Detection of optogenetic stimulation in somatosensory cortex by non-human primates - Towards artificial tactile sensation

PLoS ONE

Volumn 9, Issue 12, 2014, Pages

  May, Travis ^a   Ozden, Ilker ^a   Brush, Benjamin ^a   Borton, David ^a,b   Wagner, Fabien ^c   Agha, Naubahar ^a   Sheinberg, David L ^c   Nurmikko, Arto V ^a,d  

^a Brown University   (United States)

^b EPFL   (Switzerland)

^c BROWN UNIVERSITY   (United States)

^d BROWN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

OPSIN;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; ELECTROSTIMULATION; NERVE CELL; NERVOUS SYSTEM ELECTROPHYSIOLOGY; NEUROMODULATION; NONHUMAN; OPTOGENETIC STIMULATION; OPTOGENETICS; RHESUS MONKEY; SOMATOSENSORY CORTEX; TACTILE STIMULATION; TASK PERFORMANCE; ADMINISTRATION AND DOSAGE; ANIMAL; DEPENDOPARVOVIRUS; EVOKED SOMATOSENSORY RESPONSE; GENE VECTOR; GENETICS; METABOLISM; PHYSIOLOGY; PROCEDURES; PROSTHESES AND ORTHOSES; TOUCH; VIROLOGY;

ANIMALIA; PRIMATES;

ANIMALS; DEPENDOVIRUS; EVOKED POTENTIALS, SOMATOSENSORY; GENETIC VECTORS; MACACA MULATTA; OPSINS; OPTOGENETICS; PROSTHESES AND IMPLANTS; SOMATOSENSORY CORTEX; TOUCH;

EID: 84919940775     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0114529     Document Type: Article

References (62)

1. Collinger JL, Wodlinger B, Downey JE, Wang W, Tyler-Kabara EC, et al. (2013) High-performance neuroprosthetic control by an individual with tetraplegia. Lancet 381: 557-64.
2. Hochberg LR, Bacher D, Jarosiewicz B, Masse NY, Simeral JD, et al. (2012) Reach and grasp by people with tetraplegia using a neurally controlled robotic arm. Nature 485: 372-5.
3. Hochberg LR, Serruya MD, Friehs GM, Mukand JA, Saleh M, et al. (2006) Neuronal ensemble control of prosthetic devices by a human with tetraplegia. Nature 442: 164-71.
4. Bensmaia SJ, Miller LE (2014) Restoring sensorimotor function through intracortical interfaces: progress and looming challenges. Nature reviews Neuroscience 15: 313-25.
5. Johansson RS, Flanagan JR (2009) Coding and use of tactile signals from the fingertips in object manipulation tasks. Nature reviews Neuroscience 10: 345-59.
6. Shaikhouni A, Donoghue JP, Hochberg LR (2013) Somatosensory responses in a human motor cortex. J Neurophysiol 109: 2192-204.
7. Botvinick M, Cohen J (1998) Rubber hands 'feel' touch that eyes see. Nature 391: 756.
8. Weber DJ, Friesen R, Miller LE (2012) Interfacing the somatosensory system to restore touch and proprioception: essential considerations. J Mot Behav 44: 403-18.
9. Hernandez A, Salinas E, Garcia R, Romo R (1997) Discrimination in the sense of flutter: new psychophysical measurements in monkeys. J Neurosci 17: 6391-400.
10. London BM, Jordan LR, Jackson CR, Miller LE (2008) Electrical stimulation of the proprioceptive cortex (area 3a) used to instruct a behaving monkey. IEEE Trans Neural Syst Rehabil Eng 16: 32-6.
11. O'Doherty JE, Lebedev MA, Li Z, Nicolelis MA (2012) Virtual active touch using randomly patterned intracortical microstimulation. IEEE Trans Neural Syst Rehabil Eng 20: 85-93.
12. Romo R, Hernandez A, Zainos A, Salinas E (1998) Somatosensory discrimination based on cortical microstimulation. Nature 392: 387-90.
13. Romo R, Merchant H, Zainos A, Hernandez A (1996) Categorization of somaesthetic stimuli: sensorimotor performance and neuronal activity in primary somatic sensory cortex of awake monkeys. Neuroreport 7: 1273-9.
14. Tabot GA, Kim SS, Winberry JE, Bensmaia SJ (2014) Restoring tactile and proprioceptive sensation through a brain interface. Neurobiol Dis.
15. Penfield W, Boldrey E (1937) Somatic motor and sensory representation in the cerebral cortex of man as studied by electrical stimulation. Brain 60: 389-443.
16. Rolston JD, Gross RE, Potter SM (2009) A low-cost multielectrode system for data acquisition enabling real-time closed-loop processing with rapid recovery from stimulation artifacts. Front Neuroeng 2: 12.
17. Butovas S, Schwarz C (2003) Spatiotemporal effects of microstimulation in rat neocortex: a parametric study using multielectrode recordings. J Neurophysiol 90: 3024-39.
18. Histed MH, Bonin V, Reid RC (2009) Direct activation of sparse, distributed populations of cortical neurons by electrical microstimulation. Neuron 63: 508-22.
19. Tehovnik EJ, Tolias AS, Sultan F, Slocum WM, Logothetis NK (2006) Direct and indirect activation of cortical neurons by electrical microstimulation. J Neurophysiol 96: 512-21.
20. Bernstein JG, Boyden ES (2011) Optogenetic tools for analyzing the neural circuits of behavior. Trends Cogn Sci 15: 592-600.
21. Deisseroth K (2011) Optogenetics. Nat Methods 8: 26-9.
22. Packer AM, Roska B, Hausser M (2013) Targeting neurons and photons for optogenetics. Nat Neurosci 16: 805-15.
23. Tye KM, Deisseroth K (2012) Optogenetic investigation of neural circuits underlying brain disease in animal models. Nat Rev Neurosci 13: 251-66.
24. Yizhar O, Fenno LE, Prigge M, Schneider F, Davidson TJ, et al. (2011) Neocortical excitation/inhibition balance in information processing and social dysfunction. Nature 477: 171-8.
25. Covington HE, Lobo MK, Maze I, Vialou V, Hyman JM, et al. (2010) Antidepressant effect of optogenetic stimulation of the medial prefrontal cortex. The Journal of neuroscience: the official journal of the Society for Neuroscience 30: 16082-90.
26. Haubensak W, Kunwar PS, Cai H, Ciocchi S, Wall NR, et al. (2010) Genetic dissection of an amygdala microcircuit that gates conditioned fear. Nature 468: 270-6.
27. Kravitz AV, Freeze BS, Parker PR, Kay K, Thwin MT, et al. (2010) Regulation of parkinsonian motor behaviours by optogenetic control of basal ganglia circuitry. Nature 466: 622-6.
28. Tye KM, Mirzabekov JJ, Warden MR, Ferenczi EA, Tsai HC, et al. (2013) Dopamine neurons modulate neural encoding and expression of depression-related behaviour. Nature 493: 537-41.
29. Cardin JA, Carlen M, Meletis K, Knoblich U, Zhang F, et al. (2009) Driving fast-spiking cells induces gamma rhythm and controls sensory responses. Nature 459: 663-7.
30. Guo ZV, Li N, Huber D, Ophir E, Gutnisky D, et al. (2014) Flow of cortical activity underlying a tactile decision in mice. Neuron 81: 179-94.
31. Huber D, Petreanu L, Ghitani N, Ranade S, Hromadka T, et al. (2008) Sparse optical microstimulation in barrel cortex drives learned behaviour in freely moving mice. Nature 451: 61-4.
32. Mateo C, Avermann M, Gentet LJ, Zhang F, Deisseroth K, et al. (2011) In vivo optogenetic stimulation of neocortical excitatory neurons drives brain-state-dependent inhibition. Curr Biol 21: 1593-602.
33. Petreanu L, Huber D, Sobczyk A, Svoboda K (2007) Channelrhodopsin-2-assisted circuit mapping of long-range callosal projections. Nat Neurosci 10: 663-8.
34. Stamatakis AM, Jennings JH, Ung RL, Blair GA, Weinberg RJ, et al. (2013) A unique population of ventral tegmental area neurons inhibits the lateral habenula to promote reward. Neuron 80: 1039-53.
35. Warden MR, Selimbeyoglu A, Mirzabekov JJ, Lo M, Thompson KR, et al. (2012) A prefrontal cortex-brainstem neuronal projection that controls response to behavioural challenge. Nature 492: 428-32.
36. O'Connor DH, Hires SA, Guo ZV, Li N, Yu J, et al. (2013) Neural coding during active somatosensation revealed using illusory touch. Nature neuroscience 16: 958-65.
37. Diester I, Kaufman MMT, Mogri M, Pashaie R, Goo W, et al. (2011) An optogenetic toolbox designed for primates. Nature Neuroscience 14: 387-397.
38. Han X (2012) Optogenetics in the nonhuman primate, volume 196. Elsevier B.V., 1 edition, 215-33 pp. doi:10.1016/B978-0-444-59426-6.00011-2.
39. Jazayeri M, Lindbloom-Brown Z, Horwitz GD (2012) Saccadic eye movements evoked by optogenetic activation of primate v1. Nat Neurosci 15: 1368-70.
40. Gerits A, Farivar R, Rosen B, Wald L, Boyden E, et al. (2012) Optogenetically Induced Behavioral and Functional Network Changes in Primates. Current Biology: 1-5.
41. Ohayon S, Grimaldi P, Schweers N, Tsao DY (2013) Saccade modulation by optical and electrical stimulation in the macaque frontal eye field. J Neurosci 33: 16684-97.
42. Dai J, Brooks DI, Sheinberg DL (2014) Optogenetic and electrical microstimulation systematically bias visuospatial choice in primates. Curr Biol 24: 63-9.
43. Ozden I, Wang J, Lu Y, May T, Lee J, et al. (2013) A coaxial optrode as multifunction write-read probe for optogenetic studies in non-human primates. Journal of neuroscience methods: 1-12.
44. Wickens TD (2001) Elementary signal detection theory, volume 1. Oxford University Press, 262 pp.
45. Tabot Ga, Dammann JF, Berg Ja, Tenore FV, Boback JL, et al. (2013) Restoring the sense of touch with a prosthetic hand through a brain interface. Proceedings of the National Academy of Sciences of the United States of America.
46. Venkatraman S, Carmena JM (2011) Active sensing of target location encoded by cortical microstimulation. IEEE transactions on neural systems and rehabilitation engineering: a publication of the IEEE Engineering in Medicine and Biology Society 19: 317-24.
47. O'Doherty JE, Lebedev MA, Ifft PJ, Zhuang KZ, Shokur S, et al. (2011) Active tactile exploration using a brain-machine-brain interface. Nature 479: 228-31.
48. Doty R (1969) Electrical stimulation of the brain in behavioral context. Annual review of psychology.
49. Ochoa JL (2010) Intraneural microstimulation in humans. Neuroscience Letters 470: 162-167.
50. Houweling AR, Brecht M (2008) Behavioural report of single neuron stimulation in somatosensory cortex. Nature 451: 65-8.
51. Histed M, Maunsell J (2014) Cortical neural populations can guide behavior by integrating inputs linearly, independent of synchrony. Proceedings of the National ... 2013.
52. Histed MH, Ni AM, Maunsell JHR (2013) Progress in Neurobiology Insights into cortical mechanisms of behavior from microstimulation experiments. Progress in Neurobiology 103: 115-130.
53. Ni AM, Maunsell JHR (2010) Microstimulation reveals limits in detecting different signals from a local cortical region. Current biology: CB 20: 824-8.
54. Murphey DK, Maunsell JHR, Beauchamp MS, Yoshor D (2009) Perceiving electrical stimulation of identified human visual areas. Proceedings of the National Academy of Sciences of the United States of America 106: 5389-93.
55. Murphey DK, Maunsell JHR (2007) Behavioral detection of electrical microstimulation in different cortical visual areas. Current biology: CB 17: 862-7.
56. O'Doherty JE, Lebedev MA, Hanson TL, Fitzsimmons NA, Nicolelis MA (2009) A brain-machine interface instructed by direct intracortical microstimulation. Front Integr Neurosci 3: 20.
57. Berg J, Dammann J, Tenore F, Tabot G, Boback J, et al. (2013) Behavioral demonstration of a somatosensory neuroprosthesis. IEEE transactions on neural systems and rehabilitation engineering: a publication of the IEEE Engineering in Medicine and Biology Society.
58. Goodwin AW, Wheat HE (2004) Sensory signals in neural populations underlying tactile perception and manipulation. Annu Rev Neurosci 27: 53-77.
59. Luna R, Hernández A, Brody CD, Romo R (2005) Neural codes for perceptual discrimination in primary somatosensory cortex. Nature neuroscience 8: 1210-9.
60. Nicolelis MA, Ghazanfar AA, Stambaugh CR, Oliveira LM, Laubach M, et al. (1998) Simultaneous encoding of tactile information by three primate cortical areas. Nat Neurosci 1: 621-30.
61. Ghazanfar AA, Stambaugh CR, Nicolelis MA (2000) Encoding of tactile stimulus location by somatosensory thalamocortical ensembles. J Neurosci 20: 3761-75.
62. Nevalainen P, Lauronen L, Pihko E (2014) Development of human somatosensory cortical functions what have we learned from magnetoencephalography: A review. Frontiers in Human Neuroscience 8.