What single-cell stimulation has told us about neural coding

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 370, Issue 1677, 2015, Pages

  Doron, Guy ^a   Brecht, Michael ^a  

^a HUMBOLDT UNIVERSITY   (Germany)

Author keywords

Motor control; Nanostimulation; Patch clamp; Sensation; Single neuron

Indexed keywords

BRAIN; CELLS AND CELL COMPONENTS; ELECTRIC FIELD; NERVOUS SYSTEM; NEUROLOGY; SENSORY SYSTEM;

ANIMAL; BIOLOGICAL MODEL; BRAIN; CYTOLOGY; ELECTROSTIMULATION; EVOKED RESPONSE; HUMAN; MOTONEURON; MOTOR CORTEX; NERVE CELL; OPTOGENETICS; PHYSIOLOGY; PROCEDURES; SENSORY NERVE CELL; SINGLE CELL ANALYSIS; SOMATOSENSORY CORTEX;

ANIMALS; BRAIN; ELECTRIC STIMULATION; EVOKED POTENTIALS; HUMANS; MODELS, NEUROLOGICAL; MOTOR CORTEX; MOTOR NEURONS; NEURONS; OPTOGENETICS; SENSORY RECEPTOR CELLS; SINGLE-CELL ANALYSIS; SOMATOSENSORY CORTEX;

EID: 84938529984     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2014.0204     Document Type: Review

References (125)

1. Fritsch G, Hitzig E. 1870 Ueber die elektrische Erregbarkeit des Grosshirns. Arch. Anat. Physiol Wiss. Med. 37, 300–332
2. Penfield W, Boldery P. 1937 Somatic motor and sensory representation in the cerebral cortex of man as studied by electrical stimulation. Brain 60, 389–443. (doi:10.1093/brain/60.4.389)
3. Asanuma H, Sakata H. 1967 Functional organization of a cortical efferent system examined with focal depth stimulation in cats. J. Neurophysiol. 30, 35–54
4. Tehovnik EJ. 1996 Electrical stimulation of neural tissue to evoke behavioral responses. J. Neurosci. Methods 65, 1–17. (doi:10.1016/0165-0270(95)00131-X)
5. Clark KL, Armstrong KM, Moore T. 2011 Probing neural circuitry and function with electrical microstimulation. Proc. R. Soc. B 278, 1121–1130 (doi:10.1098/rspb.2010.2211)
6. Salzman CD, Britten KH, Newsome WT. 1990 Cortical microstimulation influences perceptual judgements of motion direction. Nature 346, 174–177. (doi:10.1038/346174a0)
7. Romo R, Hernandez A, Zainos A, Salinas E. 1998 Somatosensory discrimination based on cortical microstimulation. Nature 392, 387–390. (doi:10.1038/32891)
8. Afraz SR, Kiani R, Esteky H. 2006 Microstimulation of inferotemporal cortex influences face categorization. Nature 442, 692–695. (doi:10.1038/nature04982)
9. Strick PL, Preston JB. 1978 Multiple representation in the primate motor cortex. Brain Res. 154, 366–370. (doi:10.1016/0006-8993(78)90707-2)
10. Graziano MSA, Taylor CSR, Moore T. 2002 Complex movements evoked by microstimulation of precentral cortex. Neuron 34, 841–851. (doi:10.1016/S0896-6273(02)00698-0)
11. Graziano MSA, Patel KT, Taylor CSR. 2004 Mapping from motor cortex to biceps and triceps altered by elbow angle. J. Neurophysiol. 92, 395–407. (doi:10.1152/jn.01241.2003)
12. Moore T, Fallah M. 2001 Control of eye movements and spatial attention. Proc. Natl Acad. Sci. USA 98, 1273–1276. (doi:10.1073/pnas021549498)
13. Hanks TD, Ditterich J, Shadlen MN. 2006 Microstimulation of macaque area LIP affects decision-making in a motion discrimination task Nat. Neurosci. 9, 682–689. (doi:10.1038/nn1683)
14. Williams ZM, Eskandar EN. 2006 Selective enhancement of associative learning by microstimulation of the anterior caudate. Nat Neurosci. 9, 562–568. (doi:10.1038/nn1662)
15. Salzman CD, Murasugi CM, Britten KH, Newsome WT. 1992 Microstimulation in visual area MT: effects on direction discrimination performance. J. Neurosci 12, 2331–2355
16. Salzman CD, Newsome WT. 1994 Neural mechanisms for forming a perceptual decision Science 264, 231–237. (doi:10.1126/science8146653)
17. Murasugi CM, Salzman CD, Newsome WT. 1993 Microstimulation in visual area MT: effects of varying pulse amplitude and frequency. J. Neurosci 13, 1719–1729
18. DeAngelis GC, Cumming BG, Newsome WT. 1998 Cortical area MT and the perception of stereoscopic depth. Nature 394, 677–680. (doi:10.1038/29299)
19. Krug K, Cicmil N, Parker AJ, Cumming BG. 2013 A causal role for V5/MT neurons coding motiondisparity conjunctions in resolving perceptual ambiguity. Curr. Biol. 23, 1454–1459. (doi:10.1016/j.cub.2013.06.023)
20. Romo R, Hernández A, Zainos A, Brody CD, Lemus L 2000 Sensing without touching: psychophysical performance based on cortical microstimulation Neuron 26, 273–278. (doi:10.1016/S0896-6273(00)81156-3)
21. Butovas S, Schwarz C. 2007 Detection psychophysics of intracortical microstimulation in rat primary somatosensory cortex. Eur. J. Neurosci. 25, 2161–169. (doi:10.1111/j.1460-9568.2007.05449.x)
22. Brecht M, Sakmann B. 2002 Whisker maps of neuronal subclasses of the rat ventral posterior medial thalamus, identified by whole-cell voltage recording and morphological reconstruction J. Physiol. 538, 495–515. (doi:10.1113/jphysiol2001.012334)
23. Brecht M, Roth A, Sakmann B. 2003 Dynamic receptive fields of reconstructed pyramidal cells in layers 3 and 2 of rat somatosensory barrel cortex J. Physiol. 553, 243–265. (doi:10.1113/jphysiol2003.044222)
24. Greenberg DS, Houweling AR, Kerr JN. 2008 Population imaging of ongoing neuronal activity in the visual cortex of awake rats. Nat. Neurosci. 11, 749–751. (doi:10.1038/nn.2140)
25. Hahnloser RH, Kozhevnikov AA, Fee MS. 2002 An ultra-sparse code underlies the generation of neural sequences in a songbird. Nature 419, 65–70 (doi:10.1038/nature00974)
26. Huber D, Petreanu L, Ghitani N, Ranade S, Hromadka T, Mainen Z, Svoboda K. 2008 Sparse optical microstimulation in barrel cortex drives learned behaviour in freely moving mice. Nature 451, 61–64. (doi:10.1038/nature06445)
27. Olshausen BA, Field DJ. 2004 Sparse coding of sensory inputs. Curr. Opin. Neurobiol. 14, 481–487 (doi:10.1016/j.conb.2004.07.007)
28. Wolfe J, Houweling AR, Brecht M. 2010 Sparse and powerful cortical spikes. Curr. Opin. Neurobiol. 20, 306–312. (doi:10.1016/j.conb.2010.03.006)
29. Vallbo AB, Olsson KA, Westberg KG, Clark FJ. 1984 Microstimulation of single tactile afferents from the human hand. Sensory attributes related to unit type and properties of receptive fields. Brain 107, 727–749. (doi:10.1093/brain/107.3.727)
30. Voigt BC, Brecht M, Houweling AR. 2008 Behavioral detectability of single-cell stimulation in the ventral posterior medial nucleus of the thalamus J. Neurosci. 28, 12362–12367. (doi:10.1523/JNEUROSCI.3046-08.2008)
31. Doron G, von Heimendahl M, Schlattmann P, Houweling AR, Brecht M. 2014 Spiking irregularity and frequency modulate the behavioral report of single-neuron stimulation. Neuron 81, 653–663 (doi:10.1016/j.neuron.2013.11.032)
32. Vallbo AB. 1981 Sensations evoked from the glabrous skin of the human hand by electrical stimulation of unitary mechanosensitive afferents Brain Res. 215, 359–363. (doi:10.1016/0006-8993(81)90517-5)
33. Torebjörk HE, Ochoa JL. 1980 Specific sensations evoked by activity in single identified sensory units in man. Acta Physiol. Scand. 110, 445–447 (doi:10.1111/j.1748-1716.1980.tb06695.x)
34. Torebjörk HE, Vallbo AB, Ochoa JL. 1987 Intraneural microstimulation in man. Its relation to specificity of tactile sensations. Brain J. Neurol. 110 1509–1529. (doi:10.1093/brain/110.6.1509)
35. Hamill OP, Marty A, Neher E, Sakmann B, Sigworth FJ. 1981 Improved patch-clamp techniques for highresolution current recording from cells and cell-free membrane patches. Pflu¨g. Arch. Eur. J. Physiol. 391, 85–100. (doi:10.1007/BF00656997)
36. Helmchen F, Waters J. 2002 Ca2þ imaging in the mammalian brain in vivo. Eur. J. Pharmacol. 447, 119–129. (doi:10.1016/S0014-2999(02)01836-8)
37. Mainen ZF, Sejnowski TJ. 1995 Reliability of spike timing in neocortical neurons. Science 268, 1503–1506. (doi:10.1126/science.7770778)
38. Crochet S, Petersen CC. 2006 Correlating whisker behavior with membrane potential in barrel cortex of awake mice. Nat. Neurosci. 9, 608–610. (doi:10.1038/nn1690)
39. Lee AK, Manns ID, Sakmann B, Brecht M. 2006 Whole-cell recordings in freely moving rats. Neuron 51, 399–407. (doi:10.1016/j.neuron.2006.07.004)
40. Margrie TW, Brecht M, Sakmann B. 2002 In vivo, low-resistance, whole-cell recordings from neurons in the anaesthetized and awake mammalian brain Pflu¨g. Arch. Eur. J. Physiol. 444, 491–498. (doi:10.1007/s00424-002-0831-z)
41. Steriade M, Timofeev I, Grenier F. 2001 Natural waking and sleep states: a view from inside neocortical neurons. J. Neurophysiol. 85, 1969–1985
42. Margrie TW, Meyer AH, Caputi A, Monyer H, Hasan MT, Schaefer AT, Denk W, Brecht M. 2003 Targeted whole-cell recordings in the mammalian brain in vivo. Neuron 39, 911–918. (doi:10.1016/j.neuron2003.08.012)
43. Kitamura K, Judkewitz B, Kano M, Denk W, Häusser M. 2008 Targeted patch-clamp recordings and single-cell electroporation of unlabeled neurons in vivo. Nat. Methods 5, 61–67. (doi:10.1038/nmeth1150)
44. Houweling AR, Doron G, Voigt BC, Herfst LJ, Brecht M. 2010 Nanostimulation: manipulation of single neuron activity by juxtacellular current injection J. Neurophysiol. 103, 1696–1704. (doi:10.1152/ jn.00421.2009)
45. Pinault D. 1994 Golgi-like labeling of a single neuron recorded extracellularly. Neurosci. Lett. 170, 255–260. (doi:10.1016/0304-3940(94)90332-8)
46. Pinault D. 1996 A novel single-cell staining procedure performed in vivo under electrophysiological control: morpho-functional features of juxtacellularly labeled thalamic cells and other central neurons with biocytin or neurobiotin J. Neurosci. Methods 65, 113–136. (doi:10.1016/0165-0270(95)00144-1)
47. Andrew RD, Fagan M. 1990 A technique for controlling the membrane potential of neurons during unit recording. J. Neurosci. Methods 33, 55–60. (doi:10.1016/0165-0270(90)90082-Q)
48. Brons JF, Woody CD, Allon N. 1982 Changes in excitability to weak-intensity extracellular electrical stimulation of units of pericruciate cortex in cats J. Neurophysiol. 47, 377–388
49. Cruikshank SJ, Weinberger NM. 1996 Receptive-field plasticity in the adult auditory cortex induced by Hebbian covariance. J. Neurosci. 16, 861–875
50. Frégnac Y, Shulz D, Thorpe S, Bienenstock E. 1988 A cellular analogue of visual cortical plasticity. Nature 333, 367–370. (doi:10.1038/333367a0)
51. Frégnac Y, Shulz D, Thorpe S, Bienenstock E. 1992 Cellular analogs of visual cortical pigenesis I. Plasticity of orientation selectivity. J. Neurosci 12, 1280–1300
52. Lavallé P, Deschênes M. 2004 Dendroarchitecture and lateral inhibition in thalamic barreloids J. Neurosci. 24, 6098–6105. (doi:10.1523/ JNEUROSCI.0973-04.2004)
53. Doron G, Doose J, Brecht M, Lindner B. 2014 Enhancement and modelling of spike timing reliability in vivo using noise evoked by juxtacellular stimulation [Abstract]. Soc. Neurosci. Abstr. 15, 441
54. Houweling AR, Brecht M. 2008 Behavioural report of single neuron stimulation in somatosensory cortex Nature 451, 65–68. (doi:10.1038/nature06447)
55. Feldmeyer D, Egger V, Lubke J, Sakmann B. 1999 Reliable synaptic connections between pairs of excitatory layer 4 neurones within a single ‘barrel’ of developing rat somatosensory cortex. J. Physiol 521, 169–190. (doi:10.1111/j.1469-7793.199900169.x)
56. Lübke J, Egger V, Sakmann B, Feldmeyer D. 2000 Columnar organization of dendrites and axons of single and synaptically coupled excitatory spiny neurons in layer 4 of the rat barrel cortex J. Neurosci. 20, 5300–5311
57. Bruno RM, Sakmann B. 2006 Cortex is driven by weak but synchronously active thalamocortical synapses. Science 312, 1622–1627. (doi:10.1126/science.1124593)
58. Liu B, Wu GK, Arbuckle R, Tao HW, Zhang LI. 2007 Defining cortical frequency tuning with recurrent excitatory circuitry. Nat. Neurosci. 10, 1594–1600 (doi:10.1038/nn2012)
59. Douglas RJ, Koch C, Mahowald M, Martin KA, Suarez HH. 1995 Recurrent excitation in neocortical circuits. Science 269, 981–985. (doi:10.1126/science.7638624)
60. Brecht M, Grinevich V, Jin T-E, Margrie T, Osten P 2006 Cellular mechanisms of motor control in the vibrissal system. Pflüg. Arch. Eur. J. Physiol. 453, 269–281. (doi:10.1007/s00424-006-0101-6)
61. Berg RW, Kleinfeld D. 2003 Rhythmic whisking by rat: retraction as well as protraction of the vibrissae is under active muscular control. J. Neurophysiol. 89, 104–117. (doi:10.1152/jn.00600.2002)
62. Berg RW, Kleinfeld D. 2003 Vibrissa movement elicited by rhythmic electrical microstimulation to motor cortex in the aroused rat mimics exploratory whisking. J. Neurophysiol. 90, 2950–2963. (doi:10.1152/jn.00511.2003)
63. Dörfl J. 1982 The musculature of the mystacial vibrissae of the white mouse. J. Anat. 135, 147–154
64. Grinevich V, Brecht M, Osten P. 2005 Monosynaptic pathway from rat vibrissa motor cortex to facial motor neurons revealed by lentivirus-based axonal tracing. J. Neurosci. 25, 8250–8258. (doi:10.1523/JNEUROSCI.2235-05.2005)
65. Brecht M, Krauss A, Muhammad S, Sinai-Esfahani L, Bellanca S, Margrie TW. 2004 Organization of rat vibrissa motor cortex and adjacent areas according to cytoarchitectonics, microstimulation, and intracellular stimulation of identified cells J. Comp. Neurol. 479, 360–373. (doi:10.1002/cne.20306)
66. Herfst LJ, Brecht M. 2008 Whisker movements evoked by stimulation of single motor neurons in the facial nucleus of the rat. J. Neurophysiol. 99, 2821–2832. (doi:10.1152/jn.01014.2007)
67. Brecht M, Schneider M, Sakmann B, Margrie TW 2004 Whisker movements evoked by stimulation of single pyramidal cells in rat motor cortex. Nature 427, 704–710. (doi:10.1038/nature02266)
68. Ferrier D. 1874 On the localisation of the functions of the brain. Br. Med. J. 2, 766–767. (doi:10.1136/bmj.2.729.766)
69. Sherrington CS. 1906 Observations on the scratchreflex in the spinal dog. J. Physiol. 34, 1–50 (doi:10.1113/jphysiol.1906.sp001139)
70. Georgopoulos AP, Kalaska JF, Caminiti R, Massey JT 1982 On the relations between the direction of tworstbdimensional arm movements and cell discharge in primate motor cortex. J. Neurosci. 2, 1527–1537
71. Scott SH, Gribble PL, Graham KM, Cabel DW. 2001 Dissociation between hand motion and population vectors from neural activity in motor cortex. Nature 413, 161–165. (doi:10.1038/35093102)
72. Reina GA, Schwartz AB. 2003 Eye-hand coupling during closed-loop drawing: evidence of shared motor planning? Hum. Mov. Sci. 22, 137–152 (doi:10.1016/S0167-9457(02)00156-2)
73. Taylor DM, Tillery SIH, Schwartz AB. 2002 Direct cortical control of 3D neuroprosthetic devices. Science 296, 1829–1832. (doi:10.1126/science.1070291)
74. Nicolelis MAL. 2003 Brain-machine interfaces to restore motor function and probe neural circuits Nat. Rev. Neurosci. 4, 417–422. (doi:10.1038/nrn1105)
75. Velliste M, Perel S, Spalding MC, Whitford AS, Schwartz AB. 2008 Cortical control of a prosthetic arm for self-feeding. Nature 453, 1098–1101 (doi:10.1038/nature06996)
76. Chase SM, Schwartz AB. 2011 Inference from populations: going beyond models. Prog. Brain Res 192, 103–112. (doi:10.1016/B978-0-444-53355-500007-5)
77. Georgopoulos AP. 1995 Current issues in directional motor control. Trends Neurosci. 18, 506–510 (doi:10.1016/0166-2236(95)92775-L)
78. Schwartz AB, Moran DW. 2000 Arm trajectory and representation of movement processing in motor cortical activity. Eur. J. Neurosci. 12, 1851–1856 (doi:10.1046/j.1460-9568.2000.00097.x)
79. Chapin JK, Moxon KA, Markowitz RS, Nicolelis MA 1999 Real-time control of a robot arm using simultaneously recorded neurons in the motor cortex Nat. Neurosci. 2, 664–670. (doi:10.1038/10223)
80. Wessberg J et al. 2000 Real-time prediction of hand trajectory by ensembles of cortical neurons in primates. Nature 408, 361–365. (doi:10.1038/35042582)
81. Porter R, Lemon R. 1995 Corticospinal function and voluntary movement. Oxford, UK: Oxford University Press
82. Cheney PD, Fetz EE. 1980 Functional classes of primate corticomotoneuronal cells and their relation to active force. J. Neurophysiol. 44, 773–791
83. Woody CD, Black-Cleworth P. 1973 Differences in excitability of cortical neurons as a function of motor projection in conditioned cats J. Neurophysiol. 36, 1104–1116
84. Silberberg G, Markram H. 2007 Disynaptic inhibition between neocortical pyramidal cells mediated by Martinotti cells. Neuron 53, 735–746. (doi:10.1016/j.neuron.2007.02.012)
85. Reyes A, Lujan R, Rozov A, Burnashev N, Somogyi P, Sakmann B. 1998 Target-cell-specific facilitation and depression in neocortical circuits. Nat. Neurosci. 1, 279–285. (doi:10.1038/1092)
86. Kapfer C, Glickfeld LL, Atallah BV, Scanziani M. 2007 Supralinear increase of recurrent inhibition during sparse activity in the somatosensory cortex. Nat Neurosci. 10, 743–753. (doi:10.1038/nn1909)
87. Adesnik H, Bruns W, Taniguchi H, Huang ZJ, Scanziani M. 2012 A neural circuit for spatial summation in visual cortex. Nature 490, 226–231 (doi:10.1038/nature11526)
88. Kwan AC, Dan Y. 2012 Dissection of cortical microcircuits by single-neuron stimulation in vivo Curr. Biol. 22, 1459–1467. (doi:10.1016/j.cub.201206.007)
89. Li CY, Poo MM, Dan Y. 2009 Burst spiking of a single cortical neuron modifies global brain state. Science 324, 643–646. (doi:10.1126/science.1169957)
90. London M, Roth A, Beeren L, Häusser M, Latham PE 2010 Sensitivity to perturbations in vivo implies high noise and suggests rate coding in cortex. Nature 466, 123–127. (doi:10.1038/nature09086)
91. Butovas S, Schwarz C. 2003 Spatiotemporal effects of microstimulation in rat neocortex: a parametric study using multielectrode recordings. J. Neurophysiol. 90, 3024–3039. (doi:10.1152/jn.00245.2003)
92. Pfeffer CK, Xue M, He M, Huang ZJ, Scanziani M 2013 Inhibition of inhibition in visual cortex: the logic of connections between molecularly distinct interneurons. Nat. Neurosci. 16, 1068–1076 (doi:10.1038/nn.3446)
93. Bonifazi P, Goldin M, Picardo MA, Jorquera I, Cattani A, Bianconi G, Represa A, Ben-Ari Y, Cossart R. 2009 GABAergic hub neurons orchestrate synchrony in developing hippocampal networks. Science 326, 1419–1424. (doi:10.1126/science.1175509)
94. Ellender TJ, Nissen W, Colgin LL, Mann EO, Paulsen O. 2010 Priming of hippocampal population bursts by individual perisomatic-targeting interneurons J. Neurosci. 30, 5979–5991. (doi:10.1523/JNEUROSCI.3962-09.2010)
95. Kozloski J, Hamzei-Sichani F, Yuste R. 2001 Stereotyped position of local synaptic targets in neocortex. Science 293, 868–872. (doi:10.1126/science.293.5531.868)
96. Molnár G, Oláh S, Komlósi G, Füle M, Szabadics J, Varga C, Barzó P, Tamás G. 2008 Complex events initiated by individual spikes in the human cerebral cortex. PLoS Biol. 6, e222. (doi:10.1371/journal.pbio0060222)
97. Shadlen MN, Newsome WT. 1995 Is there a signal in the noise? Curr. Opin. Neurobiol. 5, 248–250 (doi:10.1016/0959-4388(95)80033-6)
98. Shadlen MN, Newsome WT. 1998 The variable discharge of cortical neurons: implications for connectivity, computation, and information coding J. Neurosci. 18, 3870–3896
99. Softky WR, Koch C. 1993 The highly irregular firing of cortical cells is inconsistent with temporal integration of random EPSPs. J. Neurosci. 13, 334–350
100. Golomb D, Kleinfeld D, Reid RC, Shapley RM, Shraiman BI. 1994 On temporal codes and the spatiotemporal response of neurons in the lateral geniculate nucleus. J. Neurophysiol. 72, 2990–3003
101. Adrian ED, Zotterman Y. 1926 The impulses produced by sensory nerve endings: part 3. Impulses set up by touch and pressure. J. Physiol 61, 465–483. (doi:10.1113/jphysiol.1926.sp002308)
102. Bair W, Koch C. 1996 Temporal precision of spike trains in extrastriate cortex of the behaving macaque monkey. Neural Comput. 8, 1185–1202 (doi:10.1162/neco.1996.8.6.1185)
103. Buracas GT, Zador AM, DeWeese MR, Albright TD 1998 Efficient discrimination of temporal patterns by motion-sensitive neurons in primate visual cortex. Neuron 20, 959–969. (doi:10.1016/S0896-6273(00)80477-8)
104. Histed MH, Maunsell JHR. 2014 Cortical neural populations can guide behavior by integrating inputs linearly, independent of synchrony. Proc. Natl Acad. Sci. USA 111, E178–E187. (doi:10.1073/pnas1318750111)
105. ƠConnor DH, Hires SA, Guo ZV, Li N, Yu J, Sun Q-Q, Huber D, Svoboda K. 2013 Neural coding during active somatosensation revealed using illusory touch. Nat. Neurosci. 16, 958–U238. (doi:10.1038/nn.3419)
106. Romo R, Hernández A, Zainos A, Brody C, Salinas E 2002 Exploring the cortical evidence of a sensorydiscrimination process. Phil. Trans. R. Soc. Lond. B 357, 1039–1051. (doi:10.1098/rstb.2002.1100)
107. Lak A, Arabzadeh E, Diamond ME. 2008 Enhanced response of neurons in rat somatosensory cortex to stimuli containing temporal noise. Cereb. Cortex 18, 1085–1093. (doi:10.1093/cercor/bhm144)
108. DeWeese MR, Hromádka T, Zador AM. 2005 Reliability and representational bandwidth in the auditory cortex. Neuron 48, 479–488. (doi:10.1016/j.neuron.2005.10.016)
109. Harris CM, Wolpert DM. 1998 Signal-dependent noise determines motor planning. Nature 394, 780–784. (doi:10.1038/29528)
110. Eccles SJC. 1973 Understanding of the brain New York, NY: McGraw-Hill
111. Stein RB, Gossen ER, Jones KE. 2005 Neuronal variability: noise or part of the signal? Nat. Rev Neurosci. 6, 389–397. (doi:10.1038/nrn1668)
112. Yizhar O, Fenno LE, Davidson TJ, Mogri M, Deisseroth K. 2011 Optogenetics in neural systems. Neuron 71, 9–34. (doi:10.1016/j.neuron.2011.06.004)
113. Asanuma H, Ward JE. 1971 Patterns of contraction of distal forelimb muscles produced by intracortical stimulation in cats. Brain Res. 27, 97–109. (doi:11016/0006-8993(71)90374-X)
114. Young NA, Vuong J, Flynn C, Teskey GC. 2011 Optimal parameters for microstimulation derived forelimb movement thresholds and motor maps in rats and mice. J. Neurosci. Methods 196, 60–69 (doi:10.1016/j.jneumeth.2010.12.028)
115. Van Acker GM, Amundsen SL, Messamore WG, Zhang HY, Luchies CW, Kovac A, Cheney PD. 2013 Effective intracortical microstimulation parameters applied to primary motor cortex for evoking forelimb movements to stable spatial end points. J. Neurophysiol. 110, 1180–1189. (doi:10.1152/jn.00172.2012)
116. Graziano MSA, Aflalo TNS, Cooke DF. 2005 Arm movements evoked by electrical stimulation in the motor cortex of monkeys. J. Neurophysiol. 94, 4209–4223. (doi:10.1152/jn.01303.2004)
117. Ethier C, Brizzi L, Darling WG, Capaday C. 2006 Linear summation of cat motor cortex outputs J. Neurosci. 26, 5574–5581. (doi:10.1523/JNEUROSCI.5332-05.2006)
118. Graziano M. 2006 The organization of behavioral repertoire in motor cortex. Annu. Rev. Neurosci. 29, 105–134. (doi:10.1146/annurev.neuro.29.051605112924)
119. Haiss F, Schwarz C. 2005 Spatial segregation of different modes of movement control in the whisker representation of rat primary motor cortex J. Neurosci. 25, 1579–1587. (doi:10.1523/JNEUROSCI.3760-04.2005)
120. Stepniewska I, Fang P-C, Kaas JH. 2005 Microstimulation reveals specialized subregions for different complex movements in posterior parietal cortex of prosimian galagos. Proc. Natl Acad. Sci USA 102, 4878–4883. (doi:10.1073/pnas0501048102)
121. Ramanathan D, Conner JM, Tuszynski MH. 2006 A form of motor cortical plasticity that correlates with recovery of function after brain injury. Proc. Natl Acad. Sci. USA 103, 11 370–11 375. (doi:10.1073/pnas.0601065103)
122. Harrison TC, Ayling OGS, Murphy TH. 2012 Distinct cortical circuit mechanisms for complex forelimb movement and motor map topography. Neuron 74, 397–409. (doi:10.1016/j.neuron.2012.02.028)
123. Dai J, Brooks DI, Sheinberg DL. 2014 Optogenetic and electrical microstimulation systematically bias visuospatial choice in primates. Curr. Biol. 24, 63–69. (doi:10.1016/j.cub.2013.11.011)
124. Packer AM, Russell LE, Dalgleish HWP, Hüsser M 2015 Simultaneous all-optical manipulation and recording of neural circuit activity with cellular resolution in vivo. Nat. Methods 12, 140–146 (doi:10.1038/nmeth.3217)
125. Szabo V, Ventalon C, De Sars V, Bradley J, Emiliani V. 2014 Spatially selective holographic photoactivation and functional fluorescence imaging in freely behaving mice with a fiberscope Neuron 84, 1157–1169. (doi:10.1016/j.neuron2014.11.005)