Sublayer-specific microcircuits of corticospinal and corticostriatal neurons in motor cortex (original) (raw)

References

  1. Thomson, A.M. & Bannister, A.P. Interlaminar connections in the neocortex. Cereb. Cortex 13, 5–14 (2003).
    Article Google Scholar
  2. Douglas, R.J. & Martin, K.A. Neuronal circuits of the neocortex. Annu. Rev. Neurosci. 27, 419–451 (2004).
    Article CAS Google Scholar
  3. Weiler, N., Wood, L., Yu, J., Solla, S.A. & Shepherd, G.M.G. Top-down laminar organization of the excitatory network in motor cortex. Nat. Neurosci. 11, 360–366 (2008).
    Article CAS Google Scholar
  4. Shepherd, G.M.G. Intracortical cartography in an agranular area. Front. Neurosci. 3, 337–343 (2009).
    Article Google Scholar
  5. Morishima, M. & Kawaguchi, Y. Recurrent connection patterns of corticostriatal pyramidal cells in frontal cortex. J. Neurosci. 26, 4394–4405 (2006).
    Article CAS Google Scholar
  6. Otsuka, T. & Kawaguchi, Y. Firing-pattern-dependent specificity of cortical excitatory feedforward subnetworks. J. Neurosci. 28, 11186–11195 (2008).
    Article CAS Google Scholar
  7. Brown, S.P. & Hestrin, S. Intracortical circuits of pyramidal neurons reflect their long-range axonal targets. Nature 457, 1133–1136 (2009).
    Article CAS Google Scholar
  8. Hattox, A.M. & Nelson, S.B. Layer V neurons in mouse cortex projecting to different targets have distinct physiological properties. J. Neurophysiol. 98, 3330–3340 (2007).
    Article Google Scholar
  9. Miller, M.N., Okaty, B.W. & Nelson, S.B. Region-specific spike-frequency acceleration in layer 5 pyramidal neurons mediated by Kv1 subunits. J. Neurosci. 28, 13716–13726 (2008).
    Article CAS Google Scholar
  10. Stevens, C.F. Neuronal diversity: too many cell types for comfort? Curr. Biol. 8, R708–R710 (1998).
    Article CAS Google Scholar
  11. Nelson, S. Cortical microcircuits: diverse or canonical? Neuron 36, 19–27 (2002).
    Article CAS Google Scholar
  12. Kaneko, T., Cho, R., Li, Y., Nomura, S. & Mizuno, N. Predominant information transfer from layer III pyramidal neurons to corticospinal neurons. J. Comp. Neurol. 423, 52–65 (2000).
    Article CAS Google Scholar
  13. Rathelot, J.A. & Strick, P.L. Subdivisions of primary motor cortex based on cortico-motoneuronal cells. Proc. Natl. Acad. Sci. USA 106, 918–923 (2009).
    Article CAS Google Scholar
  14. Yu, J. et al. Local-circuit phenotypes of layer 5 neurons in motor-frontal cortex of YFP-H mice. Front. Neural Circuits 2, 6 (2008).
    Article Google Scholar
  15. Wilson, C.J. Morphology and synaptic connections of crossed corticostriatal neurons in the rat. J. Comp. Neurol. 263, 567–580 (1987).
    Article CAS Google Scholar
  16. Lévesque, M., Charara, A., Gagnon, S., Parent, A. & Deschêěnes, M. Corticostriatal projections from layer V cells in rat are collaterals of long-range corticofugal axons. Brain Res. 709, 311–315 (1996).
    Article Google Scholar
  17. Reiner, A., Jiao, Y., Del Mar, N., Laverghetta, A.V. & Lei, W.L. Differential morphology of pyramidal tract–type and intratelencephalically projecting–type corticostriatal neurons and their intrastriatal terminals in rats. J. Comp. Neurol. 457, 420–440 (2003).
    Article Google Scholar
  18. Shibuki, K. et al. Dynamic imaging of somatosensory cortical activity in the rat visualized by flavoprotein autofluorescence. J. Physiol. (Lond.) 549, 919–927 (2003).
    Article CAS Google Scholar
  19. Llano, D.A., Theyel, B.B., Mallik, A.K., Sherman, S.M. & Issa, N.P. Rapid and sensitive mapping of long-range connections in vitro using flavoprotein autofluorescence imaging combined with laser photostimulation. J. Neurophysiol. 101, 3325–3340 (2009).
    Article CAS Google Scholar
  20. Mizuno, H., Hirano, T. & Tagawa, Y. Evidence for activity-dependent cortical wiring: formation of interhemispheric connections in neonatal mouse visual cortex requires projection neuron activity. J. Neurosci. 27, 6760–6770 (2007).
    Article CAS Google Scholar
  21. Petreanu, L., Huber, D., Sobczyk, A. & Svoboda, K. Channelrhodopsin-2-assisted circuit mapping of long-range callosal projections. Nat. Neurosci. 10, 663–668 (2007).
    Article CAS Google Scholar
  22. Wang, C.L. et al. Activity-dependent development of callosal projections in the somatosensory cortex. J. Neurosci. 27, 11334–11342 (2007).
    Article CAS Google Scholar
  23. Shepherd, G.M.G., Stepanyants, A., Bureau, I., Chklovskii, D.B. & Svoboda, K. Geometric and functional organization of cortical circuits. Nat. Neurosci. 8, 782–790 (2005).
    Article CAS Google Scholar
  24. Stepanyants, A. & Chklovskii, D.B. Neurogeometry and potential synaptic connectivity. Trends Neurosci. 28, 387–394 (2005).
    Article CAS Google Scholar
  25. Larsen, D.D., Wickersham, I.R. & Callaway, E.M. Retrograde tracing with recombinant rabies virus reveals correlations between projection targets and dendritic architecture in layer 5 of mouse barrel cortex. Front. Neural Circuits 1, 5 (2007).
    PubMed Google Scholar
  26. Groh, A. et al. Cell type–specific properties of pyramidal neurons in neocortex underlying a layout that is modifiable depending on the cortical area. Cereb. Cortex 20, 826–836 (2010).
    Article Google Scholar
  27. Zarrinpar, A. & Callaway, E.M. Local connections to specific types of layer 6 neurons in the rat visual cortex. J. Neurophysiol. 95, 1751–1761 (2006).
    Article Google Scholar
  28. Molyneaux, B.J., Arlotta, P., Menezes, J.R. & Macklis, J.D. Neuronal subtype specification in the cerebral cortex. Nat. Rev. Neurosci. 8, 427–437 (2007).
    Article CAS Google Scholar
  29. Lübke, J., Roth, A., Feldmeyer, D. & Sakmann, B. Morphometric analysis of the columnar innervation domain of neurons connecting layer 4 and layer 2/3 of juvenile rat barrel cortex. Cereb. Cortex 13, 1051–1063 (2003).
    Article Google Scholar
  30. Binzegger, T., Douglas, R.J. & Martin, K.A. A quantitative map of the circuit of cat primary visual cortex. J. Neurosci. 24, 8441–8453 (2004).
    Article CAS Google Scholar
  31. Stepanyants, A. et al. Local potential connectivity in cat primary visual cortex. Cereb. Cortex 18, 13–28 (2008).
    Article Google Scholar
  32. Brown, S.P. & Hestrin, S. Cell-type identity: a key to unlocking the function of neocortical circuits. Curr. Opin. Neurobiol. 19, 415–421 (2009).
    Article CAS Google Scholar
  33. Binzegger, T., Douglas, R.J. & Martin, K.A. Topology and dynamics of the canonical circuit of cat V1. Neural Netw. 22, 1071–1078 (2009).
    Article CAS Google Scholar
  34. Chklovskii, D.B., Mel, B.W. & Svoboda, K. Cortical rewiring and information storage. Nature 431, 782–788 (2004).
    Article CAS Google Scholar
  35. Gao, W.J. & Zheng, Z.H. Target-specific differences in somatodendritic morphology of layer V pyramidal neurons in rat motor cortex. J. Comp. Neurol. 476, 174–185 (2004).
    Article Google Scholar
  36. Gerfen, C.R. The neostriatal mosaic: striatal patch-matrix organization is related to cortical lamination. Science 246, 385–388 (1989).
    Article CAS Google Scholar
  37. Striedter, G.F. Principles of Brain Evolution (Sinauer Associates, Sunderland, Massachusetts, 2005).
  38. Phillips, C.G. & Porter, R. Corticospinal Neurones: their Role in Movement (Academic Press, London, 1977).
  39. Rathelot, J.A. & Strick, P.L. Muscle representation in the macaque motor cortex: an anatomical perspective. Proc. Natl. Acad. Sci. USA 103, 8257–8262 (2006).
    Article CAS Google Scholar
  40. Grinevich, V., Brecht, M. & Osten, P. Monosynaptic pathway from rat vibrissa motor cortex to facial motor neurons revealed by lentivirus-based axonal tracing. J. Neurosci. 25, 8250–8258 (2005).
    Article CAS Google Scholar
  41. Alstermark, B. & Ogawa, J. In vivo recordings of bulbospinal excitation in adult mouse forelimb motoneurons. J. Neurophysiol. 92, 1958–1962 (2004).
    Article Google Scholar
  42. Alstermark, B., Ogawa, J. & Isa, T. Lack of monosynaptic corticomotoneuronal EPSPs in rats: disynaptic EPSPs mediated via reticulospinal neurons and polysynaptic EPSPs via segmental interneurons. J. Neurophysiol. 91, 1832–1839 (2004).
    Article CAS Google Scholar
  43. Li, C.X. & Waters, R.S. Organization of the mouse motor cortex studied by retrograde tracing and intracortical microstimulation (ICMS) mapping. Can. J. Neurol. Sci. 18, 28–38 (1991).
    Article CAS Google Scholar
  44. Ayling, O.G., Harrison, T.C., Boyd, J.D., Goroshkov, A. & Murphy, T.H. Automated light-based mapping of motor cortex by photoactivation of channelrhodopsin-2 transgenic mice. Nat. Methods 6, 219–224 (2009).
    Article CAS Google Scholar
  45. Hazan, J. et al. Spastin, a new AAA protein, is altered in the most frequent form of autosomal dominant spastic paraplegia. Nat. Genet. 23, 296–303 (1999).
    Article CAS Google Scholar
  46. Pasinelli, P. & Brown, R.H. Molecular biology of amyotrophic lateral sclerosis: insights from genetics. Nat. Rev. Neurosci. 7, 710–723 (2006).
    Article CAS Google Scholar
  47. Ballion, B., Mallet, N., Bezard, E., Lanciego, J.L. & Gonon, F. Intratelencephalic corticostriatal neurons equally excite striatonigral and striatopallidal neurons and their discharge activity is selectively reduced in experimental parkinsonism. Eur. J. Neurosci. 27, 2313–2321 (2008).
    Article Google Scholar
  48. Dombeck, D.A., Graziano, M.S. & Tank, D.W. Functional clustering of neurons in motor cortex determined by cellular resolution imaging in awake behaving mice. J. Neurosci. 29, 13751–13760 (2009).
    Article CAS Google Scholar
  49. Cheatwood, J.L., Corwin, J.V. & Reep, R.L. Overlap and interdigitation of cortical and thalamic afferents to dorsocentral striatum in the rat. Brain Res. 1036, 90–100 (2005).
    Article CAS Google Scholar
  50. Wood, L., Gray, N.W., Zhou, Z., Greenberg, M.E. & Shepherd, G.M. Synaptic circuit abnormalities of motor-frontal layer 2/3 pyramidal neurons in an RNA interference model of methyl-CpG–binding protein 2 deficiency. J. Neurosci. 29, 12440–12448 (2009).
    Article CAS Google Scholar

Download references