Restoring tactile and proprioceptive sensation through a brain interface

Neurobiology of Disease

Volumn 83, Issue , 2015, Pages 191-198

  Tabot, Gregg A ^a   Kim, Sung Shin ^b   Winberry, Jeremy E ^b   Bensmaia, Sliman J ^a,b  

^a UNIVERSITY OF CHICAGO   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

Author keywords

Brain machine interface; Intracortical microstimulation; Neuroprosthetics; Somatosensation; Somatosensory cortex

Indexed keywords

AGNOSIA; ARM PROSTHESIS; BRAIN COMPUTER INTERFACE; DEVICE SAFETY; ELECTROSTIMULATION THERAPY; HUMAN; MOTOR CONTROL; NERVE CELL PLASTICITY; NEUROPROSTHESIS; NONHUMAN; PRIORITY JOURNAL; PROPRIOCEPTION; RELIABILITY; REVIEW; SOMATOSENSORY CORTEX; TACTILE DISCRIMINATION; TOUCH; ADAPTATION; AMPUTEE; ANIMAL; BIOMIMETICS; ELECTROSTIMULATION; INNERVATION; NERVE CELL; PATHOPHYSIOLOGY; PHYSIOLOGY; PROSTHESES AND ORTHOSES; PSYCHOMOTOR PERFORMANCE; REHABILITATION; SELF CONCEPT; SENSORY FEEDBACK; UPPER LIMB;

ADAPTATION, PHYSIOLOGICAL; AMPUTEES; ANIMALS; BIOMIMETICS; BRAIN-COMPUTER INTERFACES; ELECTRIC STIMULATION; FEEDBACK, SENSORY; HUMANS; NEURONAL PLASTICITY; NEURONS; PROPRIOCEPTION; PROSTHESES AND IMPLANTS; PSYCHOMOTOR PERFORMANCE; SELF CONCEPT; SOMATOSENSORY CORTEX; TOUCH; TOUCH PERCEPTION; UPPER EXTREMITY;

EID: 84948775961     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2014.08.029     Document Type: Review

References (85)

1. Barrese J.C., et al. Failure mode analysis of silicon-based intracortical microelectrode arrays in non-human primates. J. Neural Eng. 2013, 10:066014.
2. Bensmaia S.J., Tillery S.H. Tactile feedback from the hand. The Human Hand: A Source of Inspiration for Robotic Hands 2013, Springer, New York. R. Balasubramaniam (Ed.).
3. Bensmaia S.J., et al. The representation of stimulus orientation in the early stages of somatosensory processing. J. Neurosci. 2008, 28:776-786.
4. Berg J.A., et al. Behavioral demonstration of a somatosensory neuroprosthesis. IEEE Trans. Neural Syst. Rehabil. Eng. 2013, 21:500-507.
5. Biddiss E., et al. Consumer design priorities for upper limb prosthetics. Disabil. Rehabil. Assist. Technol. 2007, 2:346-357.
6. Birbaumer N., et al. Effects of regional anesthesia on phantom limb pain are mirrored in changes in cortical reorganization. J. Neurosci. 1997, 17:5503-5508.
7. Bjorkman A., et al. Phantom digit somatotopy: a functional magnetic resonance imaging study in forearm amputees. Eur. J. Neurosci. 2012, 36:2098-2106.
8. Björnsdotter M., et al. Somatotopic organization of gentle touch processing in the posterior insular cortex. J. Neurosci. 2009, 29:9314-9320.
9. Borsook D., et al. Acute plasticity in the human somatosensory cortex following amputation. Neuroreport 1998, 9:1013-1017.
10. Botvinick M., Cohen J. Rubber hands 'feel' touch that eyes see. Nature 1998, 391:756.
11. Brochier T., et al. The effects of muscimol inactivation of small regions of motor and somatosensory cortex on independent finger movements and force control in the precision grip. Exp. Brain Res. 1999, 128:31-40.
12. Chen K.H., et al. The effect of chronic intracortical microstimulation on the electrode-tissue interface. J. Neural Eng. 2014, 11:026004.
13. Collinger J.L., et al. High-performance neuroprosthetic control by an individual with tetraplegia. Lancet 2013, 381:557-564.
14. Dadarlat M.C., et al. Multisensory integration of vision and intracortical microstimulation for sensory substitution and augmentation. Society for Neuroscience 2012, Society for Neuroscience, New Orleans, LA. S. Neuroscience (Ed.).
15. Daly J., et al. Optimal space-time precoding of artificial sensory feedback through mutichannel microstimulation in bi-directional brain-machine interfaces. J. Neural Eng. 2012, 9:065004.
16. Davis K.D., et al. Phantom sensations generated by thalamic microstimulation. Nature 1998, 391:385-387.
17. Dinse H.R., et al. Alterations in correlated activity parallel ICMS-induced representational plasticity. Neuroreport 1993, 5:173-176.
18. Edin B.B. Finger joint movement sensitivity of non-cutaneous mechanoreceptor afferents in the human radial nerve. Exp. Brain Res. 1990, 82:417-422.
19. Edin B.B. Quantitative analyses of dynamic strain sensitivity in human skin mechanoreceptors. J. Neurophysiol. 2004, 92:3233-3243.
20. Elbert T., et al. Increased cortical representation of the fingers of the left hand in string players. Science 1995, 270:305-307.
21. Farne A., et al. Face or hand, not both: perceptual correlates of reafferentation in a former amputee. Curr. Biol. 2002, 12:1342-1346.
22. Flor H., et al. Phantom-limb pain as a perceptual correlate of cortical reorganization following arm amputation. Nature 1995, 375:482-484.
23. Frey S.H., et al. Chronically deafferented sensory cortex recovers a grossly typical organization after allogenic hand transplantation. Curr. Biol. 2008, 18:1530-1534.
24. Gazzola V., et al. Primary somatosensory cortex discriminates affective significance in social touch. Proc. Natl. Acad. Sci. 2012, 109:E1657-E1666.
25. Godde B., et al. Plasticity of orientation preference maps in the visual cortex of adult cats. Proc. Natl. Acad. Sci. 2002, 99:6352-6357.
26. Gordon J., et al. Impairments of reaching movements in patients without proprioception. I. Spatial errors. J. Neurophysiol. 1995, 73:347-360.
27. Grusser S.M., et al. The relationship of perceptual phenomena and cortical reorganization in upper extremity amputees. Neuroscience 2001, 102:263-272.
28. Harvey M.A., et al. Multiplexing stimulus information through rate and temporal codes in primate somatosensory cortex. PLoS Biol. 2013, 11:e1001558.
29. Hertenstein M.J., et al. The communication of emotion via touch. Emotion 2009, 9:566.
30. Histed M.H., et al. Direct activation of sparse, distributed populations of cortical neurons by electrical microstimulation. Neuron 2009, 63:508-522.
31. Hochberg L.R., et al. Reach and grasp by people with tetraplegia using a neurally controlled robotic arm. Nature 2012, 485:372-375.
32. Jenkins W.M., et al. Functional reorganization of primary somatosensory cortex in adult owl monkeys after behaviorally controlled tactile stimulation. J. Neurophysiol. 1990, 63:82-104.
33. Johansson R.S., Flanagan J.R. Coding and use of tactile signals from the fingertips in object manipulation tasks. Nat. Rev. Neurosci. 2009, 10:345-359.
34. Johnson L.A., et al. Direct electrical stimulation of the somatosensory cortex in humans using electrocorticography electrodes: a qualitative and quantitative report. J. Neural Eng. 2013, 10:036021.
35. Kambi N., et al. Large-scale reorganization of the somatosensory cortex following spinal cord injuries is due to brainstem plasticity. Nat. Commun. 2014, 5:3602.
36. Kane S., et al. Electrical performance of penetrating microelectrodes chronically implanted in cat cortex. IEEE Trans. Biomed. Eng. 2013, 60:2153-2160.
37. Karl A., et al. Reorganization of motor and somatosensory cortex in upper extremity amputees with phantom limb pain. J. Neurosci. 2001, 21:3609-3618.
38. Keysers C., et al. Somatosensation in social perception. Nat. Rev. Neurosci. 2010, 11:417-428.
39. Kringelbach M.L. The human orbitofrontal cortex: linking reward to hedonic experience. Nat. Rev. Neurosci. 2005, 6:691-702.
40. Lenz F.A., Byl N.N. Reorganization in the cutaneous core of the human thalamic principal somatic sensory nucleus (Ventral caudal) in patients with dystonia. J. Neurophysiol. 1999, 82:3204-3212.
41. Lenz F.A., et al. Neuronal activity in the region of the thalamic principal sensory nucleus (ventralis caudalis) in patients with pain following amputations. Neuroscience 1998, 86:1065-1081.
42. Logothetis N.K., et al. The effects of electrical microstimulation on cortical signal propagation. Nat. Neurosci. 2010, 13:1283-1291.
43. Löken L.S., et al. Coding of pleasant touch by unmyelinated afferents in humans. Nat. Neurosci. 2009, 12:547-548.
44. London B.M., Miller L.E. Responses of somatosensory area 2 neurons to actively and passively generated limb movements. J. Neurophysiol. 2013, 109:1505-1513.
45. London B.M., et al. Electrical stimulation of the proprioceptive cortex (area 3a) used to instruct a behaving monkey. IEEE Trans. Neural Syst. Rehabil. Eng. 2008, 16:32-36.
46. Makin T.R., et al. Deprivation-related and use-dependent plasticity go hand in hand. Elife. 2013, 2:e01273. (Nov 12). 10.7554/eLife.01273.
47. Marasco P.D., et al. Robotic touch shifts perception of embodiment to a prosthesis in targeted reinnervation amputees. Brain 2011, 134:747-758.
48. Marsden C., et al. The use of peripheral feedback in the control of movement. Trends Neurosci. 1984, 7:253-257.
49. McCreery D., et al. Neuronal loss due to prolonged controlled-current stimulation with chronically implanted microelectrodes in the cat cerebral cortex. J. Neural Eng. 2010, 7:036005.
50. Merzenich M.M., et al. Somatosensory cortical map changes following digit amputation in adult monkeys. J. Comp. Neurol. 1984, 224:591-605.
51. Nelson A.J., et al. Digit-specific aberrations in the primary somatosensory cortex in Writer's cramp. Ann. Neurol. 2009, 66:146-154.
52. O'Connor D.H., et al. Neural coding during active somatosensation revealed using illusory touch. Nat. Neurosci. 2013, 16:958-965.
53. O'Doherty J.E., et al. Active tactile exploration using a brain-machine-brain interface. Nature 2011, 479:228-231.
54. Ojemann J.G., Silbergeld D.L. Cortical stimulation mapping of phantom limb rolandic cortex. Case report. J. Neurosurg. 1995, 82:641-644.
55. Overstreet C., et al. Computational modeling of direct neuronal recruitment during intracortical microstimulation in somatosensory cortex. J. Neural Eng. 2013, 10:066016.
56. Parker R.A., et al. The functional consequences of chronic, physiologically effective intracortical microstimulation. Progress in Brain Research 2011, 145-165. Elsevier. J. Schouenborg (Ed.).
57. Pei Y.C., et al. Convergence of submodality-specific input onto neurons in primary somatosensory cortex. J. Neurophysiol. 2009, 102:1843-1853.
58. Pei Y.C., et al. Shape invariant coding of motion direction in somatosensory cortex. PLoS Biol. 2010, 8:e1000305.
59. Pei Y.C., et al. Neural mechanisms of tactile motion integration in somatosensory cortex. Neuron 2011, 69:536-547.
60. Penfield W., Boldrey E. Somatic motor and sensory representation in the cerebral cortex of man as studied by electrical stimulation. Brain 1937, 60:389-443.
61. Prasad A., et al. Comprehensive characterization and failure modes of tungsten microwire arrays in chronic neural implants. J. Neural Eng. 2012, 9:056015.
62. Ramachandran V.S., Hirstein W. The perception of phantom limbs. The D. O. Hebb lecture. Brain 1998, 121(Pt 9):1603-1630.
63. Rolls E.T., et al. Representations of pleasant and painful touch in the human orbitofrontal and cingulate cortices. Cereb. Cortex 2003, 13:308-317.
64. Romo R., et al. Somatosensory discrimination based on cortical microstimulation. Nature 1998, 392:387-390.
65. Romo R., et al. Sensing without touching: psychophysical performance based on cortical microstimulation. Neuron 2000, 26:273-278.
66. Rosselet C., et al. Experience-dependent changes in spatiotemporal properties of cutaneous inputs remodel somatosensory cortical maps following skin flap rotation. Eur. J. Neurosci. 2008, 27:1245-1260.
67. Sainburg R.L., et al. Loss of proprioception produces deficits in interjoint coordination. J. Neurophysiol. 1993, 70:2136-2147.
68. Sainburg R.L., et al. Control of limb dynamics in normal subjects and patients without proprioception. J. Neurophysiol. 1995, 73:820-835.
69. Sherman R.A. Stump and phantom limb pain. Neurol. Clin. 1989, 7:249-264.
70. Shokur S., et al. Expanding the primate body schema in sensorimotor cortex by virtual touches of an avatar. Proc. Natl. Acad. Sci. 2013, 110:15121-15126.
71. Simeral J.D., et al. Some preliminary longitudinal findings from five trial participants using the BrainGate neural interface system. Soc. Neurosci. 2011, 142.04. (Society for Neuroscience, San Diego, CA).
72. Stoney S., et al. Excitation of pyramidal tract cells by intracortical microstimulation: effective extent of stimulating current. J. Neurophysiol. 1968, 31:659-669.
73. Stuart G., et al. Action potential initiation and backpropagation in neurons of the mammalian CNS. Trends Neurosci. 1997, 20:125-131.
74. Tabot G.A., et al. Restoring the sense of touch with a prosthetic hand through a brain interface. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:18279-18284.
75. Tecchio F., et al. Carpal tunnel syndrome modifies sensory hand cortical somatotopy: a MEG study. Hum. Brain Mapp. 2002, 17:28-36.
76. Tehovnik E.J. Electrical stimulation of neural tissue to evoke behavioral responses. J. Neurosci. Methods 1996, 65:1-17.
77. Thomson E.E., et al. Perceiving invisible light through a somatosensory cortical prosthesis. Nat. Commun. 2013, 4:1482.
78. Tomlinson T., Miller L.E. Multi-electrode stimulation in somatosensory are 2 induces a natural sensation of limb movement. Society for Neuroscience 2013, Society for Neuroscience, San Diego, CA.
79. Tsakiris M., Haggard P. The rubber hand illusion revisited: visuotactile integration and self-attribution. J. Exp. Psychol. Hum. Percept. Perform. 2005, 31:80-91.
80. Venkatraman S., Carmena J.M. Active sensing of target location encoded by cortical microstimulation. IEEE Trans. Neural Syst. Rehabil. Eng. 2011, 19:317-324.
81. Waberski T.D., et al. Immediate cortical reorganization after local anesthetic block of the thumb: source localization of somatosensory evoked potentials in human subjects. Neurosci. Lett. 2003, 347:151-154.
82. Waberski T.D., et al. Short-term cortical reorganization by deafferentation of the contralateral sensory cortex. Neuroreport 2007, 18:1199-1203.
83. Weiss T., et al. Rapid functional plasticity of the somatosensory cortex after finger amputation. Exp. Brain Res. 2000, 134:199-203.
84. Woolsey C.N., et al. Localization in somatic sensory and motor areas of human cerebral cortex as determined by direct recording of evoked potentials and electrical stimulation. J. Neurosurg. 1979, 51:476-506.
85. Wright T.W., et al. Prosthetic usage in major upper extremity amputations. J. Hand. Surg. [Am.] 1995, 20:619-622.