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Functional Convergence of Thalamic and Intrinsic Projections to Cortical Layers 4 and 6

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Neurophysiology Aims and scope

An Erratum to this article was published on 01 February 2014

Ascending sensory information is conveyed from the thalamus to layers 4 and 6 of the sensory cortical areas. Interestingly, receptive field properties of cortical layer-6 neurons differ from those in layer 4. Do such differences reflect distinct inheritance patterns from the thalamus, or are they derived instead from local cortical circuits? To distinguish between these possibilities, we utilized in vitro slice preparations containing the thalamo-cortical pathways of the auditory and somatosensory systems. Responses from neurons in layers 4 and 6 that resided in the same column were recorded using whole-cell patch clamp. Laser-scanning photostimulation via uncaging of glutamate in the thalamus and cortex was used to map the functional topography of thalamo-cortical and intracortical inputs to each layer. In addition, we assessed the functional divergence of thalamo-cortical inputs by optical imaging of flavoprotein autofluorescence. We found that the thalamo-cortical inputs to layers 4 and 6 originated from the same thalamic domain, but the intracortical projections to the same neurons differed dramatically. Our results suggest that the intracortical projections, rather than the thalamic inputs, to each layer contribute more to the differences in their receptive field properties.

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References

  1. C. L. Huang and J. A. Winer, “Auditory thalamocortical projections in the cat: laminar and areal patterns of input,” J. Comp. Neurol., 427, 302-331 (2000).

    Article  CAS  PubMed  Google Scholar 

  2. P. H. Smith, D. J. Uhlrich, K. A. Manning, and M. I. Banks, “Thalamocortical projections to rat auditory cortex from the ventral and dorsal divisions of the medial geniculate nucleus.,” J. Comp. Neurol., 520, 34-51 (2012).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  3. P. Landry and M. Deschênes, “Intracortical arborizations and receptive fields of identified ventrobasal thalamocortical afferents to the primary somatic sensory cortex in the cat.,” J. Comp. Neurol., 199, 345-372 (1981).

    Article  CAS  PubMed  Google Scholar 

  4. A. L. Humphrey, M. Sur, D. J. Ulrich, and S. M. Sherman, “Termination patterns of individual X- and Y-cell axons in the visual cortex of the cat: projections to area 18, to the 17/18 border region, and to both areas 17 and 18,” J. Comp. Neurol., 233, 190-212 (1985).

    Article  CAS  PubMed  Google Scholar 

  5. M. Beierlein and B. W. Connors, “Short-term dynamics of thalamocortical and intracortical synapses onto layer 6 neurons in neocortex,” J. Neurophysiol., 88, 1924-1932 (2002).

    PubMed  Google Scholar 

  6. H. J. Rose and R. Metherate, “Auditory thalamocortical transmission is reliable and temporally precise.,” J. Neurophysiol., 94, 2019-2030 (2005).

    Article  PubMed  Google Scholar 

  7. K. J. Stratford, K. Tarczy-Hornoch, K. A. Martin, et al., “Excitatory synaptic inputs to spiny stellate cells in cat visual cortex,” Nature, 382, 258-261 (1996).

    Article  CAS  PubMed  Google Scholar 

  8. J. N. MacLean, V. Fenstermaker, B. O. Watson, and R. Yuste, “A visual thalamocortical slice,” Nat. Methods, 3, 129-134 (2006).

    Article  CAS  PubMed  Google Scholar 

  9. C. C. Lee and S. M. Sherman, “Synaptic properties of thalamic and intracortical intputs to layer 4 of the first- and higher-order cortical areas in the auditory and somatosensory systems.,” J. Neurophysiol., 100, 317-326 (2008).

    Article  PubMed Central  PubMed  Google Scholar 

  10. S. M. Sherman and R. W. Guillery, “On the actions that one nerve cell can have on another: distinguishing ‘drivers’ from ‘modulators’,” Proc. Natl. Acad. Sci. USA, 95, 7121-7126 (1998).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  11. C. C. Lee and S. M. Sherman, “On the classification of pathways in the auditory midbrain, thalamus, and cortex.,” Hear. Res., 276, 79-87 (2011).

    Article  PubMed Central  PubMed  Google Scholar 

  12. C. C. Lee and S. M. Sherman, “Drivers and modulators in the central auditory pathways,” Front. Neurosci., 4, 79-86 (2010).

    Article  PubMed Central  PubMed  Google Scholar 

  13. C. D. Gilbert, “Laminar differences in receptive field properties of cells in cat primary visual cortex,” J. Physiol., 268, 391-421 (1977).

    CAS  PubMed Central  PubMed  Google Scholar 

  14. C. A. Atencio and C. E. Schreiner, “Laminar diversity of dynamic sound processing in cat primary auditory cortex,” J. Neurophysiol., 103, 192-205 (2010).

    Article  PubMed Central  PubMed  Google Scholar 

  15. R. W. Dykes and Y. Lamour, “An electrophysiological study of single somatosensory neurons in rat granular cortex serving the limbs: a laminar analysis,” J. Neurophysiol., 70, 703-724 (1988).

    Google Scholar 

  16. L. M. Martinez, Q. Wang, R. C. Reid, et al., “Receptive field structure varies with layer in the primary visual cortex,” Nat, Neurosci,, 8, 372-379 (2005).

    Article  CAS  Google Scholar 

  17. J. C. Brumberg, D. J. Pinto, and D. J. Simons, “Cortical columnar processing in the rat whisker-to-barrel system,” J. Neurophysiol., 82, 1808-1817 (1999).

    CAS  PubMed  Google Scholar 

  18. M. N. Wallace and A. R. Palmer, “Laminar differences in the response properties of cells in the primary auditory cortex,” Exp Brain Res, 184, 179-191 (2008).

    Article  CAS  PubMed  Google Scholar 

  19. C. C. Lee and J. A. Winer, “Connections of cat auditory cortex: III. Corticocortical system,” J. Comp. Neurol., 507, 1920-1943 (2008).

    Article  PubMed Central  PubMed  Google Scholar 

  20. C. C. Lee and J. A. Winer, “Convergence of thalamic and cortical pathways in cat auditory cortex,” Hear. Res., 274, 85-94 (2011).

    Article  PubMed Central  PubMed  Google Scholar 

  21. C. C. Lee and J. A. Winer, “A synthesis of auditory cortical connections: thalamocortical, commissural, and corticocortical systems,” in: The auditory cortex, J. A. Winer and C. E. Schreiner(eds.), Springer, New York (2011), pp. 147-170.

  22. T. Binzegger, R. Douglas, and K. Martin, “A quantitative map of the circuit of cat primary visual cortex,” J. Neurosci., 24, 8441-8453 (2004).

    Article  CAS  PubMed  Google Scholar 

  23. B. Ahmed, J. C. Anderson, R. J. Douglas, et al., “Polyneuronal innervation of spiny stellate neurons in cat visual cortex,” J. Comp. Neurol., 341, 39-49 (1994).

    Article  CAS  PubMed  Google Scholar 

  24. C. C. Lee and S. M. Sherman, “Modulator property of the intrinsic cortical projections from layer 6 to layer 4,” Front. Syst. Neurosci., 3, 3 (2009).

    Article  PubMed Central  PubMed  Google Scholar 

  25. C. C. Lee and S. M. Sherman, “Intrinsic modulators of auditory thalamocortical transmission,” Hear. Res., 287, 43-50 (2012).

    Article  PubMed Central  PubMed  Google Scholar 

  26. C. C. Lee, Y. W. Lam, and S. M. Sherman, “Intracortical convergence of layer 6 neurons,” Neuroreport, 23, 736-740 (2012).

    Article  PubMed Central  PubMed  Google Scholar 

  27. S. J. Cruikshank, H. J. Rose, and R. Metherate, “Auditory thalamocortical synaptic transmission in vitro,” J. Neurophysiol., 87, 361-384 (2002).

    PubMed  Google Scholar 

  28. A. Agmon and B. W. Connors, “Thalamocortical responses of mouse somatosensory (barrel) cortex in vitro,” Neuroscience, 41, 365-379 (1991).

    Article  CAS  PubMed  Google Scholar 

  29. J. A. Winer and C. C. Lee, “The distributed auditory cortex,” Hear. Res., 229, 3-13 (2007).

    Article  PubMed Central  PubMed  Google Scholar 

  30. J. A. Winer and J. J. Prieto, “Layer V in cat primary auditory cortex (AI): cellular architecture and identification of projection neurons,” J. Comp. Neurol., 434, 379-412 (2001).

    Article  CAS  PubMed  Google Scholar 

  31. C. C. Lee and S. M. Sherman, “Glutamatergic inhibition in sensory neocortex,” Cereb. Cortex, 19, 2281-2289 (2009).

    Article  PubMed Central  PubMed  Google Scholar 

  32. B. A. Suter, T. O’Connor, V. Iyer, et al., “Ephus: multipurpose data acquisition software for neuroscience experiments,” Front. Neural Circuit., 4, 100 (2010).

    Article  Google Scholar 

  33. C. C. Lee and S. M. Sherman, “Topography and physiology of ascending streams in the auditory tectothalamic pathway,” Proc. Natl. Acad. Sci. USA, 107, 372-377 (2010).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  34. B. B. Theyel, D. A. Llano, N. P. Issa, et al., “In vitro imaging using laser photostimulation with flavoprotein autofluorescence.,” Nat. Protoc., 6, 502-508 (2011).

    Article  CAS  PubMed  Google Scholar 

  35. B. B. Theyel, C. C. Lee, and S. M. Sherman, “Specific and nonspecific thalamocortical connectivity in the auditory and somatosensory thalamo-cortical slices,” Neuroreport, 21, 861-864 (2010).

    Article  PubMed Central  PubMed  Google Scholar 

  36. D. A. Llano and S. M. Sherman, “Evidence for non-reciprocal organization of the mouse auditory thalamocortical-corticothalamic projections systems.,” J. Comp. Neurol., 507, 1209-1227 (2008).

    Article  PubMed  Google Scholar 

  37. J. A. Winer, J. J. Diehl, and D. T. Larue, “Projections of auditory cortex to the medial geniculate body of the cat,” J. Comp. Neurol., 430, 27-55 (2001).

    Article  CAS  PubMed  Google Scholar 

  38. I. Reichova and S. M. Sherman, “Somatosensory corticothalamic projections: distinguishing drivers from modulators,” J. Neurophysiol., 92, 2185-2197 (2004).

    Article  PubMed  Google Scholar 

  39. D. H. Sanes and V. C. Kotak, “Developmental plasticity of auditory cortical inhibitory synapses,” Hear. Res., 279, 140-148 (2011).

    Article  PubMed Central  PubMed  Google Scholar 

  40. R. S. Erzurumlu and P. Gaspar, “Development and critical period plasticity of the barrel cortex,” Eur. J. Neurosci., 35, 1540-1553 (2012).

    Article  PubMed Central  PubMed  Google Scholar 

  41. A. M. Oswald and A. D. Reyes, “Development of inhibitory timescales in auditory cortex,” Cereb. Cortex, 21, 1351-1361 (2011).

    Article  PubMed Central  PubMed  Google Scholar 

  42. Y. Zhou, B. H. Liu, G. K. Wu, et al., “Preceding inhibition silences layer 6 neurons in auditory cortex,” Neuron, 65, 706-717 (2010 ).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  43. M. Wehr and A. M. Zador, “Balanced inhibition underlies tuning and sharpens spike timing in auditory cortex,” Nature, 426, 442-446 (2003).

    Article  CAS  PubMed  Google Scholar 

  44. I. Bureau, F. von Saint Paul, and K. Svoboda, “Interdigitated paralemniscal and lemniscal pathways in the mouse barrel cortex.,” PLoS Biol., 4, e382 (2006).

    Article  PubMed Central  PubMed  Google Scholar 

  45. H. V. Oviedo, I. Bureau, K. Svoboda, and A. M. Zador, “The functional asymmetry of auditory cortex is reflected in the organization of local cortical circuits,” Nat. Neurosci., 13, 1413-1420 (2010).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  46. V. C. Wimmer, R. M. Bruno, C. P. de Kock, et al., “Dimensions of a projection column and architecture of VPM and POm axons in rat vibrissal cortex,” Cereb. Cortex, 20, 2265-2276 (2010).

    Article  PubMed Central  PubMed  Google Scholar 

  47. D. A. Llano, B. B. Theyel, A. K. Mallik, et al., “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  PubMed Central  PubMed  Google Scholar 

  48. S. Higashi, M. C. Crair, T. Kurotani, et al., “Altered spatial patterns of functional thalamocortical connections in the barrel cortex after neonatal infraorbital nerve cut revealed by optical recording,” Neuroscience, 91, 439-452 (1999).

    Article  CAS  PubMed  Google Scholar 

  49. N. Laaris, G. C. Carlson, and A. Keller, “Thalamicevoked synaptic interactions in barrel cortex revealed by optical imaging,” J. Neurosci., 20, 1529-1537 (2000).

    CAS  PubMed  Google Scholar 

  50. T. A. Hackett, T. R. Barkat, B. M. O’Brien, et al., “Linking topography to tonotopy in the mouse auditory thalamocortical circuit,” J. Neurosci., 31, 2983-2995 (2011).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  51. R. R. Llinas, E. Leznik, and F. J. Urbano, “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. USA, 99, 449-454 (2002).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  52. M. Beierlein, C. P. Fall, J. Rinzel, and R. Yuste, “Thalamo-cortical bursts trigger recurrent activity in neocortical networks: layer 4 as a frequency-dependent gate,” J. Neurosci., 22, 9885-9894 (2002).

    CAS  PubMed  Google Scholar 

  53. M. Kubota and S. Sugimoto and J. Horikawa, et al., “Optical imaging of dynamic horizontal spread of excitation in rat auditory cortex slices,” Neuosci Lett, 237, 77-80 (1997).

    Article  CAS  Google Scholar 

  54. M. Kubota, M. Nasu, and I. Taniguchi, “Layer-specific horizontal propagation of excitation in the auditory cortex,” Neuroreport, 10, 2865–2867 (1999).

    Article  CAS  PubMed  Google Scholar 

  55. T. Broicher and H. J. Bidmon and B. Kamuf, et al., “Thalamic afferent activation of supragranular layers in auditory cortex in vitro: a voltage sensitive dye study,” Neuroscience, 165, 371-385 (2010).

    Article  CAS  PubMed  Google Scholar 

  56. S. Kaur, H. J. Rose, R. Lazar, et al., “Spectral integration in primary auditory cortex: laminar processing of afferent input, in vivo and in vitro,” Neuroscience, 134, 1033-1045 (2005).

    Article  CAS  PubMed  Google Scholar 

  57. D. Contreras and R. Llinas, “Voltage-sensitive dye imaging of neocortical spatiotemporal dynamics to afferent activation frequency,” J. Neurosci., 21, 9403-9413 (2001).

    CAS  PubMed  Google Scholar 

  58. D. L. Barbour and E. M. Callaway, “Excitatory local connections of superficial neurons in rat auditory cortex,” J. Neurosci., 28, 11174-11185 (2008).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  59. D. A. Llano and S. M. Sherman, “Differences in intrinsic properties and local network connectivity of identified layer 5 and layer 6 adult mouse auditory corticothalamic neurons support a dual corticothalamic projection hypothesis,” Cereb. Cortex, 19, 2810-2826 (2009).

    Article  PubMed Central  PubMed  Google Scholar 

  60. B. M. Hooks, S. A. Hires, Y. X. Zhang, et al., “Laminar analysis of excitatory local circuits in vibrissal motor and sensory cortical areas,” PLoS Biol., 9, e1000572 (2011).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  61. A. Zarrinpar and E. M. Callaway, “Local connections to specific types of layer 6 neurons in the rat visual cortex,” J. Neurophysiol., 95, 1751-1761 (2006).

    Article  PubMed  Google Scholar 

  62. Y. Yoshimura, J. L. Dantzker, and E. M. Callaway, “Excitatory cortical neurons form fine-scale functional networks,” Nature, 433, 868-873 (2005).

    Article  CAS  PubMed  Google Scholar 

  63. F. Briggs and E. M. Callaway, “Layer-specific input to distinct cell types in layer 6 of monkey primary visual cortex,” J. Neurosci., 15, 3600-3608 (2001).

    Google Scholar 

  64. G. M. Shepherd, A. Stepanyants, I. Bureau, et al., “Geometric and functional organization of cortical circuits,” Nat. Neurosci., 8, 782-790 (2005).

    Article  CAS  PubMed  Google Scholar 

  65. G. M. Shepherd, T. A. Pologruto, and K. Svoboda, “Circuit analysis of experience-dependent plasticity in the developing rat barrel cortex,” Neuron, 38, 277-289 (2003).

    Article  CAS  PubMed  Google Scholar 

  66. H. Ojima, C. N. Honda, and E. G. Jones, “Patterns of axon collateralization of identified supragranular pyramidal neurons in the cat auditory cortex,” Cereb. Cortex, 1, 80-94 (1991).

    Article  CAS  PubMed  Google Scholar 

  67. H. Ojima, C. N. Honda, and E. G. Jones, “Characteristics of intracellularly injected infragranular pyramidal neurons in cat primary auditory cortex,” Cereb. Cortex, 2, 197-216 (1992).

    Article  CAS  PubMed  Google Scholar 

  68. J. A. Winer, “Anatomy of layer IV in cat primary auditory cortex (AI),” J. Comp. Neurol., 224, 535-567 (1984).

    Article  CAS  PubMed  Google Scholar 

  69. J. A. Winer, “The non-pyramidal neurons in layer III of cat primary auditory cortex (AI),” J. Comp. Neurol., 229, 512-530 (1984).

    Article  CAS  PubMed  Google Scholar 

  70. J. A. Winer, “The pyramidal cells in layer III of cat primary auditory cortex,” J. Comp. Neurol., 229, 476-496 (1984).

    Article  CAS  PubMed  Google Scholar 

  71. J. J. Prieto and J. A. Winer, “Layer VI in cat primary auditory cortex: Golgi study and sublaminar origins of projection neurons,” J. Comp. Neurol., 404, (1999).

  72. J. A. Winer, L. M. Miller, C. C. Lee, and C. E. Schreiner, “Auditory thalamo-cortical transformation: structure and function,” Trends Neurosci, 28, 255-263 (2005).

    Article  CAS  PubMed  Google Scholar 

  73. L. M. Miller, M. A. Escabí, H. L. Read, and C. E. Schreiner, “Functional convergence of response properties in the auditory thalamo-cortical system,” Neuron, 32, 151-160 (2001).

    Article  CAS  PubMed  Google Scholar 

  74. C. C. Lee and J. A. Winer, “Connections of cat auditory cortex: I. Thalamo-cortical system,” J. Comp. Neurol., 507, 1879-1900 (2008).

    Article  PubMed Central  PubMed  Google Scholar 

  75. J. W. Scannell, C. Blakemore, and M. P. Young, “Analysis of connectivity in the cat cerebral cortex,” J. Neurosci., 15, 1463-1483 (1995).

    CAS  PubMed  Google Scholar 

  76. R. M. Bruno and B. Sakmann, “Cortex is driven by weak but synchronously active thalamo-cortical synapses,” Science, 312, 1622-1627 (2006).

    Article  CAS  PubMed  Google Scholar 

  77. R. J. Douglas, C. Koch, M. Mahowald, et al., “Recurrent excitation in neocortical circuits,” Science, 269, 981-985 (1995).

    Article  CAS  PubMed  Google Scholar 

  78. R. Ben-Yishai, R. L. Bar-Or, and H. Sompolinsky, “Theory of orientation tuning in visual cortex,” Proc. Natl. Acad. Sci. USA, 92, 3844-3848 (1995).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  79. B. H. Liu, G. K. Wu, R. Arbuckle, et al., “Defining cortical frequency tuning with recurrent excitatory circuitry,” Nat. Neurosci., 10, 1594-1600 (2007).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  80. J. N. MacLean, B. O. Watson, G. B. Aaron, and R. Yuste, “Internal dynamics determine the cortical response to thalamic stimulation,” Neuron, 8, 811-823 (2005).

    Article  Google Scholar 

  81. C. R. Stoelzel, Y. Bereshpolova, A. G. Gusev, and H. A. Swadlow, “The impact of an LGNd impulse on the awake visual cortex: synaptic dynamics and the sustained/transient distinction,” J. Neurosci., 28, 5018-5028 (2008).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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  1. Department of Comparative Biomedical Sciences, LSU School of Veterinary Medicine, Baton Rouge, Louisiana, USA

    C. C. Lee & K. Imaizumi

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Lee, C.C., Imaizumi, K. Functional Convergence of Thalamic and Intrinsic Projections to Cortical Layers 4 and 6. Neurophysiology 45, 396–406 (2013). https://doi.org/10.1007/s11062-013-9385-2

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