Retrograde tracing with recombinant rabies virus reveals correlations between projection targets and dendritic architecture in layer 5 of mouse barrel cortex

Frontiers in Neural Circuits

Volumn 1, Issue MAR, 2008, Pages

  Larsen, DeLaine D ^a,b   Wickersham, Ian R ^a,c   Callaway, Edward M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Axonal branching; Barrel cortex; Local circuits; Pyramidal neuron; Rabies virus; Superior colliculus; Thalamus

Indexed keywords

EID: 84890867695     PISSN: 16625110     EISSN: None     Source Type: Journal    
DOI: 10.3389/neuro.04.005.2007     Document Type: Article

References (50)

1. Akemann, W., Zhong, Y. M., Ichinohe, N., Rockland, K. S., and Knopfel, T. (2004). Transgenic mice expressing a fluorescent in vivo label in a distinct subpopulation of neocortical layer 5 pyramidal cells. J. Comp. Neurol. 480, 72-88.
2. Anderson, J. C., Martin, K. A., and Picanco-Diniz, C. W. (1992). The neurons in layer 1 of cat visual cortex. Proc. R. Soc. Lond., B, Biol. Sci. 248, 27-33.
3. 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.
4. Briggs, F., and Callaway, E. M. (2005). Laminar patterns of local excitatory input to layer 5 neurons in macaque primary visual cortex. Cereb. Cortex 15, 479-488.
5. Cauller, L. J., Clancy, B., and Connors, B. W. (1998). Backward cortical projections to primary somatosensory cortex in rats extend long horizontal axons in layer I. J. Comp. Neurol. 390, 297-310.
6. Cetas, J. S., de Venecia, R. K., and McMullen, N. T. (1999). Thalamocortical afferents of Lorente de No: medial geniculate axons that project to primary auditory cortex have collateral branches to layer I. Brain Res. 830, 203-208.
7. Chagnac-Amitai, Y., Luhmann, H. J., and Prince, D. A. (1990). Burst generating and regular spiking layer 5 pyramidal neurons of rat neocortex have different morphological features. J. Comp. Neurol. 296, 598-613.
8. Chu, Z., Galarreta, M., and Hestrin, S. (2003). Synaptic interactions of late-spiking neocortical neurons in layer 1. J. Neurosci. 23, 96-102.
9. Contreras, D. (2004). Electrophysiological classes of neocortical neurons. Neural Netw. 17, 633-646.
10. Dantzker, J. L., and Callaway, E. M. (2000). Laminar sources of synaptic input to cortical inhibitory interneurons and pyramidal neurons. Nat. Neurosci. 3, 701-707.
11. 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.
12. Deuchars, J., West, D. C., and Thomson, A. M. (1994). Relationships between morphology and physiology of pyramid-pyramid single axon connections in rat neocortex in vitro. J. Physiol. 478, 423-435.
13. Feldmeyer, D., and Sakmann, B. (2000). Synaptic efficacy and reliability of excitatory connections between the principal neurones of the input (layer 4) and output layer (layer 5) of the neocortex. J. Physiol. 525, 31-39.
14. Games, K. D., and Winer, J. A. (1988). Layer V in rat auditory cortex: projections to the inferior colliculus and contralateral cortex. Hear. Res. 34, 1-25.
15. Hallman, L. E., Schofield, B. R., and Lin, C. S. (1988). Dendritic morphology and axon collaterals of corticotectal, corticopontine, and callosal neurons in layer V of primary visual cortex of the hooded rat. J. Comp. Neurol. 272, 149-160.
16. Herkenham, M. (1980). Laminar organization of thalamic projections to the rat neocortex. Science 207, 532-535.
17. Hestrin, S., and Armstrong, W. E. (1996). Morphology and physiology of cortical neurons in layer I. J. Neurosci. 16, 5290-5300.
18. Hubener, M., and Bolz, J. (1988). Morphology of identified projection neurons in layer 5 of rat visual cortex. Neurosci. Lett. 94, 76-81.
19. Hubener, M., Schwarz, C., and Bolz, J. (1990). Morphological types of projection neurons in layer 5 of cat visual cortex. J. Comp. Neurol. 301, 655-674.
20. Katz, L. C. (1987). Local circuitry of identified projection neurons in cat visual cortex brain slices. J. Neurosci. 7, 1223-1249.
21. Killackey, H. P., Koralek, K. A., Chiaia, N. L., and Rhodes, R. W. (1989). Laminar and areal differences in the origin of the subcortical projection neurons of the rat somatosensory cortex. J. Comp. Neurol. 282, 428-445.
22. Kim, H. G., and Connors, B. W. (1993). Apical dendrites of the neocortex: correlation between sodium-and calcium-dependent spiking and pyramidal cell morphology. J. Neurosci. 13, 5301-5311.
23. Koester, S. E., and O'Leary, D. D. (1992). Functional classes of cortical projection neurons develop dendritic distinctions by class-specific sculpting of an early common pattern. J. Neurosci. 12, 1382-1393.
24. Larkman, A., and Mason, A. (1990). Correlations between morphology and electrophysiology of pyramidal neurons in slices of rat visual cortex. I. Establishment of cell classes. J. Neurosci. 10, 1407-1414.
25. Larsen, D. D., and Callaway, E. M. (2006). Development of layer-specific axonal arborizations in mouse primary somatosensory cortex. J. Comp. Neurol. 494, 398-414.
26. Llinas, R. R., Leznik, E., and Urbano, F. J. (2002). Temporal binding via cortical coincidence detection of specific and nonspecific thalamocortical inputs: a voltagedependent dye-imaging study in mouse brain slices. Proc. Natl. Acad. Sci. U.S.A. 99, 449-454.
27. Lu, S. M., and Lin, R. C. (1993). Thalamic afferents of the rat barrel cortex: a light-and electron-microscopic study using Phaseolus vulgaris leucoagglutinin as an anterograde tracer. Somatosens. Mot. Res. 10, 1-16.
28. Markram, H. (1997). A network of tufted layer 5 pyramidal neurons. Cereb. Cortex 7, 523-533.
29. Markram, H., Lubke, J., Frotscher, M., Roth, A., and Sakmann, B. (1997). Physiology and anatomy of synaptic connections between thick tufted pyramidal neurones in the developing rat neocortex. J. Physiol. 500, 409-440.
30. Mitchell, B. D., and Cauller, L. J. (2001). Corticocortical and thalamocortical projections to layer I of the frontal neocortex in rats. Brain Res. 921, 68-77.
31. Oda, S., Kishi, K., Yang, J., Chen, S., Yokofujita, J., Igarashi, H., Tanihata, S., and Kuroda, M. (2004). Thalamocortical projection from the ventral posteromedial nucleus sends its collaterals to layer I of the primary somatosensory cortex in rat. Neurosci. Lett. 367, 394-398.
32. Reyes, A., and Sakmann, B. (1999). Developmental switch in the short-term modification of unitary EPSPs evoked in layer 2/3 and layer 5 pyramidal neurons of rat neocortex. J. Neurosci. 19, 3827-3835.
33. Rockland, K. S., and Pandya, D. N. (1979). Laminar origins and terminations of cortical connections of the occipital lobe in the rhesus monkey. Brain Res. 179, 3-20.
34. Schofield, B. R., Hallman, L. E., and Lin, C. S. (1987). Morphology of corticotectal cells in the primary visual cortex of hooded rats. J. Comp. Neurol. 261, 85-97.
35. Schubert, D., Staiger, J. F., Cho, N., Kotter, R., Zilles, K., and Luhmann, H. J. (2001). Layer-specific intracolumnar and transcolumnar functional connectivity of layer V pyramidal cells in rat barrel cortex. J. Neurosci. 21, 3580-3592.
36. Shepherd, G. M., Stepanyants, A., Bureau, I., Chklovskii, D., and Svoboda, K. (2005). Geometric and functional organization of cortical circuits. Nat. Neurosci. 8, 782-790.
37. Shepherd, G. M., and Svoboda, K. (2005). Laminar and columnar organization of ascending excitatory projections to layer 2/3 pyramidal neurons in rat barrel cortex. J. Neurosci. 25, 5670-5679.
38. Silberberg, G., and Markram, H. (2007). Disynaptic inhibition between neocortical pyramidal cells mediated by Martinotti cells. Neuron 53, 735-746.
39. Thomson, A. M., and Bannister, A. P. (1998). Postsynaptic pyramidal target selection by descending layer III pyramidal axons: dual intracellular recordings and biocytin filling in slices of rat neocortex. Neuroscience 84, 669-683.
40. Thomson, A. M., and Deuchars, J. (1997). Synaptic interactions in neocortical local circuits: dual intracellular recordings in vitro. Cereb. Cortex 7, 510-522.
41. Tsiola, A., Hamzei-Sichani, F., Peterlin, Z., and Yuste, R. (2003). Quantitative morphologic classification of layer 5 neurons from mouse primary visual cortex. J. Comp. Neurol. 461, 415-428.
42. Veinante, P., Lavallee, P., and Deschenes, M. (2000). Corticothalamic projections from layer 5 of the vibrissal barrel cortex in the rat. J. Comp. Neurol. 424, 197-204.
43. Wang, Z., and McCormick, D. A. (1993). Control of firing mode of corticotectal and corticopontine layer V burst-generating neurons by norepinephrine, acetylcholine, and 1S,3R-ACPD. J. Neurosci. 13, 2199-2216.
44. Wang, Y., Toledo-Rodriguez, M., Gupta, A., Wu, C., Silberberg, G., Luo, J., and Markram, H. (2004). Anatomical, physiological and molecular properties of Martinotti cells in the somatosensory cortex of the juvenile rat. J. Physiol. 561, 65-90.
45. 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.
46. Winer, J. A., and Larue, D. T. (1989). Populations of GABAergic neurons and axons in layer I of rat auditory cortex. Neuroscience 33, 499-515.
47. Wise, S. P., and Jones, E. G. (1976). The organization and postnatal development of the commissural projection of the rat somatic sensory cortex. J. Comp. Neurol. 168, 313-343.
48. Wise, S. P., and Jones, E. G. (1977). Somatotopic and columnar organization in the corticotectal projection of the rat somatic sensory cortex. Brain Res. 133, 223-235.
49. Wise, S. P., and Jones, E. G. (1978). Developmental studies of thalamocortical and commissural connections in the rat somatic sensory cortex. J. Comp. Neurol. 178, 187-208.
50. Zhou, F. M., and Hablitz, J. J. (1996). Morphological properties of intracellularly labeled layer I neurons in rat neocortex. J. Comp. Neurol. 376, 198-213.