Simultaneous visualization of extrinsic and intrinsic axon collaterals in golgi-like detail for mouse corticothalamic and corticocortical cells: A double viral infection method

Frontiers in Neural Circuits

Volumn 8, Issue , 2014, Pages

  Watakabe, Akiya ^a   Takaji, Masafumi ^a   Kato, Shigeki ^b   Kobayashi, Kazuto ^b   Mizukami, Hiroaki ^c   Ozawa, Keiya ^c   Ohsawa, Sonoko ^a   Matsui, Ryosuke ^d   Watanabe, Dai ^d   Yamamori, Tetsuo ^a  

^a NATIONAL INSTITUTE FOR BASIC BIOLOGY   (Japan)

^b FUKUSHIMA MEDICAL UNIVERSITY   (Japan)

^c JICHI MEDICAL UNIVERSITY   (Japan)

^d KYOTO UNIVERSITY   (Japan)

Author keywords

AAV; Axon collateral; Corticothalamic; Pyramidal; Retrograde viral vector; Tracer

Indexed keywords

SYNAPTOPHYSIN; AXON; CHOLERA TOXIN; PHOTOPROTEIN; VESICULAR GLUTAMATE TRANSPORTER 2;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL LABELING; CLAUSTRUM; CONTROLLED STUDY; CORPUS STRIATUM; CORTICOCORTICAL CELL; CORTICOTHALAMIC CELL; DENDRITE; EXTRINSIC AXON COLLATERAL; FEMALE; GOLGI COMPLEX; HUMAN; HUMAN CELL; INTRINSIC AXON COLLATERAL; ION EXCHANGE CHROMATOGRAPHY; MALE; MORPHOLOGY; MOTOR CORTEX; MOUSE; NERVE CELL; NERVE FIBER; NERVE FIBER GROWTH; NERVE PROJECTION; NONHUMAN; PLASMID; PROMOTER REGION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SOMATOSENSORY CORTEX; THALAMUS; THALAMUS VENTRAL NUCLEUS; VIRUS INFECTION; ANIMAL; C57BL MOUSE; CYTOLOGY; DEPENDOPARVOVIRUS; GENE VECTOR; GENETIC TRANSDUCTION; GENETICS; HEMISPHERIC DOMINANCE; LENTIVIRUS; METABOLISM; NERVE CELL NETWORK; NERVE TRACT; PHYSIOLOGY;

ANIMALS; AXONS; CHOLERA TOXIN; DEPENDOVIRUS; FEMALE; FUNCTIONAL LATERALITY; GENETIC VECTORS; LENTIVIRUS; LUMINESCENT PROTEINS; MALE; MICE; MICE, INBRED C57BL; MOTOR CORTEX; NERVE NET; NEURAL PATHWAYS; SOMATOSENSORY CORTEX; THALAMUS; TRANSDUCTION, GENETIC; VESICULAR GLUTAMATE TRANSPORT PROTEIN 2;

EID: 84907292474     PISSN: 16625110     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncir.2014.00110     Document Type: Article

References (81)

1. Alloway, K. D., Olson, M. L., and Smith, J. B. (2008). Contralateral corticothalamic projections from MI whisker cortex: Potential route for modulating hemispheric interactions. J. Comp. Neurol. 510, 100-116. doi: 10.1002/cne.21782
2. Beier, K. T., Saunders, A., Oldenburg, I. A., Miyamichi, K., Akhtar, N., Luo, L., et al. (2011). Anterograde or retrograde transsynaptic labeling of CNS neurons with vesicular stomatitis virus vectors. Proc. Natl. Acad. Sci. U.S.A. 108, 15414-15419. doi: 10.1073/pnas.1110854108
3. Bortone, D. S., Olsen, S. R., and Scanziani, M. (2014). Translaminar inhibitory cells recruited by layer 6 corticothalamic neurons suppress visual cortex. Neuron 82, 474-485. doi: 10.1016/j.neuron.2014.02.021
4. Bourassa, J., Pinault, D., and Deschenes, M. (1995). Corticothalamic projections from the cortical barrel field to the somatosensory thalamus in rats: a single-fibre study using biocytin as an anterograde tracer. Eur. J. Neurosci. 7, 19-30. doi: 10.1111/j.1460-9568.1995.tb01016.x
5. Briggs, F., and Callaway, E. M. (2001). Layer-specific input to distinct cell types in layer 6 of monkey primary visual cortex. J. Neurosci. 21, 3600-3608.
6. Britanova, O, de Juan Romero, C, Cheung, A, Kwan, K. Y, Schwark, M., Gyorgy, A. et al. (2008). Satb2 is a postmitotic determinant for upper-layer neuron specification in the neocortex. Neuron 57, 378-392. doi: 10.1016/j.neuron.2007.12.028
7. Burger, C., Gorbatyuk, O. S., Velardo, M. J., Peden, C. S., Williams, P., Zolotukhin, S., et al. (2004). Recombinant AAV viral vectors pseudotyped with viral cap-sids from serotypes 1, 2, and 5 display differential efficiency and cell tropism after delivery to different regions of the central nervous system. Mol. Ther. 10, 302-317. doi: 10.1016/j.ymthe.2004.05.024
8. Chomiak, T., Peters, S., and Hu, B. (2008). Functional architecture and spike timing properties of corticofugal projections from rat ventral temporal cortex. J. Neurophysiol. 100, 327-335. doi: 10.1152/jn.90392.2008
9. Deschenes, M., Bourassa, J., and Pinault, D. (1994). Corticothalamic projections from layer V cells in rat are collaterals of long-range corticofugal axons. Brain Res. 664, 215-219. doi: 10.1016/0006-8993(94)91974-7
10. Fame, R. M., MacDonald, J. L., and Macklis, J. D. (2011). Development, specification, and diversity of callosal projection neurons. Trends Neurosci. 34, 41-50. doi: 10.1016/j.tins.2010.10.002
11. Ferland, R. J., Cherry, T. J., Preware, P. O., Morrisey, E. E., and Walsh, C. A. (2003). Characterization of Foxp2 and Foxp1 mRNA and protein in the developing and mature brain. J. Comp. Neurol. 460, 266-279. doi: 10.1002/cne.10654
12. Fishell, G., and Heintz, N. (2013). The neuron identity problem: Form meets function. Neuron 80, 602-612. doi: 10.1016/j.neuron.2013.10.035
13. Fitzpatrick, D. (1996). The functional organization of local circuits in visual cortex: Insights from the study of tree shrew striate cortex. Cereb. Cortex 6, 329-341. doi: 10.1093/cercor/6.3.329
14. Garcez, P. P., Henrique, N. P., Furtado, D. A., Bolz, J., Lent, R., and Uziel, D. (2007). Axons of callosal neurons bifurcate transiently at the white matter before consolidating an interhemispheric projection. Eur. J. Neurosci. 25, 1384-1394. doi: 10.1111/j.1460-9568.2007.05387.x
15. Gilbert, C. D. (1983). Microcircuitry of the visual cortex. Annu. Rev. Neurosci. 6, 217-247. doi: 10.1146/annurev.ne.06.030183.001245
16. Greig, L. C., Woodworth, M. B., Galazo, M. J., Padmanabhan, H., and Macklis, J. D. (2013). Molecular logic of neocortical projection neuron specification, development and diversity. Nat. Rev. Neurosci. 14, 755-769. doi: 10.1038/nrn3586
17. Hagmann, P., Cammoun, L., Gigandet, X., Meuli, R., Honey, C. J., Wedeen, V. J., et al. (2008). Mapping the structural core of human cerebral cortex. PLoS Biol. 6:e159. doi: 10.1371/journal.pbio.0060159
18. Hattox, A. M., and Nelson, S. B. (2007). Layer V neurons in mouse cortex projecting to different targets have distinct physiological properties. J. Neurophysiol. 98, 3330-3340. doi: 10.1152/jn.00397.2007
19. Hioki, H., Kuramoto, E., Konno, M., Kameda, H., Takahashi, Y., Nakano, T., et al. (2009). High-level transgene expression in neurons by lentivirus with Tet-Off system. Neurosci. Res. 63, 149-154. doi: 10.1016/j.neures.2008.10.010
20. Hirai, Y., Morishima, M., Karube, F., and Kawaguchi, Y. (2012). Specialized cortical subnetworks differentially connect frontal cortex to parahippocampal areas. J. Neurosci. 32, 1898-1913. doi: 10.1523/JNEUROSCI.2810-11.2012
21. Hooks, B. M., Hires, S. A., Zhang, Y. X., Huber, D., Petreanu, L., Svoboda, K., et al. (2011). Laminar analysis of excitatory local circuits in vibrissal motor and sensory cortical areas. PLoS Biol. 9:e1000572. doi: 10.1371/journal.pbio.1000572
22. Huang, C. C., Sugino, K., Shima, Y., Guo, C., Bai, S., Mensh, B. D., et al. (2013). Convergence of pontine and proprioceptive streams onto multimodal cerebellar granule cells. Elife 2:e00400. doi: 10.7554/eLife.00400
23. Huang, Z. J., and Zeng, H. (2013). Genetic approaches to neural circuits in the mouse. Annu. Rev. Neurosci. 36, 183-215. doi: 10.1146/annurev-neuro-062012-170307
24. Ichinohe, N., Borra, E., and Rockland, K. (2012). Distinct feedforward and intrinsic neurons in posterior inferotemporal cortex revealed by in vivo connection imaging. Sci. Rep. 2:934. doi: 10.1038/srep00934
25. Kaneko, T. (2013). Local connections of excitatory neurons in motor-associated cortical areas of the rat. Front. Neural Circuits 7:75. doi: 10.3389/fncir.2013.00075
26. Kaneko, T., Fujiyama, F., and Hioki, H. (2002). Immunohistochemical localization of candidates for vesicular glutamate transporters in the rat brain. J. Comp. Neurol. 444, 39-62. doi: 10.1002/cne.10129
27. Kasper, E. M., Larkman, A. U., Lubke, J., and Blakemore, C. (1994). Pyramidal neurons in layer 5 of the rat visual cortex. I. Correlation among cell morphology, intrinsic electrophysiological properties, and axon targets. J. Comp. Neurol. 339, 459-474. doi: 10.1002/cne.903390402
28. Kato, S., Inoue, K., Kobayashi, K., Yasoshima, Y., Miyachi, S., Inoue, S., et al. (2007). Efficient gene transfer via retrograde transport in rodent and primate brains using a human immunodeficiency virus type 1-based vector pseudotyped with rabies virus glycoprotein. Hum. Gene Ther. 18, 1141-1151. doi: 10.1089/hum.2007.082
29. Kato, S., Kobayashi, K., Inoue, K., Kuramochi, M., Okada, T., Yaginuma, H., et al. (2011). A lentiviral strategy for highly efficient retrograde gene transfer by pseudotyping with fusion envelope glycoprotein. Hum. Gene Ther. 22, 197-206. doi: 10.1089/hum.2009.179
30. Kato, S., Kobayashi, K., and Kobayashi, K. (2013). Dissecting circuit mechanisms by genetic manipulation of specific neural pathways. Rev. Neurosci. 24, 1-8. doi: 10.1515/revneuro-2012-0043
31. Kato, S., Kuramochi, M., Kobayashi, K., Fukabori, R., Okada, K., Uchigashima, M., et al. (2011). Selective neural pathway targeting reveals key roles of tha-lamostriatal projection in the control of visual discrimination. J. Neurosci. 31, 17169-17179. doi: 10.1523/JNEUROSCI.4005-11.2011
32. Kato, S., Kuramochi, M., Takasumi, K., Kobayashi, K., Inoue, K., Takahara, D., et al. (2011). Neuron-specific gene transfer through retrograde transport of lentiviral vector pseudotyped with a novel type of fusion envelope glycoprotein. Hum. Gene Ther. 22, 1511-1523. doi: 10.1089/hum.2011.111
33. Killackey, H. P., and Sherman, S. M. (2003). Corticothalamic projections from the rat primary somatosensory cortex. J. Neurosci. 23, 7381-7384.
34. Kim, J., Matney, C. J., Blankenship, A., Hestrin, S., and Brown, S. P. (2014). Layer 6 corticothalamic neurons activate a cortical output layer, layer 5a. J. Neurosci. 34, 9656-9664. doi: 10.1523/JNEUROSCI.1325-14.2014
35. Kimura, F., and Itami, C. (2009). Myelination and isochronicity in neural networks. Front. Neuroanat. 3:12. doi: 10.3389/neuro.05.012.2009
36. Kinoshita, M., Matsui, R., Kato, S., Hasegawa, T., Kasahara, H., Isa, K., et al. (2012). Genetic dissection of the circuit for hand dexterity in primates. Nature 487, 235-238. doi: 10.1038/nature11206
37. Koester, S. E., and O’Leary, D. D. (1993). Connectional distinction between callosal and subcortically projecting cortical neurons is determined prior to axon extension. Dev. Biol. 160, 1-14. doi: 10.1006/dbio.1993.1281
38. Kwon, I., and Schaffer, D. V. (2008). Designer gene delivery vectors: molecular engineering and evolution of adeno-associated viral vectors for enhanced gene transfer. Pharm. Res. 25, 489-499. doi: 10.1007/s11095-007-9431-0
39. Lee, C. C., Lam, Y. W., and Sherman, S. M. (2012). Intracortical convergence of layer 6 neurons. Neuroreport 23, 736-740. doi: 10.1097/WNR.0b013e328356c1aa
40. Leone, D. P., Srinivasan, K., Chen, B., Alcamo, E., and McConnell, S. K. (2008). The determination of projection neuron identity in the developing cerebral cortex. Curr. Opin. Neurobiol. 18, 28-35. doi: 10.1016/j.conb.2008.05.006
41. Levesque, M., Charara, A., Gagnon, S., Parent, A., and Deschenes, M. (1996). Corticostriatal projections from layer V cells in rat are collaterals of long-range corticofugal axons. Brain Res. 709, 311-315. doi: 10.1016/0006-8993(95)01333-4
42. Li, L., Tasic, B., Micheva, K. D., Ivanov, V. M., Spletter, M. L., Smith, S. J., et al. (2010). Visualizing the distribution of synapses from individual neurons in the mouse brain. PLoS ONE 5:e11503. doi: 10.1371/journal.pone.0011503
43. Lund, J. S., Yoshioka, T., and Levitt, J. B. (1994). Substrates for interlaminar connections in area V1 of macaque monkey cerebral cortex, in Volume 10 Primary Visual Cortex in Primates, eds A. Peters and K. S. Rockland (New York; London: Plenum Press), 3737-3760. doi: 10.1007/978-1-4757-9628-5_2
44. Luo, L., and O’Leary, D. D. (2005). Axon retraction and degeneration in development and disease. Annu. Rev. Neurosci. 28, 127-156. doi: 10.1146/annurev.neuro.28.061604.135632
45. Masamizu, Y., Tanaka, Y. R., Tanaka, Y. H., Hira, R., Ohkubo, F., Kitamura, K., et al. (2014). Two distinct layer-specific dynamics of cortical ensembles during learning of a motor task. Nat. Neurosci. 17, 987-994. doi: 10.1038/nn.3739
46. Mitchell, B. D., and Macklis, J. D. (2005). Large-scale maintenance of dual projections by callosal and frontal cortical projection neurons in adult mice. J. Comp. Neurol. 482, 17-32. doi: 10.1002/cne.20428
47. Miyoshi, H., Blomer, U., Takahashi, M., Gage, F. H., and Verma, I. M. (1998). Development of a self-inactivating lentivirus vector. J. Virol. 72, 8150-8157.
48. Molnar, Z., and Cheung, A. F. (2006). Towards the classification of subpopulations of layer V pyramidal projection neurons. Neurosci. Res. 55, 105-115. doi: 10.1016/j.neures.2006.02.008
49. Molyneaux, B. J., Arlotta, P., Menezes, J. R., and Macklis, J. D. (2007). Neuronal subtype specification in the cerebral cortex. Nat. Rev. Neurosci. 8, 427-437. doi: 10.1038/nrn2151
50. Morishima, M., and Kawaguchi, Y. (2006). Recurrent connection patterns of corticostriatal pyramidal cells in frontal cortex. J. Neurosci. 26, 4394-4405. doi: 10.1523/JNEUROSCI.0252-06.2006
51. Morishima, M., Morita, K., Kubota, Y., and Kawaguchi, Y. (2011). Highly differentiated projection-specific cortical subnetworks. J. Neurosci. 31, 10380-10391. doi: 10.1523/JNEUROSCI.0772-11.2011
52. Nelson, S. B., Sugino, K., and Hempel, C. M. (2006). The problem of neuronal cell types: a physiological genomics approach. Trends Neurosci. 29, 339-345. doi: 10.1016/j.tins.2006.05.004
53. Olsen, S. R., Bortone, D. S., Adesnik, H., and Scanziani, M. (2012). Gain control by layer six in cortical circuits of vision. Nature 483, 47-52. doi: 10.1038/nature10835
54. Packer, A. M., Roska, B., and Hausser, M. (2013). Targeting neurons and photons for optogenetics. Nat. Neurosci. 16, 805-815. doi: 10.1038/nn.3427
55. Paxinos, G., and Franklin, K. B. J. (2003). The Mouse Brain in Stereotaxic Coordinates: Compact, 2nd Edn. New York, NY: Academic Press.
56. Reiner, A., Hart, N. M., Lei, W., and Deng, Y. (2010). Corticostriatal projection neurons - dichotomous types and dichotomous functions. Front. Neuroanat. 4:142. doi: 10.3389/fnana.2010.00142
57. Rockland, K. S. (2013). Collateral branching of long-distance cortical projections in monkey. J. Comp. Neurol. 521, 4112-4123. doi: 10.1002/cne.23414
58. Rotolo, T., Smallwood, P. M., Williams, J., and Nathans, J. (2008). Genetically-directed, cell type-specific sparse labeling for the analysis of neuronal morphology. PLoS ONE 3:e4099. doi: 10.1371/journal.pone.0004099
59. Rouiller, E. M., and Welker, E. (2000). A comparative analysis of the morphology of corticothalamic projections in mammals. Brain Res. Bull. 53, 727-741. doi: 10.1016/S0361-9230(00)00364-6
60. Sato, T. R., and Svoboda, K. (2010). The functional properties of barrel cortex neurons projecting to the primary motor cortex. J. Neurosci. 30, 4256-4260. doi: 10.1523/JNEUROSCI.3774-09.2010
61. Schmahmann, J., and Pandya, D. (2009). Fiber Pathways of the Brain. Oxford: Oxford University Press.
62. Seidl, A. H. (2013). Regulation of conduction time along axons. Neuroscience 276C, 126-134. doi: 10.1016/j.neuroscience.2013.06.047
63. Sohur, U. S., Padmanabhan, H. K., Kotchetkov, I. S., Menezes, J. R., and Macklis, J. D. (2014). Anatomic and molecular development of corticostriatal projection neurons in mice. Cereb. Cortex 24, 293-303. doi: 10.1093/cercor/bhs342
64. Sorensen, S. A., Bernard, A., Menon, V., Royall, J. J., Glattfelder, K. J., Hirokawa, K., et al. (2013). Correlated gene expression and target specificity demonstrate excitatory projection neuron diversity. Cereb. Cortex. doi: 10.1093/cercor/bht243. [Epub ahead of print].
65. Staiger, J. F., Zilles, K., and Freund, T. F. (1996). Recurrent axon collaterals of corticothalamic projection neurons in rat primary somatosensory cortex contribute to excitatory and inhibitory feedback-loops. Anat. Embryol. (Berl). 194, 533-543. doi: 10.1007/BF00187467
66. Tanaka, Y. R., Tanaka, Y. H., Konno, M., Fujiyama, F., Sonomura, T., Okamoto- Furuta, K., et al. (2011). Local connections of excitatory neurons to corticothalamic neurons in the rat barrel cortex. J. Neurosci. 31, 18223-18236. doi: 10.1523/JNEUROSCI.3139-11.2011
67. Thomson, A. M., and Lamy, C. (2007). Functional maps of neocortical local circuitry. Front. Neurosci. 1, 19-42. doi: 10.3389/neuro.01.1.1.002.2007
68. Tomioka, R., and Rockland, K. S. (2006). Improved Golgi-like visualization in retrogradely projecting neurons after EGFP-adenovirus infection in adult rat and monkey. J. Histochem. Cytochem. 54, 539-548. doi: 10.1369/jhc.5A6838.2005
69. Ueta, Y., Otsuka, T., Morishima, M., Ushimaru, M., and Kawaguchi, Y. (2013). Multiple layer 5 pyramidal cell subtypes relay cortical feedback from secondary to primary motor areas in rats. Cereb. Cortex 24, 2362-2376. doi: 10.1093/cercor/bht088
70. Ugolini, G. (2010). Advances in viral transneuronal tracing. J. Neurosci. Methods 194, 2-20. doi: 10.1016/j.jneumeth.2009.12.001
71. Van Essen, D. C., Anderson, C. H., and Felleman, D. J. (1992). Information processing in the primate visual system: An integrated systems perspective. Science 255, 419-423. doi: 10.1126/science.1734518
72. Veinante, P., and Deschenes, M. (2003). Single-cell study of motor cortex projections to the barrel field in rats. J. Comp. Neurol. 464, 98-103. doi: 10.1002/cne.10769
73. Wang, Q., Henry, A. M., Harris, J. A., Oh, S. W., Joines, K. M., Nyhus, J., et al. (2014). Systematic comparison of adeno-associated virus and biotinylated dextran amine reveals equivalent sensitivity between tracers and novel projection targets in the mouse brain. J. Comp. Neurol. 522, 1989-2012. doi: 10.1002/cne.23567
74. Watakabe, A., Ichinohe, N., Ohsawa, S., Hashikawa, T., Komatsu, Y., Rockland, K. S., et al. (2007). Comparative analysis of layer-specific genes in Mammalian neocortex. Cereb. Cortex 17, 1918-1933. doi: 10.1093/cercor/bhl102
75. Watakabe, A., Kato, S., Kobayashi, K., Takaji, M., Nakagami, Y., Sadakane, O., et al. (2012). Visualization of cortical projection neurons with retrograde TET-off lentiviral vector. PLoS ONE 7:e46157. doi: 10.1371/journal.pone.0046157
76. Wickersham, I. R., Finke, S., Conzelmann, K. K., and Callaway, E. M. (2007). Retrograde neuronal tracing with a deletion-mutant rabies virus. Nat. Methods 4, 47-49. doi: 10.1038/nmeth999
77. Wilson, C. J. (1986). Postsynaptic potentials evoked in spiny neostriatal projection neurons by stimulation of ipsilateral and contralateral neocortex. Brain Res. 367, 201-213. doi: 10.1016/0006-8993(86)91593-3
78. Xu, W., and Sudhof, T. C. (2013). A neural circuit for memory specificity and generalization. Science 339, 1290-1295. doi: 10.1126/science.1229534
79. Yagi, H., Ogura, T., Mizukami, H., Urabe, M., Hamada, H., Yoshikawa, H., et al. (2011). Complete restoration of phenylalanine oxidation in phenylketonuria mouse by a self-complementary adeno-associated virus vector. J. Gene Med. 13, 114-122. doi: 10.1002/jgm.1543
80. Zarrinpar, A., and Callaway, E. M. (2006). Local connections to specific types of layer 6 neurons in the rat visual cortex. J. Neurophysiol. 95, 1751-1761. doi: 10.1152/jn.00974.2005
81. Zhang, Z. W., and Deschenes, M. (1997). Intracortical axonal projections of lamina VI cells of the primary somatosensory cortex in the rat: A single-cell labeling study. J. Neurosci. 17, 6365-6379.