 705-724.
88. Wall, J.T., Xu, J. & 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.
89. Wall, P.D., Fitzgerald, M. & Gibson, S.J. (1981) The response of rat spinal cord cells to unmyelinated afferents after peripheral nerve section and after changes in substance P levels. Neuroscience, 6, 2205-2215.
90. Warren, R., Tremblay, N. & Dykes, R.W. (1989) Quantitative study of glutamic acid decarboxylase-immunoreactive neurons and cytochrome oxidase activity in normal and partially deafferented rat hindlimb somatosensory cortex. J. Comp. Neurol., 288, 583-592.
91. Welker, E., Soriano, E. & Van der, L.H. (1989) Plasticity in the barrel cortex of the adult mouse: effects of peripheral deprivation on GAD-immunoreactivity. Exp. Brain Res., 74, 441-452.
92. West, M.J., Slomianka, L. & Gundersen, H.J. (1991) Unbiased stereological estimation of the total number of neurons in thesubdivisions of the rat hippocampus using the optical fractionator. Anat. Rec., 231, 482-497.
93. Whittingstall, K. & Logothetis, N.K. (2009) Frequency-band coupling in surface EEG reflects spiking activity in monkey visual cortex. Neuron, 64, 281-289.
94. Wong-Riley, M. (1979) Changes in the visual system of monocularly sutured or enucleated cats demonstrable with cytochrome oxidase histochemistry. Brain Res., 171, 11-28.
95. Wong-Riley, M.T. (1989) Cytochrome oxidase: an endogenous metabolic marker for neuronal activity. Trends Neurosci., 12, 94-101.
96. Wong-Riley, M.T. & Carroll, E.W. (1984) Quantitative light and electron microscopic analysis of cytochrome oxidase-rich zones in V II prestriate cortex of the squirrel monkey. J. Comp. Neurol., 222, 18-37.
97. Woolsey, T.A., Welker, C. & Schwartz, R.H. (1975) Comparative anatomical studies of the SmL face cortex with special reference to the occurrence of "barrels" in layer IV. J. Comp. Neurol., 164, 79-94.