Long-range population dynamics of anatomically defined neocortical networks

eLife

Volumn 5, Issue MAY2016, 2016, Pages

  Chen, Jerry L ^a,b   Voigt, Fabian F ^a   Javadzadeh, Mitra ^a   Krueppel, Roland ^a,c   Helmchen, Fritjof ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b Boston University   (United States)

^c Federal Ministry of Agriculture   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ANIMAL EXPERIMENT; ARTICLE; BEHAVIORAL SCIENCE; FLUORESCENCE MICROSCOPY; LOCOMOTION; MATHEMATICAL MODEL; MOTOR COORDINATION; MOUSE; NERVE CELL NETWORK; NEUROIMAGING; NONHUMAN; POPULATION DYNAMICS; SOMATOSENSORY CORTEX; ANIMAL; C57BL MOUSE; EXPLORATORY BEHAVIOR; MALE; METABOLISM; MOLECULAR IMAGING; MOTOR ACTIVITY; MULTIPHOTON MICROSCOPY; NERVE CELL; NERVE TRACT; PHYSIOLOGY; SMELLING; SYNAPTIC TRANSMISSION; TRANSGENIC MOUSE; ULTRASTRUCTURE;

CALCIUM;

ANIMALS; CALCIUM; EXPLORATORY BEHAVIOR; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROSCOPY, FLUORESCENCE, MULTIPHOTON; MOLECULAR IMAGING; MOTOR ACTIVITY; NEURAL PATHWAYS; NEURONS; OLFACTORY PERCEPTION; SOMATOSENSORY CORTEX; SYNAPTIC TRANSMISSION;

EID: 84975215472     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.14679     Document Type: Article

References (67)

1. Akemann W, Sasaki M, Mutoh H, Imamura T, Honkura N, Knöpfel T. 2013. Two-photon voltage imaging using a genetically encoded voltage indicator. Scientific Reports 3. doi: 10.1038/srep02231
2. Akerboom J, Carreras Calderón N, Tian L, Wabnig S, Prigge M, TolöJ, Gordus A, Orger MB, Severi KE, Macklin JJ, Patel R, Pulver SR, Wardill TJ, Fischer E, Schüler C, Chen TW, Sarkisyan KS, Marvin JS, Bargmann CI, Kim DS, et al. 2013. Genetically encoded calcium indicators for multi-color neural activity imaging and combination with optogenetics. Frontiers in Molecular Neuroscience 6. doi: 10.3389/fnmol.2013.00002
3. Aronoff R, Matyas F, Mateo C, Ciron C, Schneider B, Petersen CC. 2010. Long-range connectivity of mouse primary somatosensory barrel cortex. The European Journal of Neuroscience 31:2221-2233. doi: 10.1111/j. 1460-9568.2010.07264.x
4. Bathellier B, Ushakova L, Rumpel S. 2012. Discrete neocortical dynamics predict behavioral categorization of sounds. Neuron 76:435-449. doi: 10.1016/j.neuron.2012.07.008
5. Bosman LW, Houweling AR, Owens CB, Tanke N, Shevchouk OT, Rahmati N, Teunissen WH, Ju C, Gong W, Koekkoek SK, De Zeeuw CI. 2011. Anatomical pathways involved in generating and sensing rhythmic whisker movements. Frontiers in Integrative Neuroscience 5. doi: 10.3389/fnint.2011.00053
6. 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
7. Bressler SL, Menon V. 2010. Large-scale brain networks in cognition: emerging methods and principles. Trends in Cognitive Sciences 14:277-290. doi: 10.1016/j.tics.2010.04.004
8. Buschman TJ, Miller EK. 2007. Top-down versus bottom-up control of attention in the prefrontal and posterior parietal cortices. Science 315:1860-1862. doi: 10.1126/science.1138071
9. Cai D, Cohen KB, Luo T, Lichtman JW, Sanes JR. 2013. Improved tools for the Brainbow toolbox. Nature Methods 10:540-547. doi: 10.1038/nmeth.2450
10. Chen JL, Andermann ML, Keck T, Xu NL, Ziv Y. 2013a. Imaging neuronal populations in behaving rodents:paradigms for studying neural circuits underlying behavior in the mammalian cortex. The Journal of Neuroscience 33:17631-17640. doi: 10.1523/JNEUROSCI.3255-13.2013
11. Chen JL, Carta S, Soldado-Magraner J, Schneider BL, Helmchen F. 2013b. Behaviour-dependent recruitment of long-range projection neurons in somatosensory cortex. Nature 499:336-340. doi: 10.1038/nature12236
12. Chen JL, Margolis DJ, Stankov A, Sumanovski LT, Schneider BL, Helmchen F. 2015. Pathway-specific reorganization of projection neurons in somatosensory cortex during learning. Nature Neuroscience 18:1101-1108. doi: 10.1038/nn.4046
13. Cheng A, Gonçalves JT, Golshani P, Arisaka K, Portera-Cailliau C. 2011. Simultaneous two-photon calcium imaging at different depths with spatiotemporal multiplexing. Nature Methods 8:139-142. doi: 10.1038/nmeth. 1552
14. Cong F, Lin QH, Kuang LD, Gong XF, Astikainen P, Ristaniemi T. 2015. Tensor decomposition of EEG signals: a brief review. Journal of Neuroscience Methods 248:59-69. doi: 10.1016/j.jneumeth.2015.03.018
15. Deschênes M, Veinante P, Zhang ZW. 1998. The organization of corticothalamic projections: reciprocity versus parity. Brain Research. Brain Research Reviews 28:286-308. doi: 10.1016/S0165-0173(98)00017-4
16. 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
17. Fenno LE, Mattis J, Ramakrishnan C, Hyun M, Lee SY, He M, Tucciarone J, Selimbeyoglu A, Berndt A, Grosenick L, Zalocusky KA, Bernstein H, Swanson H, Perry C, Diester I, Boyce FM, Bass CE, Neve R, Huang ZJ, Deisseroth K. 2014. Targeting cells with single vectors using multiple-feature Boolean logic. Nature Methods 11:763-772. doi: 10.1038/nmeth.2996
18. Fisher RA. 1936. The Use of Multiple Measurements in Taxonomic Problems. Annals of Eugenics 7:179-188. doi:10.1111/j.1469-1809.1936.tb02137.x
19. Gilbert CD, Li W. 2013. Top-down influences on visual processing. Nature Reviews. Neuroscience 14:350-363. doi: 10.1038/nrn3476
20. Glickfeld LL, Andermann ML, Bonin V, Reid RC. 2013. Cortico-cortical projections in mouse visual cortex are functionally target specific. Nature Neuroscience 16:219-226. doi: 10.1038/nn.3300
21. Green DM, Swets JA. 1966. Signal Detection Theory and Psychophysics. New York: Wiley and Sons.
22. Grewe BF, Langer D, Kasper H, Kampa BM, Helmchen F. 2010. High-speed in vivo calcium imaging reveals neuronal network activity with near-millisecond precision. Nature Methods 7:399-405. doi: 10.1038/nmeth. 1453
23. Grewe BF, Voigt FF, van ‘t Hoff M, Helmchen F. 2011. Fast two-layer two-photon imaging of neuronal cell populations using an electrically tunable lens. Biomedical Optics Express 2:2035-2046. doi: 10.1364/BOE.2. 002035
24. Ferezou I, Haiss F, Gentet LJ, Aronoff R, Weber B, Petersen CC. 2007. Spatiotemporal dynamics of cortical sensorimotor integration in behaving mice. Neuron 56:907-923. doi: 10.1016/j.neuron.2007.10.007
25. Hitchcock FL. 1927. The Expression of a Tensor or a Polyadic as a Sum of Products. Journal of Mathematics and Physics 6:164-189. doi: 10.1002/sapm192761164
26. Horikawa K, Yamada Y, Matsuda T, Kobayashi K, Hashimoto M, Matsu-ura T, Miyawaki A, Michikawa T, Mikoshiba K, Nagai T. 2010. Spontaneous network activity visualized by ultrasensitive Ca(2+) indicators, yellow Cameleon-Nano. Nature Methods 7:729-732. doi: 10.1038/nmeth.1488
27. Huber D, Gutnisky DA, Peron S, O’Connor DH, Wiegert JS, Tian L, Oertner TG, Looger LL, Svoboda K. 2012. Multiple dynamic representations in the motor cortex during sensorimotor learning. Nature 484:473-478. doi:10.1038/nature11039
28. Hutchison RM, Womelsdorf T, Allen EA, Bandettini PA, Calhoun VD, Corbetta M, Della Penna S, Duyn JH, Glover GH, Gonzalez-Castillo J, Handwerker DA, Keilholz S, Kiviniemi V, Leopold DA, de Pasquale F, Sporns O, Walter M, Chang C. 2013. Dynamic functional connectivity: promise, issues, and interpretations. NeuroImage 80:360-378. doi: 10.1016/j.neuroimage.2013.05.079
29. Jarosiewicz B, Schummers J, Malik WQ, Brown EN, Sur M. 2012. Functional biases in visual cortex neurons with identified projections to higher cortical targets. Current Biology 22:269-277. doi: 10.1016/j.cub.2012.01.011
30. Kleinfeld D, Deschênes 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
31. Knutsen PM, Derdikman D, Ahissar E. 2005. Tracking whisker and head movements in unrestrained behaving rodents. Journal of Neurophysiology 93:2294-2301. doi: 10.1152/jn.00718.2004
32. Komiyama T, Sato TR, O’Connor DH, Zhang YX, Huber D, Hooks BM, Gabitto M, Svoboda K. 2010. Learning-related fine-scale specificity imaged in motor cortex circuits of behaving mice. Nature 464:1182-1186. doi: 10. 1038/nature08897
33. Lecoq J, Savall J, Vučinić D, Grewe BF, Kim H, Li JZ, Kitch LJ, Schnitzer MJ, Vucinic D. 2014. Visualizing mammalian brain area interactions by dual-axis two-photon calcium imaging. Nature Neuroscience 17:1825-1829. doi: 10.1038/nn.3867
34. Lim DH, Ledue J, Mohajerani MH, Vanni MP, Murphy TH. 2013. Optogenetic approaches for functional mouse brain mapping. Frontiers in Neuroscience 7. doi: 10.3389/fnins.2013.00054
35. Lütcke H, Gerhard F, Zenke F, Gerstner W, Helmchen F. 2013. Inference of neuronal network spike dynamics and topology from calcium imaging data. Frontiers in Neural Circuits 7. doi: 10.3389/fncir.2013.00201
36. Madisen L, Garner AR, Shimaoka D, Chuong AS, Klapoetke NC, Li L, van der Bourg A, Niino Y, Egolf L, Monetti C, Gu H, Mills M, Cheng A, Tasic B, Nguyen TN, Sunkin SM, Benucci A, Nagy A, Miyawaki A, Helmchen F, et al. 2015. Transgenic mice for intersectional targeting of neural sensors and effectors with high specificity and performance. Neuron 85:942-958. doi: 10.1016/j.neuron.2015.02.022
37. Markov NT, Ercsey-Ravasz M, Van Essen DC, Knoblauch K, Toroczkai Z, Kennedy H. 2013. Cortical high-density counterstream architectures. Science 342. doi: 10.1126/science.1238406
38. Matsuda T, Cepko CL. 2007. Controlled expression of transgenes introduced by in vivo electroporation. Proceedings of the National Academy of Sciences of the United States of America 104:1027-1032. doi: 10. 1073/pnas.0610155104
39. Melzer P, Champney GC, Maguire MJ, Ebner FF. 2006. Rate code and temporal code for frequency of whisker stimulation in rat primary and secondary somatic sensory cortex. Experimental Brain Research 172:370-386. doi: 10.1007/s00221-005-0334-1
40. Minderer M, Liu W, Sumanovski LT, Kügler S, Helmchen F, Margolis DJ. 2012. Chronic imaging of cortical sensory map dynamics using a genetically encoded calcium indicator. The Journal of Physiology 590:99-107. doi: 10.1113/jphysiol.2011.219014
41. Miri A, Daie K, Burdine RD, Aksay E, Tank DW. 2011. Regression-based identification of behavior-encoding neurons during large-scale optical imaging of neural activity at cellular resolution. Journal of Neurophysiology 105:964-980. doi: 10.1152/jn.00702.2010
42. Moore JD, Mercer Lindsay N, Deschênes M, Kleinfeld D. 2015. Vibrissa Self-Motion and Touch Are Reliably Encoded along the Same Somatosensory Pathway from Brainstem through Thalamus. PLoS Biology 13:e1002253. doi: 10.1371/journal.pbio.1002253
43. Musall S, von der Behrens W, Mayrhofer JM, Weber B, Helmchen F, Haiss F. 2014. Tactile frequency discrimination is enhanced by circumventing neocortical adaptation. Nature Neuroscience 17:1567-1573. doi:10.1038/nn.3821
44. O’Connor DH, Peron SP, Huber D, Svoboda K. 2010. Neural activity in barrel cortex underlying vibrissa-based object localization in mice. Neuron 67:1048-1061. doi: 10.1016/j.neuron.2010.08.026
45. Oh SW, Harris JA, Ng L, Winslow B, Cain N, Mihalas S, Wang Q, Lau C, Kuan L, Henry AM, Mortrud MT, Ouellette B, Nguyen TN, Sorensen SA, Slaughterbeck CR, Wakeman W, Li Y, Feng D, Ho A, Nicholas E, et al. 2014. A mesoscale connectome of the mouse brain. Nature 508:207-214. doi: 10.1038/nature13186
46. Pais-Vieira M, Lebedev MA, Wiest MC, Nicolelis MA. 2013. Simultaneous top-down modulation of the primary somatosensory cortex and thalamic nuclei during active tactile discrimination. Journal of Neuroscience 33:4076-4093. doi: 10.1523/JNEUROSCI.1659-12.2013
47. Petreanu L, Gutnisky DA, Huber D, Xu NL, O’Connor DH, Tian L, Looger L, Svoboda K. 2012. Activity in motor-sensory projections reveals distributed coding in somatosensation. Nature 489:299-303. doi: 10.1038/nature11321
48. Piatkevich KD, Hulit J, Subach OM, Wu B, Abdulla A, Segall JE, Verkhusha VV. 2010. Monomeric red fluorescent proteins with a large Stokes shift. Proceedings of the National Academy of Sciences of the United States of America 107:5369-5374. doi: 10.1073/pnas.0914365107
49. Pierret T, Lavallée P, Deschênes M. 2000. Parallel streams for the relay of vibrissal information through thalamic barreloids. Journal of Neuroscience 20:7455-7462.
50. Pinto L, Dan Y. 2015. Cell-Type-Specific Activity in Prefrontal Cortex during Goal-Directed Behavior. Neuron 87:437-450. doi: 10.1016/j.neuron.2015.06.021
51. Quirin S, Jackson J, Peterka DS, Yuste R. 2014. Simultaneous imaging of neural activity in three dimensions. Frontiers in Neural Circuits 8. doi: 10.3389/fncir.2014.00029
52. Saalmann YB, Pinsk MA, Wang L, Li X, Kastner S. 2012. The pulvinar regulates information transmission between cortical areas based on attention demands. Science 337:753-756. doi: 10.1126/science.1223082
53. Safaai H, von Heimendahl M, Sorando JM, Diamond ME, Maravall M. 2013. Coordinated population activity underlying texture discrimination in rat barrel cortex. Journal of Neuroscience 33:5843-5855. doi: 10.1523/JNEUROSCI.3486-12.2013
54. Salinas E, Sejnowski TJ. 2001. Correlated neuronal activity and the flow of neural information. Nature Reviews. Neuroscience 2:539-550. doi: 10.1038/35086012
55. Sato TR, Svoboda K. 2010. The functional properties of barrel cortex neurons projecting to the primary motor cortex. Journal of Neuroscience 30:4256-4260. doi: 10.1523/JNEUROSCI.3774-09.2010
56. Seely JS, Cunningham JP, Lara H, Churchland MM. 2014. Should one collect more trials, more neurons, or more conditions: a statistical solution to the experimentalist’s dilemma. Society for Neuroscience Abstracts:188.125/UU185.
57. Sherman SM, Guillery RW. 2011. Distinct functions for direct and transthalamic corticocortical connections. Journal of Neurophysiology 106:1068-1077. doi: 10.1152/jn.00429.2011
58. Stirman JN, Smith IT, Kudenov MW, Smith SL. 2014. Wide field-of-view, twin-region two-photon imaging across extended cortical networks. bioRxiv. doi: 10.1101/011320
59. Sun XR, Badura A, Pacheco DA, Lynch LA, Schneider ER, Taylor MP, Hogue IB, Enquist LW, Murthy M, Wang SS-H. 2013. Fast GCaMPs for improved tracking of neuronal activity. Nature Communications 4. doi: 10.1038/ncomms3170
60. Suter BA, Shepherd GM. 2015. Reciprocal interareal connections to corticospinal neurons in mouse M1 and S2. Journal of Neuroscience 35:2959-2974. doi: 10.1523/JNEUROSCI.4287-14.2015
61. Theyel BB, Llano DA, Sherman SM. 2010. The corticothalamocortical circuit drives higher-order cortex in the mouse. Nature Neuroscience 13:84-88. doi: 10.1038/nn.2449
62. Tsai PS, Mateo C, Field JJ, Schaffer CB, Anderson ME, Kleinfeld D. 2015. Ultra-large field-of-view two-photon microscopy. Optics Express 23:13833-13847. doi: 10.1364/OE.23.013833
63. Yamashita T, Pala A, Pedrido L, Kremer Y, Welker E, Petersen CC. 2013. Membrane potential dynamics of neocortical projection neurons driving target-specific signals. Neuron 80:1477-1490. doi: 10.1016/j.neuron. 2013.10.059
64. Yang H, Kwon SE, Severson KS, O’Connor DH. 2016. Origins of choice-related activity in mouse somatosensory cortex. Nature Neuroscience 19:127-134. doi: 10.1038/nn.4183
65. Yu C, Derdikman D, Haidarliu S, Ahissar E. 2006. Parallel thalamic pathways for whisking and touch signals in the rat. PLoS Biology 4:e124. doi: 10.1371/journal.pbio.0040124
66. Zagha E, Casale AE, Sachdev RN, McGinley MJ, McCormick DA. 2013. Motor cortex feedback influences sensory processing by modulating network state. Neuron 79:567-578. doi: 10.1016/j.neuron.2013.06.008
67. Zingg B, Hintiryan H, Gou L, Song MY, Bay M, Bienkowski MS, Foster NN, Yamashita S, Bowman I, Toga AW, Dong HW. 2014. Neural networks of the mouse neocortex. Cell 156:1096-1111. doi: 10.1016/j.cell.2014.02.023