Low-noise encoding of active touch by layer 4 in the somatosensory cortex

eLife

Volumn 4, Issue AUGUST2015, 2015, Pages

  Hires, Samuel Andrew ^a,b   Gutnisky, Diego A ^a   Yu, Jianing ^a   O’Connor, Daniel H ^a,c   Svoboda, Karel ^a  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTION POTENTIAL; ANIMAL TISSUE; ARTICLE; BEHAVIOR; CORTICAL SPIKE TRAIN; ELECTROPHYSIOLOGY; EYE MOVEMENT; HISTOLOGY; LEARNING TEST; MEDICAL PHOTOGRAPHY; MOUSE; NERVE CELL; NEUROMUSCULAR FUNCTION; NONHUMAN; SENSORY STIMULATION; SOMATOSENSORY CORTEX; SPIKE WAVE; TOUCH; TRAINING; VIBRISSA; VISUAL CORTEX; ANIMAL; LOCOMOTION; PHYSIOLOGY; SENSORIMOTOR CORTEX;

ACTION POTENTIALS; ANIMALS; LOCOMOTION; MICE; SENSORIMOTOR CORTEX; SOMATOSENSORY CORTEX; TOUCH;

EID: 84941312995     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.06619     Document Type: Article

References (72)

1. AdibiM, Clifford CW, Arabzadeh E. 2013. Informational basis of sensory adaptation: entropy and single-spike efficiency in rat barrel cortex. The Journal of Neuroscience 33:14921-14926. doi: 10.1523/JNEUROSCI.1313-13.2013.
2. Amarasingham A, Chen TL, Geman S, Harrison MT, Sheinberg DL. 2006. Spike count reliability and the Poisson hypothesis. The Journal of Neuroscience 26:801-809. doi: 10.1523/JNEUROSCI.2948-05.2006.
3. Ankerst M, Breunig MM, Kriegel HP, Sander J. 1999. OPTICS: Ordering points to identify the clustering structure. Sigmod Record 28:49-60. doi: 10.1145/304181.304187.
4. Bair W, Koch C. 1996. Temporal precision of spike trains in extrastriate cortex of the behaving macaque monkey. Neural Computation 8:1185-1202. doi: 10.1162/neco.1996.8.6.1185.
5. Bale MR, Davies K, Freeman OJ, Ince RA, Petersen RS. 2013. Low-dimensional sensory feature representation by trigeminal primary afferents. The Journal of Neuroscience 33:12003-12012. doi: 10.1523/JNEUROSCI. 0925-13.2013.
6. Baudot P, Levy M, Marre O, Monier C, Pananceau M, Fré gnac Y. 2013. Animation of natural scene by virtual eye-movements evokes high precision and low noise in V1 neurons. Frontiers in Neural Circuits 7:206. doi: 10. 3389/fncir.2013.00206.
7. Berry MJ II, Meister M. 1998. Refractoriness and neural precision. The Journal of Neuroscience 18:2200-2211.
8. Berry MJ, Warland DK, Meister M. 1997. The structure and precision of retinal spike trains. Proceedings of the National Academy of Sciences of USA 94:5411-5416. doi: 10.1073/pnas.94.10.5411.
9. Birdwell JA, Solomon JH, Thajchayapong M, Taylor MA, Cheely M, Towal RB, Conradt J, Hartmann MJ. 2007. Biomechanical models for radial distance determination by the rat vibrissal system. Journal of Neurophysiology 98:2439-2455. doi: 10.1152/jn.00707.2006.
10. Bruno RM, Sakmann B. 2006. Cortex is driven by weak but synchronously active thalamocortical synapses. Science 312:1622-1627. doi: 10.1126/science.1124593.
11. 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.
12. Bureau I, von Saint Paul F, Svoboda K. 2006. Interdigitated Paralemniscal and Lemniscal Pathways in the mouse barrel cortex. PLOS Biology 4:e382. doi: 10.1371/journal.pbio.0040382.
13. Churchland MM, Yu BM, Cunningham JP, Sugrue LP, Cohen MR, Corrado GS, Newsome WT, Clark AM, Hosseini P, Scott BB, Bradley DC, Smith MA, Kohn A, Movshon JA, Armstrong KM, Moore T, Chang SW, Snyder LH, Lisberger SG, Priebe NJ, Finn IM, Ferster D, Ryu SI, Santhanam G, Sahani M, Shenoy KV. 2010. Stimulus onset quenches neural variability: a widespread cortical phenomenon. Nature Neuroscience 13:369-378. doi: 10.1038/nn.2501.
14. Clack NG, O'Connor DH, Huber D, Petreanu L, Hires A, Peron S, Svoboda K, Myers EW. 2012. Automated tracking of whiskers in videos of head fixed rodents. PLOS Computational Biology 8:e1002591. doi: 10.1371/journal.pcbi. 1002591.
15. Cotton RJ, Froudarakis E, Storer P, Saggau P, Tolias AS. 2013. Three-dimensional mapping of microcircuit correlation structure. Frontiers in Neural Circuits 7:151. doi: 10.3389/fncir.2013.00151.
16. Crochet S, Petersen CC. 2006. Correlating whisker behavior with membrane potential in barrel cortex of awake mice. Nature Neuroscience 9:608-610. doi: 10.1038/nn1690.
17. Cunningham JP, Yu BM. 2014. Dimensionality reduction for large-scale neural recordings. Nature Neuroscience 17:1500-1509. doi: 10.1038/nn.3776.
18. Curtis JC, Kleinfeld D. 2009. Phase-to-rate transformations encode touch in cortical neurons of a scanning sensorimotor system. Nature Neuroscience 12:492-501. doi: 10.1038/nn.2283.
19. Dayan P, Abbott LF. 2001. Theoretical neuroscience: computational and mathematical modeling of neural systems: MIT Press.
20. Deschenes M, Moore J, Kleinfeld D. 2012. Sniffing and whisking in rodents. Current Opinion in Neurobiology 22:243-250. doi: 10.1016/j.conb.2011.11.013.
21. DeWeese MR, Wehr M, Zador AM. 2003. Binary spiking in auditory cortex. The Journal of Neuroscience 23:7940-7949.
22. Diamond ME, von Heimendahl M, Knutsen PM, Kleinfeld D, Ahissar E. 2008. 'Where' and 'what' in the whisker sensorimotor system. Nature Reviews. Neuroscience 9:601-612. doi: 10.1038/nrn2411.
23. Duda RO, Hart PE, Stork DG. 2001. Pattern classification, Edn. 2nd. Wiley, New York.
24. Ester M, Kriegel HP, Sander J, Xu X. 1996. A density-based algorithm for discovering clusters in large spatial databases with noise. in Proceedings of the Second International Conference on Knowledge Discovery and Data Mining (KDD'96). Association for the Advancement of Artificial Intelligence. p. 226-231.
25. Fee MS, Mitra PP, Kleinfeld D. 1997. Central versus peripheral determinants of patterned spike activity in rat vibrissa cortex during whisking. Journal of Neurophysiology 78:1144-1149.
26. Gabernet L, Jadhav SP, Feldman DE, Carandini M, Scanziani M. 2005. Somatosensory integration controlled by dynamic thalamocortical feed-forward inhibition. Neuron 48:315-327. doi: 10.1016/j.neuron.2005.09.022.
27. Gollisch T, Meister M. 2008. Rapid neural coding in the retina with relative spike latencies. Science 319:1108-1111. doi: 10.1126/science.1149639.
28. Gomez C, Smolyanskaya C, Kreiman G, Born RT. 2013. Silencing V2/V3 reduces spiking variability in MT: implications for excitatory/inhibitory balance CoSyNe Meeting.
29. Guo ZV, Hires SA, Li N, O'Connor DH, Komiyama T, Ophir E, Huber D, Bonardi C, Morandell K, Gutnisky D, Peron S, Xu NL, Cox J, Svoboda K. 2014. Procedures for behavioral experiments in head-fixed mice. PLOS ONE 9:e88678. doi: 10.1371/journal.pone.0088678.
30. Guo ZV, Li N, Huber D, Ophir E, Gutnisky D, Ting JT, Feng G, Svoboda K. 2014. Flow of cortical activity underlying a tactile decision in mice. Neuron 81:179-194. doi: 10.1016/j.neuron.2013.10.020.
31. Gur M, Beylin A, Snodderly DM. 1997. Response variability of neurons in primary visual cortex (V1) of alert monkeys. The Journal of Neuroscience 17:2914-2920.
32. Hill DN, Curtis JC, Moore JD, Kleinfeld D. 2011. Primary motor cortex reports efferent control of vibrissa motion on multiple timescales. Neuron 72:344-356. doi: 10.1016/j.neuron.2011.09.020.
33. Hippenmeyer S, Vrieseling E, Sigrist M, Portmann T, Laengle C, Ladle DR, Arber S. 2005. A developmental switch in the response of DRG neurons to ETS transcription factor signaling. PLOS Biology 3:e159. doi: 10.1371/journal. pbio.0030159.
34. Hooks BM, Hires SA, Zhang YX, Huber D, Petreanu L, Svoboda K, Shepherd GM. 2011. Laminar analysis of excitatory local circuits in vibrissal motor and sensory cortical areas. PLOS Biology 9:e1000572. doi: 10.1371/ journal.pbio.1000572.
35. Hutson KA, Masterton RB. 1986. The sensory contribution of a single vibrissa's cortical barrel. Journal of Neurophysiology 56:1196-1223.
36. Jadhav SP, Wolfe J, Feldman DE. 2009. Sparse temporal coding of elementary tactile features during active whisker sensation. Nature Neuroscience 12:792-800. doi: 10.1038/nn.2328.
37. Johansson RS, Birznieks I. 2004. First spikes in ensembles of human tactile afferents code complex spatial fingertip events. Nature Neuroscience 7:170-177. doi: 10.1038/nn1177.
38. Kara P, Reinagel P, Reid RC. 2000. Low response variability in simultaneously recorded retinal, thalamic, and cortical neurons. Neuron 27:635-646. doi: 10.1016/S0896-6273(00)00072-6.
39. Keat J, Reinagel P, Reid RC, Meister M. 2001. Predicting every spike: a model for the responses of visual neurons. Neuron 30:803-817. doi: 10.1016/S0896-6273(01)00322-1.
40. Kleinfeld D, Deschenes M. 2011. Neuronal basis for object location in the vibrissa scanning sensorimotor system. Neuron 72:455-468. doi: 10.1016/j.neuron.2011.10.009.
41. Knutsen PM, Pietr M, Ahissar E. 2006. Haptic object localization in the vibrissal system: behavior and performance. The Journal of Neuroscience 26:8451-8464. doi: 10.1523/JNEUROSCI.1516-06.2006.
42. Land PW, Simons DJ. 1985. Cytochrome oxidase staining in the rat SmI barrel cortex. The Journal of Comparative Neurology 238:225-235. doi: 10.1002/cne.902380209.
43. Lefort S, Tomm C, Floyd Sarria JC, Petersen CC. 2009. The excitatory neuronal network of the C2 barrel column in mouse primary somatosensory cortex. Neuron 61:301-316. doi: 10.1016/j.neuron.2008.12.020.
44. Lewicki MS. 1998. A review of methods for spike sorting: the detection and classification of neural action potentials. Network 9:R53-R78. doi: 10.1088/0954-898X/9/4/001.
45. Litwin-Kumar A, Doiron B. 2012. Slow dynamics and high variability in balanced cortical networks with clustered connections. Nature Neuroscience 15:1498-1505. doi: 10.1038/nn.3220.
46. London M, Roth A, Beeren L, Hausser 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.
47. Lu SM, Lin RCS. 1993. Thalamic afferents of the rat barrel cortex: a light-and electron-microscopic study using Phaseolus vulgaris leucoagglutinin as an anterograde tracer. Somatosensory & Motor Research 10:1-16. doi: 10. 3109/08990229309028819.
48. Madisen L, Mao T, Koch H, Zhuo JM, Berenyi A, Fujisawa S, Hsu YW, Garcia AJ III, Gu X, Zanella S, Kidney J, Gu H, Mao Y, Hooks BM, Boyden ES, Buzsáki G, Ramirez JM, Jones AR, Svoboda K, Han X, Turner EE, Zeng H. 2012. A toolbox of Cre-dependent optogenetic transgenic mice for light-induced activation and silencing. Nature Neuroscience 15:793-802. doi: 10.1038/nn.3078.
49. Maimon G, Assad JA. 2009. Beyond Poisson: increased spike-time regularity across primate parietal cortex. Neuron 62:426-440. doi: 10.1016/j.neuron.2009.03.021.
50. Mainen ZF, Sejnowski TJ. 1995. Reliability of spike timing in neocortical neurons. Science 268:1503-1506. doi: 10. 1126/science.7770778.
51. Masquelier T. 2013. Neural variability, or lack thereof. Frontiers in Computational Neuroscience 7:7. doi: 10.3389/ fncom.2013.00007.
52. Mazurek ME, Shadlen MN. 2002. Limits to the temporal fidelity of cortical spike rate signals. Nature Neuroscience 5:463-471. doi: 10.1038/nn836.
53. Mitchell JF, Sundberg KA, Reynolds JH. 2007. Differential attention-dependent response modulation across cell classes in macaque visual area V4. Neuron 55:131-141. doi: 10.1016/j.neuron.2007.06.018.
54. Mitchell JF, Sundberg KA, Reynolds JH. 2009. Spatial attention decorrelates intrinsic activity fluctuations in macaque area V4. Neuron 63:879-888. doi: 10.1016/j.neuron.2009.09.013.
55. Moreno-Bote R, Beck J, Kanitscheider I, Pitkow X, Latham P, Pouget A. 2014. Information-limiting correlations. Nature Neuroscience 17:1410-1417. doi: 10.1038/nn.3807.
56. O'Connor DH, Clack NG, Huber D, Komiyama T, Myers EW, Svoboda K. 2010a. Vibrissa-based object localization in head-fixed mice. The Journal of Neuroscience 30:1947-1967. doi: 10.1523/JNEUROSCI.3762-09.2010.
57. O'Connor DH, Hires SA, Guo ZV, Li N, Yu J, Sun QQ, Huber D, Svoboda K. 2013. Neural coding during active somatosensation revealed using illusory touch. Nature Neuroscience 16:958-965. doi: 10.1038/nn.3419.
58. O'Connor DH, Peron SP, Huber D, Svoboda K. 2010b. Neural activity in barrel cortex underlying vibrissa-based object localization in mice. Neuron 67:1048-1061. doi: 10.1016/j.neuron.2010.08.026.
59. Pammer L, O'Connor DH, Hires SA, Clack NG, Huber D, Myers EW, Svoboda K. 2013. The mechanical variables underlying object localization along the axis of the whisker. The Journal of Neuroscience 33:6726-6741. doi: 10. 1523/JNEUROSCI.4316-12.2013.
60. Panzeri S, Ince RA, Diamond ME, Kayser C. 2014. Reading spike timing without a clock: intrinsic decoding of spike trains. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 369:20120467. doi: 10.1098/rstb.2012.0467.
61. Petreanu L, Mao T, Sternson SM, Svoboda K. 2009. The subcellular organization of neocortical excitatory connections. Nature 457:1142-1145. doi: 10.1038/nature07709.
62. Renart A, Machens CK. 2014. Variability in neural activity and behavior. Current Opinion in Neurobiology 25: 211-220. doi: 10.1016/j.conb.2014.02.013.
63. Shadlen MN, Newsome WT. 1998. The variable discharge of cortical neurons: implications for connectivity, computation, and information coding. The Journal of Neuroscience 18:3870-3896.
64. Simons DJ. 1978. Response properties of vibrissa units in rat SI somatosensory neocortex. Journal of Neurophysiology 41:798-820.
65. Softky WR, Koch C. 1993. The highly irregular firing of cortical cells is inconsistent with temporal integration of random EPSPs. The Journal of Neuroscience 13:334-350.
66. Stevens CF, Zador AM. 1998. Input synchrony and the irregular firing of cortical neurons. Nature Neuroscience 1:210-217. doi: 10.1038/659.
67. Suter BA, O'Connor T, Iyer V, Petreanu LT, Hooks BM, Kiritani T, Svoboda K, Shepherd GM. 2010. Ephus: multipurpose data acquisition software for neuroscience experiments. Frontiers Neuroscience 4. doi: 10.3389/ fncir.2010.00100.
68. Tolhurst DJ, Movshon JA, Dean AF. 1983. The statistical reliability of signals in single neurons in cat and monkey visual cortex. Vision Research 23:775-785. doi: 10.1016/0042-6989(83)90200-6.
69. van Vreeswijk C, Sompolinsky H. 1996. Chaos in neuronal networks with balanced excitatory and inhibitory activity. Science 274:1724-1726. doi: 10.1126/science.274.5293.1724.
70. VanRullen R, Guyonneau R, Thorpe SJ. 2005. Spike times make sense. Trends in Neurosciences 28:1-4. doi: 10. 1016/j.tins.2004.10.010.
71. Wang Q, Webber RM, Stanley GB. 2010. Thalamic synchrony and the adaptive gating of information flow to cortex. Nature Neuroscience 13:1534-1541. doi: 10.1038/nn.2670.
72. Zhao S, Ting JT, Atallah HE, Qiu L, Tan J, Gloss B, Augustine GJ, Deisseroth K, Luo M, Graybiel AM, Feng G. 2011. Cell type-specific channelrhodopsin-2 transgenic mice for optogenetic dissection of neural circuitry function. Nature Methods 8:745-752. doi: 10.1038/nmeth.1668.