A disinhibitory circuit mediates motor integration in the somatosensory cortex (original) (raw)

References

  1. Jones, E.G. & Wise, S.P. Size, laminar and columnar distribution of efferent cells in the sensory-motor cortex of monkeys. J. Comp. Neurol. 175, 391–438 (1977).
    Article CAS Google Scholar
  2. White, E.L. & DeAmicis, R.A. Afferent and efferent projections of the region in mouse SmL cortex which contains the posteromedial barrel subfield. J. Comp. Neurol. 175, 455–482 (1977).
    Article CAS Google Scholar
  3. Porter, L.L. & White, E.L. Afferent and efferent pathways of the vibrissal region of primary motor cortex in the mouse. J. Comp. Neurol. 214, 279–289 (1983).
    Article CAS Google Scholar
  4. Donoghue, J.P. & Parham, C. Afferent connections of the lateral agranular field of the rat motor cortex. J. Comp. Neurol. 217, 390–404 (1983).
    Article CAS Google Scholar
  5. Veinante, P. & Deschênes, M. Single-cell study of motor cortex projections to the barrel field in rats. J. Comp. Neurol. 464, 98–103 (2003).
    Article Google Scholar
  6. Kleinfeld, D., Ahissar, E. & Diamond, M.E. Active sensation: insights from the rodent vibrissa sensorimotor system. Curr. Opin. Neurobiol. 16, 435–444 (2006).
    Article CAS Google Scholar
  7. Diamond, M.E., von Heimendahl, M., Knutsen, P.M., Kleinfeld, D. & Ahissar, E. 'Where' and 'what' in the whisker sensorimotor system. Nat. Rev. Neurosci. 9, 601–612 (2008).
    Article CAS Google Scholar
  8. Lee, S., Carvell, G.E. & Simons, D.J. Motor modulation of afferent somatosensory circuits. Nat. Neurosci. 11, 1430–1438 (2008).
    Article CAS Google Scholar
  9. Petreanu, L. et al. Activity in motor-sensory projections reveals distributed coding in somatosensation. Nature 489, 299–303 (2012).
    Article CAS Google Scholar
  10. Xu, N.L. et al. Nonlinear dendritic integration of sensory and motor input during an active sensing task. Nature 492, 247–251 (2012).
    Article CAS Google Scholar
  11. Petreanu, L., Mao, T., Sternson, S.M. & Svoboda, K. The subcellular organization of neocortical excitatory connections. Nature 457, 1142–1145 (2009).
    Article CAS Google Scholar
  12. Hooks, B.M. et al. Laminar analysis of excitatory local circuits in vibrissal motor and sensory cortical areas. PLoS Biol. 9, e1000572 (2011).
    Article CAS Google Scholar
  13. Gentet, L.J., Avermann, M., Matyas, F., Staiger, J.F. & Petersen, C.C. Membrane potential dynamics of GABAergic neurons in the barrel cortex of behaving mice. Neuron 65, 422–435 (2010).
    Article CAS Google Scholar
  14. Gentet, L.J. et al. Unique functional properties of somatostatin-expressing GABAergic neurons in mouse barrel cortex. Nat. Neurosci. 15, 607–612 (2012).
    Article CAS Google Scholar
  15. Lee, S., Hjerling-Leffler, J., Zagha, E., Fishell, G. & Rudy, B. The largest group of superficial neocortical GABAergic interneurons expresses ionotropic serotonin receptors. J. Neurosci. 30, 16796–16808 (2010).
    Article CAS Google Scholar
  16. Rudy, B., Fishell, G., Lee, S. & Hjerling-Leffler, J. Three groups of interneurons account for nearly 100% of neocortical GABAergic neurons. Dev. Neurobiol. 71, 45–61 (2011).
    Article Google Scholar
  17. Kawaguchi, Y. Physiological subgroups of nonpyramidal cells with specific morphological characteristics in layer II/III of rat frontal cortex. J. Neurosci. 15, 2638–2655 (1995).
    Article CAS Google Scholar
  18. Tamás, G., Lorincz, A., Simon, A. & Szabadics, J. Identified sources and targets of slow inhibition in the neocortex. Science 299, 1902–1905 (2003).
    Article Google Scholar
  19. Miyoshi, G. et al. Genetic fate mapping reveals that the caudal ganglionic eminence produces a large and diverse population of superficial cortical interneurons. J. Neurosci. 30, 1582–1594 (2010).
    Article CAS Google Scholar
  20. Porter, J.T. et al. Properties of bipolar VIPergic interneurons and their excitation by pyramidal neurons in the rat neocortex. Eur. J. Neurosci. 10, 3617–3628 (1998).
    Article CAS Google Scholar
  21. Chan, C.H. et al. Emx1 is a marker for pyramidal neurons of the cerebral cortex. Cereb. Cortex 11, 1191–1198 (2001).
    Article CAS Google Scholar
  22. Tsai, H.C. et al. Phasic firing in dopaminergic neurons is sufficient for behavioral conditioning. Science 324, 1080–1084 (2009).
    Article CAS Google Scholar
  23. Dantzker, J.L. & Callaway, E.M. Laminar sources of synaptic input to cortical inhibitory interneurons and pyramidal neurons. Nat. Neurosci. 3, 701–707 (2000).
    Article CAS Google Scholar
  24. Oliva, A.A. Jr., Jiang, M., Lam, T., Smith, K.L. & Swann, J.W. Novel hippocampal interneuronal subtypes identified using transgenic mice that express green fluorescent protein in GABAergic interneurons. J. Neurosci. 20, 3354–3368 (2000).
    Article CAS Google Scholar
  25. Ma, Y., Hu, H., Berrebi, A.S., Mathers, P.H. & Agmon, A. Distinct subtypes of somatostatin containing neocortical interneurons revealed in transgenic mice. J. Neurosci. 26, 5069–5082 (2006).
    Article CAS Google Scholar
  26. Mateo, C. et al. In vivo optogenetic stimulation of neocortical excitatory neurons drives brain-state-dependent inhibition. Curr. Biol. 21, 1593–1602 (2011).
    Article CAS Google Scholar
  27. Gonchar, Y. & Burkhalter, A. Differential subcellular localization of forward and feedback interareal inputs to parvalbumin expressing GABAergic neurons in rat visual cortex. J. Comp. Neurol. 406, 346–360 (1999).
    Article CAS Google Scholar
  28. Dávid, C., Schleicher, A., Zuschratter, W. & Staiger, J.F. The innervation of parvalbumin containing interneurons by VIP-immunopositive interneurons in the primary somatosensory cortex of the adult rat. Eur. J. Neurosci. 25, 2329–2340 (2007).
    Article Google Scholar
  29. Carvell, G.E., Miller, S.A. & Simons, D.J. The relationship of vibrissal motor cortex unit activity to whisking in the awake rat. Somatosens. Mot. Res. 13, 115–127 (1996).
    Article CAS Google Scholar
  30. Huber, D. et al. Multiple dynamic representations in the motor cortex during sensorimotor learning. Nature 484, 473–478 (2012).
    Article CAS Google Scholar
  31. Friedman, W.A., Zeigler, H.P. & Keller, A. Vibrissae motor cortex unit activity during whisking. J. Neurophysiol. 107, 551–563 (2012).
    Article Google Scholar
  32. Crochet, S. & Petersen, C.C. Correlating whisker behavior with membrane potential in barrel cortex of awake mice. Nat. Neurosci. 9, 608–610 (2006).
    Article CAS Google Scholar
  33. Murayama, M. et al. Dendritic encoding of sensory stimuli controlled by deep cortical interneurons. Nature 457, 1137–1141 (2009).
    Article CAS Google Scholar
  34. Larkum, M.E., Zhu, J.J. & Sakmann, B. A new cellular mechanism for coupling inputs arriving at different cortical layers. Nature 398, 338–341 (1999).
    Article CAS Google Scholar
  35. Larkum, M. A cellular mechanism for cortical associations: an organizing principle for the cerebral cortex. Trends Neurosci. 36, 141–151 (2013).
    Article CAS Google Scholar
  36. Williams, S.R. & Stuart, G.J. Mechanisms and consequences of action potential burst firing in rat neocortical pyramidal neurons. J. Physiol. (Lond.) 521, 467–482 (1999).
    Article CAS Google Scholar
  37. Lisman, J.E. Bursts as a unit of neural information: making unreliable synapses reliable. Trends Neurosci. 20, 38–43 (1997).
    Article CAS Google Scholar
  38. Kinnischtzke, A.K., Simons, D.J. & Fanselow, E.E. Motor cortex broadly engages excitatory and inhibitory neurons in somatosensory barrel cortex. Cereb. Cortex published online, 10.1093/cercor/bht085 (31 March 2013).
  39. Fabri, M. & Burton, H. Ipsilateral cortical connections of primary somatic sensory cortex in rats. J. Comp. Neurol. 311, 405–424 (1991).
    Article CAS Google Scholar
  40. Herkenham, M. Laminar organization of thalamic projections to the rat neocortex. Science 207, 532–535 (1980).
    Article CAS Google Scholar
  41. Wimmer, V.C., Bruno, R.M., de Kock, C.P., Kuner, T. & Sakmann, B. Dimensions of a projection column and architecture of VPM and POm axons in rat vibrissal cortex. Cereb. Cortex 20, 2265–2276 (2010).
    Article Google Scholar
  42. Ohno, S. et al. A morphological analysis of thalamocortical axon fibers of rat posterior thalamic nuclei: a single neuron tracing study with viral vectors. Cereb. Cortex 22, 2840–2857 (2012).
    Article Google Scholar
  43. Van der Werf, Y.D., Witter, M.P. & Groenewegen, H.J. The intralaminar and midline nuclei of the thalamus. Anatomical and functional evidence for participation in processes of arousal and awareness. Brain Res. Brain Res. Rev. 39, 107–140 (2002).
    Article Google Scholar
  44. Shirvalkar, P., Seth, M., Schiff, N.D. & Herrera, D.G. Cognitive enhancement with central thalamic electrical stimulation. Proc. Natl. Acad. Sci. USA 103, 17007–17012 (2006).
    Article CAS Google Scholar
  45. Yu, C., Derdikman, D., Haidarliu, S. & Ahissar, E. Parallel thalamic pathways for whisking and touch signals in the rat. PLoS Biol. 4, e124 (2006).
    Article Google Scholar
  46. Kleinfeld, D., Ahissar, E. & Diamond, M.E. Active sensation: insights from the rodent vibrissa sensorimotor system. Curr. Opin. Neurobiol. 16, 435–444 (2006).
    Article CAS Google Scholar
  47. Masri, R., Bezdudnaya, T., Trageser, J.C. & Keller, A. Encoding of stimulus frequency and sensor motion in the posterior medial thalamic nucleus. J. Neurophysiol. 100, 681–689 (2008).
    Article Google Scholar
  48. Cruikshank, S.J. Thalamic control of layer 1 circuits in prefrontal cortex. J. Neurosci. 32, 17813–17823 (2012).
    Article CAS Google Scholar
  49. Jiang, X., Wang, G., Lee, A.J., Stornetta, R.L. & Zhu, J.J. The organization of two new cortical interneuronal circuits. Nat. Neurosci. 16, 210–218 (2013).
    Article CAS Google Scholar
  50. Klausberger, T. & Somogyi, P. Neuronal diversity and temporal dynamics: the unity of hippocampal circuit operations. Science 321, 53–57 (2008).
    Article CAS Google Scholar
  51. Chen-Bee, C.H. et al. Visualizing and quantifying evoked cortical activity assessed with intrinsic signal imaging. J. Neurosci. Methods 97, 157–173 (2000).
    Article CAS Google Scholar
  52. Komai, S., Denk, W., Osten, P., Brecht, M. & Margrie, T.W. Two-photon targeted patching (TPTP) in vivo. Nat. Protoc. 1, 647–652 (2006).
    Article CAS Google Scholar

Download references