Mapping cortical mesoscopic networks of single spiking cortical or sub-cortical neurons

eLife

Volumn 6, Issue , 2017, Pages

  Xiao, Dongsheng ^a,b,c   Vanni, Matthieu P ^a,c   Mitelut, Catalin C ^a,c   Chan, Allen W ^a,c   Ledue, Jeffrey M ^c   Xie, Yicheng ^a,c   Chen, Andrew C N ^b   Swindale, Nicholas V ^d   Murphy, Timothy H ^a,c  

^a 4N1 2255 Wesbrook Mall   (Canada)

^b BEIJING INSTITUTE FOR BRAIN DISORDERS   (China)

^c UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^d UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; AVERAGING; BRAIN CELL; CONSENSUS; ELECTROPHYSIOLOGY; EXCITATION; IMAGING; NONHUMAN; SPIKE; THALAMUS; WAKEFULNESS; ACTION POTENTIAL; ANATOMY AND HISTOLOGY; ANESTHESIA; ANIMAL; BRAIN CORTEX; BRAIN MAPPING; CALCIUM SIGNALING; CHEMISTRY; CYTOLOGY; ELECTRODE IMPLANT; FLUORESCENCE IMAGING; GENETICS; MALE; MOLECULAR PROBE; MOUSE; NERVE CELL; NERVE CELL NETWORK; PHYSIOLOGY; PROCEDURES; STEREOTACTIC PROCEDURE; TRANSGENIC MOUSE;

CALCIUM;

ACTION POTENTIALS; ANESTHESIA; ANIMALS; BRAIN MAPPING; CALCIUM; CALCIUM SIGNALING; CEREBRAL CORTEX; ELECTRODES, IMPLANTED; MALE; MICE; MICE, TRANSGENIC; MOLECULAR PROBES; NERVE NET; NEURONS; OPTICAL IMAGING; STEREOTAXIC TECHNIQUES; THALAMUS; WAKEFULNESS;

EID: 85014109157     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.19976     Document Type: Article

References (89)

1. Aaron G, Yuste R. 2006. Reverse optical probing (ROPING) of neocortical circuits. Synapse 60:437–440. doi: 10. 1002/syn.20316, PMID: 16881073
2. Abdelfattah AS, Farhi SL, Zhao Y, Brinks D, Zou P, Ruangkittisakul A, Platisa J, Pieribone VA, Ballanyi K, Cohen AE, Campbell RE. 2016. A bright and fast red fluorescent protein voltage Indicator that reports neuronal activity in organotypic brain slices. Journal of Neuroscience 36:2458–2472. doi: 10.1523/JNEUROSCI.3484-15. 2016, PMID: 26911693
3. Aljadeff J, Lansdell BJ, Fairhall AL, Kleinfeld D. 2016. Analysis of neuronal spike trains, deconstructed. Neuron 91:221–259. doi: 10.1016/j.neuron.2016.05.039, PMID: 27477016
4. Arieli A, Shoham D, Hildesheim R, Grinvald A. 1995. Coherent spatiotemporal patterns of ongoing activity revealed by real-time optical imaging coupled with single-unit recording in the cat visual cortex. Journal of Neurophysiology 73:2072–2093. PMID: 7623099
5. Bohland JW, Wu C, Barbas H, Bokil H, Bota M, Breiter HC, Cline HT, Doyle JC, Freed PJ, Greenspan RJ, Haber SN, Hawrylycz M, Herrera DG, Hilgetag CC, Huang ZJ, Jones A, Jones EG, Karten HJ, Kleinfeld D, Kötter R, et al. 2009. A proposal for a coordinated effort for the determination of brainwide neuroanatomical connectivity in model organisms at a mesoscopic scale. PLoS Computational Biology 5:e1000334. doi: 10.1371/journal.pcbi.1000334, PMID: 19325892
6. Bruno RM, Sakmann B. 2006. Cortex is driven by weak but synchronously active thalamocortical synapses. Science 312:1622–1627. doi: 10.1126/science.1124593, PMID: 16778049
7. Busche MA, Kekuš M, Adelsberger H, Noda T, Förstl H, Nelken I, Konnerth A. 2015. Rescue of long-range circuit dysfunction in Alzheimer’s disease models. Nature Neuroscience 18:1623–1630. doi: 10.1038/nn.4137, PMID: 26457554
8. Buzsáki G. 2004. Large-scale recording of neuronal ensembles. Nature Neuroscience 7:446–451. doi: 10.1038/nn1233, PMID: 15114356
9. Carandini M, Shimaoka D, Rossi LF, Sato TK, Benucci A, Knöpfel T. 2015. Imaging the awake visual cortex with a genetically encoded voltage Indicator. Journal of Neuroscience 35:53–63. doi: 10.1523/JNEUROSCI.0594-14.2015, PMID: 25568102
10. Castro-Alamancos MA. 1997. Short-term plasticity in thalamocortical pathways: cellular mechanisms and functional roles. Reviews in the Neurosciences 8:95–116. doi: 10.1515/REVNEURO.1997.8.2.95, PMID: 9344181
11. Chan AW, Mohajerani MH, LeDue JM, Wang YT, Murphy TH. 2015. Mesoscale infraslow spontaneous membrane potential fluctuations recapitulate high-frequency activity cortical motifs. Nature Communications 6:7738. doi: 10.1038/ncomms8738, PMID: 26190168
12. Chemla S, Chavane F. 2010. Voltage-sensitive dye imaging: technique review and models. Journal of Physiology-Paris 104:40–50. doi: 10.1016/j.jphysparis.2009.11.009, PMID: 19909809
13. Chen JL, Carta S, Soldado-Magraner J, Schneider BL, Helmchen F. 2013a. Behaviour-dependent recruitment of long-range projection neurons in somatosensory cortex. Nature 499:336–340. doi: 10.1038/nature12236, PMID: 23792559
14. Chen TW, Wardill TJ, Sun Y, Pulver SR, Renninger SL, Baohan A, Schreiter ER, Kerr RA, Orger MB, Jayaraman V, Looger LL, Svoboda K, Kim DS. 2013b. Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature 499:295–300. doi: 10.1038/nature12354, PMID: 23868258
15. Connors BW, Gutnick MJ. 1990. Intrinsic firing patterns of diverse neocortical neurons. Trends in Neurosciences 13:99–104. doi: 10.1016/0166-2236(90)90185-D, PMID: 1691879
16. Cruikshank SJ, Lewis TJ, Connors BW. 2007. Synaptic basis for intense thalamocortical activation of feedforward inhibitory cells in neocortex. Nature Neuroscience 10:462–468. doi: 10.1038/nn1861, PMID: 17334362
17. de Pasquale F, Della Penna S, Snyder AZ, Lewis C, Mantini D, Marzetti L, Belardinelli P, Ciancetta L, Pizzella V, Romani GL, Corbetta M. 2010. Temporal dynamics of spontaneous MEG activity in brain networks. PNAS 107: 6040–6045. doi: 10.1073/pnas.0913863107, PMID: 20304792
18. DeNardo LA, Berns DS, DeLoach K, Luo L. 2015. Connectivity of mouse somatosensory and prefrontal cortex examined with trans-synaptic tracing. Nature Neuroscience 18:1687–1697. doi: 10.1038/nn.4131, PMID: 26457553
19. Deschênes M, Takatoh J, Kurnikova A, Moore JD, Demers M, Elbaz M, Furuta T, Wang F, Kleinfeld D. 2016. Inhibition, not excitation, drives rhythmic whisking. Neuron 90:374–387. doi: 10.1016/j.neuron.2016.03.007, PMID: 27041498
20. 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, PMID: 7638624
21. 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, PMID: 1 8054865
22. Fu Y, Tucciarone JM, Espinosa JS, Sheng N, Darcy DP, Nicoll RA, Huang ZJ, Stryker MP. 2014. A cortical circuit for gain control by behavioral state. Cell 156:1139–1152. doi: 10.1016/j.cell.2014.01.050, PMID: 24630718
23. 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, PMID: 16242411
24. Galarreta M, Hestrin S. 1998. Frequency-dependent synaptic depression and the balance of excitation and inhibition in the neocortex. Nature Neuroscience 1:587–594. doi: 10.1038/2822, PMID: 10196566
25. Gil Z, Connors BW, Amitai Y. 1997. Differential regulation of neocortical synapses by neuromodulators and activity. Neuron 19:679–686. doi: 10.1016/S0896-6273(00)80380-3, PMID: 9331357
26. Gong Y, Huang C, Li JZ, Grewe BF, Zhang Y, Eismann S, Schnitzer MJ. 2015. High-speed recording of neural spikes in awake mice and flies with a fluorescent voltage sensor. Science 350:1361–1366. doi: 10.1126/science.aab0810, PMID: 26586188
27. Guggenmos DJ, Azin M, Barbay S, Mahnken JD, Dunham C, Mohseni P, Nudo RJ. 2013. Restoration of function after brain damage using a neural prosthesis. PNAS 110:21177–21182. doi: 10.1073/pnas.1316885110, PMID: 24324155
28. 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, PMID: 24361077
29. Hamel EJ, Grewe BF, Parker JG, Schnitzer MJ. 2015. Cellular level brain imaging in behaving mammals: an engineering approach. Neuron 86:140–159. doi: 10.1016/j.neuron.2015.03.055, PMID: 25856491
30. Harvey CD, Coen P, Tank DW. 2012. Choice-specific sequences in parietal cortex during a virtual-navigation decision task. Nature 484:62–68. doi: 10.1038/nature10918, PMID: 22419153
31. Hooks BM, Mao T, Gutnisky DA, Yamawaki N, Svoboda K, Shepherd GM. 2013. Organization of cortical and thalamic input to pyramidal neurons in mouse motor cortex. Journal of Neuroscience 33:748–760. doi: 10.1523/JNEUROSCI.4338-12.2013, PMID: 23303952
32. Hu H, Agmon A. 2016. Differential excitation of distally versus proximally targeting cortical interneurons by unitary thalamocortical bursts. Journal of Neuroscience 36:6906–6916. doi: 10.1523/JNEUROSCI.0739-16.2016, PMID: 27358449
33. Hunnicutt BJ, Long BR, Kusefoglu D, Gertz KJ, Zhong H, Mao T. 2014. A comprehensive thalamocortical projection map at the mesoscopic level. Nature Neuroscience 17:1276–1285. doi: 10.1038/nn.3780, PMID: 250 86607
34. Iaccarino HF, Singer AC, Martorell AJ, Rudenko A, Gao F, Gillingham TZ, Mathys H, Seo J, Kritskiy O, Abdurrob F, Adaikkan C, Canter RG, Rueda R, Brown EN, Boyden ES, Tsai LH. 2016. Gamma frequency entrainment attenuates amyloid load and modifies microglia. Nature 540:230–235. doi: 10.1038/nature20587, PMID: 27929004
35. Kahn I, Desai M, Knoblich U, Bernstein J, Henninger M, Graybiel AM, Boyden ES, Buckner RL, Moore CI. 2011. Characterization of the functional MRI response temporal linearity via optical control of neocortical pyramidal neurons. Journal of Neuroscience 31:15086–15091. doi: 10.1523/JNEUROSCI.0007-11.2011, PMID: 22016542
36. Kenet T, Bibitchkov D, Tsodyks M, Grinvald A, Arieli A. 2003. Spontaneously emerging cortical representations of visual attributes. Nature 425:954–956. doi: 10.1038/nature02078, PMID: 14586468
37. Kim CK, Yang SJ, Pichamoorthy N, Young NP, Kauvar I, Jennings JH, Lerner TN, Berndt A, Lee SY, Ramakrishnan C, Davidson TJ, Inoue M, Bito H, Deisseroth K. 2016a. Simultaneous fast measurement of circuit dynamics at multiple sites across the mammalian brain. Nature Methods 13:325–328. doi: 10.1038/nmeth.3770, PMID: 2687 8381
38. Kim TH, Zhang Y, Lecoq J, Jung JC, Li J, Zeng H, Niell CM, Schnitzer MJ. 2016b. Long-Term optical access to an estimated one million neurons in the live mouse cortex. Cell Reports 17:3385–3394. doi: 10.1016/j.celrep.2016.12.004, PMID: 28009304
39. Kleinfeld D, Delaney KR, Fee MS, Flores JA, Tank DW, Gelperin A. 1994. Dynamics of propagating waves in the olfactory network of a terrestrial mollusk: an electrical and optical study. Journal of Neurophysiology 72:1402–1419. PMID: 7807221
40. Lim DH, Mohajerani MH, Ledue J, Boyd J, Chen S, Murphy TH. 2012. In vivo Large-Scale cortical mapping using Channelrhodopsin-2 stimulation in transgenic mice reveals asymmetric and reciprocal relationships between cortical areas. Frontiers in Neural Circuits 6:11. doi: 10.3389/fncir.2012.00011, PMID: 22435052
41. Linden JF, Schreiner CE. 2003. Columnaar transformations in auditory cortex? A comparison to visual and somatosensory cortices. Cerebral Cortex 13:83–89. doi: 10.1093/cercor/13.1.83, PMID: 12466219
42. Logothetis NK, Eschenko O, Murayama Y, Augath M, Steudel T, Evrard HC, Besserve M, Oeltermann A. 2012. Hippocampal-cortical interaction during periods of subcortical silence. Nature 491:547–553. doi: 10.1038/nature11618, PMID: 23172213
43. Ma Y, Shaik MA, Kim SH, Kozberg MG, Thibodeaux DN, Zhao HT, Yu H, Hillman EMC. 2016. Wide-field optical mapping of neural activity and brain haemodynamics: considerations and novel approaches. Philosophical Transactions of the Royal Society B: Biological Sciences 371:20150360. doi: 10.1098/rstb.2015.0360
44. 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, PMID: 25741722
45. McCormick DA, Feeser HR. 1990. Functional implications of burst firing and single spike activity in lateral geniculate relay neurons. Neuroscience 39:103–113. doi: 10.1016/0306-4522(90)90225-S
46. McCormick DA, McGinley MJ, Salkoff DB. 2015. Brain state dependent activity in the cortex and thalamus. Current Opinion in Neurobiology 31:133–140. doi: 10.1016/j.conb.2014.10.003, PMID: 25460069
47. Miller LM, Escabí MA, Read HL, Schreiner CE. 2001. Functional convergence of response properties in the auditory thalamocortical system. Neuron 32:151–160. doi: 10.1016/S0896-6273(01)00445-7, PMID: 11604146
48. Mohajerani MH, Chan AW, Mohsenvand M, LeDue J, Liu R, McVea DA, Boyd JD, Wang YT, Reimers M, Murphy TH. 2013. Spontaneous cortical activity alternates between motifs defined by regional axonal projections. Nature Neuroscience 16:1426–1435. doi: 10.1038/nn.3499, PMID: 23974708
49. Mohajerani MH, McVea DA, Fingas M, Murphy TH. 2010. Mirrored bilateral slow-wave cortical activity within local circuits revealed by fast bihemispheric voltage-sensitive dye imaging in anesthetized and awake mice. Journal of Neuroscience 30:3745–3751. doi: 10.1523/JNEUROSCI.6437-09.2010, PMID: 20220008
50. Moore JD, Deschênes M, Furuta T, Huber D, Smear MC, Demers M, Kleinfeld D. 2013. Hierarchy of orofacial rhythms revealed through whisking and breathing. Nature 497:205–210. doi: 10.1038/nature12076, PMID: 23624373
51. Murphy TH, Boyd JD, Bolaños F, Vanni MP, Silasi G, Haupt D, LeDue JM. 2016. High-throughput automated home-cage mesoscopic functional imaging of mouse cortex. Nature Communications 7:11611. doi: 10.1038/ncomms11611, PMID: 27291514
52. Nauhaus I, Busse L, Carandini M, Ringach DL. 2009. Stimulus contrast modulates functional connectivity in visual cortex. Nature Neuroscience 12:70–76. doi: 10.1038/nn.2232, PMID: 19029885
53. Nowak LG, Sanchez-Vives MV, McCormick DA. 2005. Role of synaptic and intrinsic membrane properties in short-term receptive field dynamics in cat area 17. Journal of Neuroscience 25:1866–1880. doi: 10.1523/JNEUROSCI.3897-04.2005, PMID: 15716423
54. 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, PMID: 23727820
55. 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, PMID: 24695228
56. Okun M, Steinmetz NA, Cossell L, Iacaruso MF, Ko H, Barthó P, Moore T, Hofer SB, Mrsic-Flogel TD, Carandini M, Harris KD. 2015. Diverse coupling of neurons to populations in sensory cortex. Nature 521:511–515. doi: 10.1038/nature14273, PMID: 25849776
57. Pape HC, McCormick DA. 1995. Electrophysiological and pharmacological properties of interneurons in the cat dorsal lateral geniculate nucleus. Neuroscience 68:1105–1125. doi: 10.1016/0306-4522(95)00205-W, PMID: 8544986
58. Paz JT, Davidson TJ, Frechette ES, Delord B, Parada I, Peng K, Deisseroth K, Huguenard JR. 2013. Closed-loop optogenetic control of thalamus as a tool for interrupting seizures after cortical injury. Nature Neuroscience 16: 64–70. doi: 10.1038/nn.3269, PMID: 23143518
59. Petrus E, Isaiah A, Jones AP, Li D, Wang H, Lee HK, Kanold PO. 2014. Crossmodal induction of thalamocortical potentiation leads to enhanced information processing in the auditory cortex. Neuron 81:664–673. doi: 10.1016/j.neuron.2013.11.023, PMID: 24507197
60. Pnevmatikakis EA, Soudry D, Gao Y, Machado TA, Merel J, Pfau D, Reardon T, Mu Y, Lacefield C, Yang W, Ahrens M, Bruno R, Jessell TM, Peterka DS, Yuste R, Paninski L. 2016. Simultaneous denoising, deconvolution, and demixing of calcium imaging data. Neuron 89:285–299. doi: 10.1016/j.neuron.2015.11.037, PMID: 26774160
61. Rickgauer JP, Deisseroth K, Tank DW. 2014. Simultaneous cellular-resolution optical perturbation and imaging of place cell firing fields. Nature Neuroscience 17:1816–1824. doi: 10.1038/nn.3866, PMID: 25402854
62. Serruya MD, Hatsopoulos NG, Paninski L, Fellows MR, Donoghue JP. 2002. Instant neural control of a movement signal. Nature 416:141–142. doi: 10.1038/416141a, PMID: 11894084
63. Sherman SM, Guillery RW, Sherman SM. 2006. Exploring the Thalamus and Its Role in Cortical Function. Cambridge, Massachusetts: MIT Press.
64. Sherman SM, Guillery RW. 1996. Functional organization of thalamocortical relays. Journal of Neurophysiology 76:1367–1395. PMID: 8890259
65. Sheroziya M, Timofeev I. 2014. Global intracellular slow-wave dynamics of the thalamocortical system. Journal of Neuroscience 34:8875–8893. doi: 10.1523/JNEUROSCI.4460-13.2014, PMID: 24966387
66. Shoham D, Glaser DE, Arieli A, Kenet T, Wijnbergen C, Toledo Y, Hildesheim R, Grinvald A. 1999. Imaging cortical dynamics at high spatial and temporal resolution with novel blue voltage-sensitive dyes. Neuron 24: 791–802. doi: 10.1016/S0896-6273(00)81027-2, PMID: 10624943
67. Silasi G, Xiao D, Vanni MP, Chen AC, Murphy TH. 2016. Intact skull chronic windows for mesoscopic wide-field imaging in awake mice. Journal of Neuroscience Methods 267:141–149. doi: 10.1016/j.jneumeth.2016.04.012, PMID: 27102043
68. Simons DJ, Carvell GE. 1989. Thalamocortical response transformation in the rat vibrissa/barrel system. Journal of Neurophysiology 61:311–330. PMID: 2918357
69. Sirotin YB, Das A. 2010. Spatial relationship between flavoprotein fluorescence and the hemodynamic response in the primary visual cortex of alert macaque monkeys. Frontiers in Neuroenergetics 2:6. doi: 10.3389/fnene. 2010.00006, PMID: 20577638
70. Sofroniew NJ, Flickinger D, King J, Svoboda K. 2016. A large field of view two-photon mesoscope with subcellular resolution for in vivo imaging. eLife 5:e14472. doi: 10.7554/eLife.14472, PMID: 27300105
71. Sreenivasan V, Petersen CC. 2016. Inhibition patterns the whisking rhythm. Neuron 90:211–213. doi: 10.1016/j.neuron.2016.04.012, PMID: 27100193
72. Stanley GB, Li FF, Dan Y. 1999. Reconstruction of natural scenes from ensemble responses in the lateral geniculate nucleus. The Journal of Neuroscience 19:8036–8042. PMID: 10479703
73. Steriade M, Llinás RR. 1988. The functional states of the thalamus and the associated neuronal interplay. Physiological Reviews 68:649–742. PMID: 2839857
74. Stroh A, Adelsberger H, Groh A, Rühlmann C, Fischer S, Schierloh A, Deisseroth K, Konnerth A. 2013. Making waves: initiation and propagation of corticothalamic Ca2+ waves in vivo. Neuron 77:1136–1150. doi: 10.1016/j.neuron.2013.01.031, PMID: 23522048
75. Swadlow HA, Gusev AG. 2001. The impact of ’bursting’ thalamic impulses at a neocortical synapse. Nature Neuroscience 4:402–408. doi: 10.1038/86054, PMID: 11276231
76. Swindale NV, Spacek MA. 2014. Spike sorting for polytrodes: a divide and conquer approach. Frontiers in Systems Neuroscience 8:1–21. doi: 10.3389/fnsys.2014.00006, PMID: 24574979
77. Taylor DM, Tillery SI, Schwartz AB. 2002. Direct cortical control of 3D neuroprosthetic devices. Science 296: 1829–1832. doi: 10.1126/science.1070291, PMID: 12052948
78. 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, PMID: 19966840
79. 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, PMID: 26072755
80. Tsodyks M, Kenet T, Grinvald A, Arieli A. 1999. Linking spontaneous activity of single cortical neurons and the underlying functional architecture. Science 286:1943–1946. doi: 10.1126/science.286.5446.1943, PMID: 10583955
81. Urbain N, Salin PA, Libourel PA, Comte JC, Gentet LJ, Petersen CC. 2015. Whisking-Related changes in neuronal firing and membrane potential dynamics in the somatosensory thalamus of awake mice. Cell Reports 13:647–656. doi: 10.1016/j.celrep.2015.09.029, PMID: 26489463
82. Vanni MP, Murphy TH. 2014. Mesoscale transcranial spontaneous activity mapping in GCaMP3 transgenic mice reveals extensive reciprocal connections between areas of somatomotor cortex. Journal of Neuroscience 34: 15931–15946. doi: 10.1523/JNEUROSCI.1818-14.2014, PMID: 25429135
83. Wekselblatt JB, Flister ED, Piscopo DM, Niell CM. 2016. Large-scale imaging of cortical dynamics during sensory perception and behavior. Journal of Neurophysiology 115:2852–2866. doi: 10.1152/jn.01056.2015, PMID: 26 912600
84. White BR, Bauer AQ, Snyder AZ, Schlaggar BL, Lee JM, Culver JP. 2011. Imaging of functional connectivity in the mouse brain. PLoS One 6:e16322. doi: 10.1371/journal.pone.0016322, PMID: 21283729
85. Xie Y, Chan AW, McGirr A, Xue S, Xiao D, Zeng H, Murphy TH. 2016. Resolution of High-Frequency mesoscale intracortical maps using the genetically encoded glutamate sensor iGluSnFR. Journal of Neuroscience 36:1261–1272. doi: 10.1523/JNEUROSCI.2744-15.2016, PMID: 26818514
86. Xu S, Jiang W, Poo MM, Dan Y. 2012. Activity recall in a visual cortical ensemble. Nature Neuroscience 15:449– 455. doi: 10.1038/nn.3036, PMID: 22267160
87. Zariwala HA, Borghuis BG, Hoogland TM, Madisen L, Tian L, De Zeeuw CI, Zeng H, Looger LL, Svoboda K, Chen TW. 2012. A Cre-dependent GCaMP3 reporter mouse for neuronal imaging in vivo. Journal of Neuroscience 32:3131–3141. doi: 10.1523/JNEUROSCI.4469-11.2012, PMID: 22378886
88. 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, PMID: 24581503
89. Zou P, Zhao Y, Douglass AD, Hochbaum DR, Brinks D, Werley CA, Harrison DJ, Campbell RE, Cohen AE. 2014. Bright and fast multicoloured voltage reporters via electrochromic FRET. Nature Communications 5:4625. doi: 10.1038/ncomms5625, PMID: 25118186