Cell type-specific three-dimensional structure of thalamocortical circuits in a column of rat vibrissal cortex

Cerebral Cortex

Volumn 22, Issue 10, 2012, Pages 2375-2391

  Oberlaender, Marcel ^a   De Kock, Christiaan P J ^b   Bruno, Randy M ^c   Ramirez, Alejandro ^c   Meyer, Hanno S ^a   Dercksen, Vincent J ^d   Helmstaedter, Moritz ^e   Sakmann, Bert ^a  

^a MAX PLANCK FLORIDA INSTITUTE FOR NEUROSCIENCE   (United States)

^b VU UNIVERSITY AMSTERDAM   (Netherlands)

^c Howard Hughes Medical Institute   (United States)

^d ZUSE INSTITUTE BERLIN   (Germany)

^e MAX PLANCK INSTITUTE FOR MEDICAL RESEARCH   (Germany)

Author keywords

barrel cortex; dendrite morphology; in vivo spiking; neural network; VPM innervation

Indexed keywords

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL STRUCTURE; CELL TYPE; DENDRITE; NERVE FIBER; NEUROANATOMY; NONHUMAN; PRIORITY JOURNAL; RAT; SENSORY NERVE; SYNAPSE; THALAMOCORTICAL TRACT; THREE DIMENSIONAL IMAGING; VIBRISSA;

ANIMALS; NERVE NET; RATS; RATS, WISTAR; SENSORY RECEPTOR CELLS; SOMATOSENSORY CORTEX; THALAMUS; TOUCH; VIBRISSAE;

EID: 84859217557     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhr317     Document Type: Article

References (72)

1. Ankerst M, Breunig M, Kriegel HP, Sander J. 1999. OPTICS: ordering points to identify the clustering structure. In: Delis A, Faloutsous C, Ghandeharizadeh S, editors. ACM SIGMOD'99 International Conference on Management of Data; Philadelphia. (PA): ACM Press. p. 49-60. (Pubitemid 129597323)
2. Binzegger T, Douglas RJ, Martin KA. 2004. A quantitative map of the circuit of cat primary visual cortex. J Neurosci. 24:8441-8453. (Pubitemid 39313766)
3. Bock DD, Lee WC, Kerlin AM, Andermann ML, Hood G, Wetzel AW, Yurgenson S, Soucy ER, Kim HS, Reid RC. 2011. Network anatomy and in vivo physiology of visual cortical neurons. Nature. 471:177-182.
4. Boudewijns ZS, Kleele T, Mansvelder HD, Sakmann B, de Kock CP, Oberlaender M. 2011. Semi-automated three-dimensional reconstructions of individual neurons reveal cell type-specific circuits in cortex. Commun Integr Biol. 4:486-488.
5. Brecht M, Roth A, Sakmann B. 2003. Dynamic receptive fields of reconstructed pyramidal cells in layers 3 and 2 of rat somatosensory barrel cortex. J Physiol. 553:243-265. (Pubitemid 37483932)
6. Brecht M, Sakmann B. 2002a. Dynamic representation of whisker deflection by synaptic potentials in spiny stellate and pyramidal cells in the barrels and septa of layer 4 rat somatosensory cortex. J Physiol. 543:49-70. (Pubitemid 34947296)
7. Brecht M, Sakmann B. 2002b. Whisker maps of neuronal subclasses of the rat ventral posterior medial thalamus, identified by whole-cell voltage recording and morphological reconstruction. J Physiol. 538:495-515. (Pubitemid 35175376)
8. Briggman KL, Helmstaedter M, Denk W. 2011. Wiring specificity in the direction-selectivity circuit of the retina. Nature. 471:183-188.
9. Bruno RM, Sakmann B. 2006. Cortex is driven by weak but synchronously active thalamocortical synapses. Science. 312:1622-1627. (Pubitemid 43902656)
10. Celikel T, Sakmann B. 2007. Sensory integration across space and in time for decision making in the somatosensory system of rodents. Proc Natl Acad Sci U S A. 104:1395-1400. (Pubitemid 46184015)
11. Chen CC, Abrams S, Pinhas A, Brumberg JC. 2009. Morphological heterogeneity of layer VI neurons in mouse barrel cortex. J Comp Neurol. 512:726-746.
12. Constantinople CM, Bruno RM. 2011. Effects and mechanisms of wakefulness on local cortical networks. Neuron. 69:1061-1068.
13. da Costa NM, Martin KA. 2011. How thalamus connects to spiny stellate cells in the cat's visual cortex. J Neurosci. 31:2925-2937.
14. de Kock CP, Bruno RM, Spors H, Sakmann B. 2007. Layer and cell type specific suprathreshold stimulus representation in primary somato-sensory cortex. J Physiol. 581:139-154. (Pubitemid 46712033)
15. de Kock CP, Sakmann B. 2009. Spiking in primary somatosensory cortex during natural whisking in awake head-restrained rats is cell-type specific. Proc Natl Acad Sci U S A. 106:16446-16450.
16. De Paola V, Holtmaat A, Knott G, Song S, Wilbrecht L, Caroni P, Svoboda K. 2006. Cell type-specific structural plasticity of axonal branches and boutons in the adult neocortex. Neuron. 49:861-875. (Pubitemid 43376083)
17. Dercksen VJ, Oberlaender M, Sakmann B, Hege HC. 2012. Forthcoming. Interactive visualization\-a key prerequisite for reconstruction of anatomically realistic neural networks. In: Linsen L, Hagen H, Hamann B, Hege HC, editors. Visualization in Medicine and Life Sciences II. Berlin (Germany): Springer-Verlag.
18. Dercksen VJ, Weber B, Guenther D, Oberlaender M, Prohaska S, Hege HC. 2009. Automatic alignment of stacks of filament data. In: Proceedings of the IEEE International Symposium on Biomedical Imaging: from Nano to Macro (ISBI); 2009 Jun 28-Jul 1; Boston, MA., New York: IEEE. p. 971-974.
19. Deschenes M, Veinante P, Zhang ZW. 1998. The organization of corticothalamic projections: reciprocity versus parity. Brain Res Brain Res Rev. 28:286-308. (Pubitemid 29012676)
20. Egger V, Nevian T, Bruno RM. 2008. Subcolumnar dendritic and axonal organization of spiny stellate and star pyramid neurons within a barrel in rat somatosensory cortex. Cereb Cortex. 18:876-889. (Pubitemid 351398353)
21. Feldmeyer D, Lubke J, Silver RA, Sakmann B. 2002. Synaptic connections between layer 4 spiny neurone-layer 2/3 pyramidal cell pairs in juvenile rat barrel cortex: physiology and anatomy of interlaminar signalling within a cortical column. J Physiol. 538:803-822. (Pubitemid 35190073)
22. Furuta T, Deschenes M, Kaneko T. 2011. Anisotropic distribution of thalamocortical boutons in barrels. J Neurosci. 31:6432-6439.
23. Furuta T, Kaneko T, Deschenes M. 2009. Septal neurons in barrel cortex derive their receptive field input from the lemniscal pathway. J Neurosci. 29:4089-4095.
24. Gonchar Y, Turney S, Price JL, Burkhalter A. 2002. Axo-axonic synapses formed by somatostatin-expressing GABAergic neurons in rat and monkey visual cortex. J Comp Neurol. 443:1-14. (Pubitemid 34027565)
25. Groh A, Meyer HS, Schmidt EF, Heintz N, Sakmann B, Krieger P. 2010. 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.
26. Hattox AM, Nelson SB. 2007. Layer v neurons in mouse cortex projecting to different targets have distinct physiological properties. J Neurophysiol. 98:3330-3340.
27. Helmstaedter M, de Kock CP, Feldmeyer D, Bruno RM, Sakmann B. 2007. Reconstruction of an average cortical column in silico. Brain Res Rev. 55:193-203. (Pubitemid 47538764)
28. Horikawa K, Armstrong WE. 1988. A versatile means of intracellular labeling: injection of biocytin and its detection with avidin conjugates. J Neurosci Methods. 25:1-11.
29. Hubel DH, Wiesel TN. 1959. Receptive fields of single neurones in the cat's striate cortex. J Physiol. 148:574-591.
30. Hutson KA, Masterton RB. 1986. The sensory contribution of a single vibrissa's cortical barrel. J Neurophysiol. 56:1196-1223. (Pubitemid 17174139)
31. Kerr JN, de Kock CP, Greenberg DS, Bruno RM, Sakmann B, Helmchen F. 2007. Spatial organization of neuronal population responses in layer 2/3 of rat barrel cortex. J Neurosci. 27:13316-13328. (Pubitemid 350220486)
32. Kozloski J, Sfyrakis K, Hill S, Schurmann F, Peck C, Markram H. 2008. Identifying, tabulating, and analyzing contacts between branched neuron morphologies. IBM J Res Dev. 52:43-55.
33. Kumar P, Ohana O. 2008. Inter- and intralaminar subcircuits of excitatory and inhibitory neurons in layer 6a of the rat barrel cortex. J Neurophysiol. 100:1909-1922.
34. Land PW, Buffer SA, Jr., Yaskosky JD. 1995. Barreloids in adult rat thalamus: three-dimensional architecture and relationship to somatosensory cortical barrels. J Comp Neurol. 355:573-588.
35. Land PW, Erickson SL. 2005. Subbarrel domains in rat somatosensory (S1) cortex. J Comp Neurol. 490:414-426. (Pubitemid 41232561)
36. Lang S, Dercksen VJ, Sakmann B, Oberlaender M. 2011. Simulation of signal flow in 3D reconstructions of an anatomically realistic neural network in rat vibrissal cortex. Neural Netw. 24:998-1011.
37. Larkman A, 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.
38. Lee S, Carvell GE, Simons DJ. 2008. Motor modulation of afferent somatosensory circuits. Nat Neurosci. 11:1430-1438.
39. Lubke J, Feldmeyer D. 2007. Excitatory signal flow and connectivity in a cortical column: focus on barrel cortex. Brain Struct Funct. 212:3-17. (Pubitemid 47036752)
40. Lubke J, Roth A, Feldmeyer D, Sakmann B. 2003. 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. (Pubitemid 37163204)
41. Manns ID, Sakmann B, Brecht M. 2004. Sub- and suprathreshold receptive field properties of pyramidal neurones in layers 5A and 5B of rat somatosensory barrel cortex. J Physiol. 556:601-622. (Pubitemid 38579010)
42. Margrie TW, Brecht M, Sakmann B. 2002. In vivo, low-resistance, whole-cell recordings from neurons in the anaesthetized and awake mammalian brain. Pflugers Arch. 444:491-498. (Pubitemid 35461792)
43. Markram H. 2006. The blue brain project. Nat Rev Neurosci. 7:153-160. (Pubitemid 43151601)
44. Meyer HS, Schwarz D, Wimmer VC, Schmitt AC, Kerr JN, Sakmann B, Helmstaedter M. 2011. Inhibitory interneurons in a cortical column form hot zones of inhibition in layers 2 and 5A. Proc Natl Acad Sci U S A. 108:16807-16812.
45. Meyer HS, Wimmer VC, Hemberger M, Bruno RM, de Kock CP, Frick A, Sakmann B, Helmstaedter M. 2010. Cell type-specific thalamic innervation in a column of rat vibrissal cortex. Cereb Cortex. 20:2287-2303.
46. Meyer HS, Wimmer VC, Oberlaender M, de Kock CP, Sakmann B, Helmstaedter M. 2010. Number and laminar distribution of neurons in a thalamocortical projection column of rat vibrissal cortex. Cereb Cortex. 20:2277-2286.
47. Mishchenko Y, Hu T, Spacek J, Mendenhall J, Harris KM, Chklovskii DB. 2010. Ultrastructural analysis of hippocampal neuropil from the connectomics perspective. Neuron. 67:1009-1020.
48. Mountcastle VB. 1957. Modality and topographic properties of single neurons of cat's somatic sensory cortex. J Neurophysiol. 20:408-434.
49. O'Connor DH, Peron SP, Huber D, Svoboda K. 2010. Neural activity in barrel cortex underlying vibrissa-based object localization in mice. Neuron. 67:1048-1061.
50. Oberlaender M. 2009. Three-dimensional reengineering of neuronal microcircuits. Combined faculties of the natural sciences and for mathematics. Heidelberg (Germany): University of Heidelberg. p. 145-150.
51. Oberlaender M, Boudewijns ZS, Kleele T, Mansvelder HD, Sakmann B, de Kock CP. 2011. Three-dimensional axon morphologies of individual layer 5 neurons indicate cell type-specific intracortical pathways for whisker motion and touch. Proc Natl Acad Sci U S A. 108:4188-4193.
52. Oberlaender M, Broser PJ, Sakmann B, Hippler S. 2009. Shack-Hartmann wave front measurements in cortical tissue for deconvolution of large three-dimensional mosaic transmitted light brightfield micrographs. J Microsc. 233:275-289.
53. Oberlaender M, Bruno RM, Sakmann B, Broser PJ. 2007. Transmitted light brightfield mosaic microscopy for three-dimensional tracing of single neuron morphology. J Biomed Opt. 12:064029.
54. Oberlaender M, Dercksen VJ, Egger R, Gensel M, Sakmann B, Hege HC. 2009. Automated three-dimensional detection and counting of neuron somata. J Neurosci Methods. 180:147-160.
55. Oberlaender M, Ramirez A, Bruno RM. submitted. Sensory experience restructures thalamocortical axons during adulthood.
56. Peters A. 1979. Thalamic input to the cerebral cortex. Trends Neurosci. 2:1183-1185.
57. Petreanu L, Mao T, Sternson SM, Svoboda K. 2009. The subcellular organization of neocortical excitatory connections. Nature. 457:1142-1145.
58. Pierret T, Lavallee P, Deschenes M. 2000. Parallel streams for the relay of vibrissal information through thalamic barreloids. J Neurosci. 20:7455-7462.
59. Pinault D. 1996. A novel single-cell staining procedure performed in vivo under electrophysiological control: morpho-functional features of juxtacellularly labeled thalamic cells and other central neurons with biocytin or neurobiotin. J Neurosci Methods. 65:113-136.
60. Romand S, Wang Y, Toledo-Rodriguez M, Markram H. 2011. Morphological development of thick-tufted layer v pyramidal cells in the rat somatosensory cortex. Front Neuroanat. 5:5.
61. Staiger JF, Flagmeyer I, Schubert D, Zilles K, Kotter R, Luhmann HJ. 2004. Functional diversity of layer IV spiny neurons in rat somatosensory cortex: quantitative morphology of electrophysiologically characterized and biocytin labeled cells. Cereb Cortex. 14:690-701. (Pubitemid 38669513)
62. Stalling D, Westerhoff M, Hege HC. 2005. Amira: a highly interactive system for visual data analysis. In: Hansen CD, Johnson CR, editors. The visualization handbook. Burlington (MA): Elsevier. p. 749-767.
63. Welker C. 1976. Receptive fields of barrels in the somatosensory neocortex of the rat. J Comp Neurol. 166:173-189.
64. White EL. 1979. Thalamocortical synaptic relations: a review with emphasis on the projections of specific thalamic nuclei to the primary sensory areas of the neocortex. Brain Res. 180:275-311. (Pubitemid 10176084)
65. Wickersham IR, Finke S, Conzelmann KK, Callaway EM. 2007. Retrograde neuronal tracing with a deletion-mutant rabies virus. Nat Methods. 4:47-49. (Pubitemid 46029475)
66. Wickersham IR, Lyon DC, Barnard RJ, Mori T, Finke S, Conzelmann KK, Young JA, Callaway EM. 2007. Monosynaptic restriction of trans-synaptic tracing from single, genetically targeted neurons. Neuron. 53:639-647. (Pubitemid 46283372)
67. Wimmer VC, Bruno RM, de Kock CP, Kuner T, Sakmann B. 2010. Dimensions of a projection column and architecture of VPM and POm axons in rat vibrissal cortex. Cereb Cortex. 20:2265-2276.
68. Wise SP, Jones EG. 1977. Cells of origin and terminal distribution of descending projections of the rat somatic sensory cortex. J Comp Neurol. 175:129-157. (Pubitemid 8164474)
69. Wong-Riley M. 1979. Changes in the visual system of monocularly sutured or enucleated cats demonstrable with cytochrome oxidase histochemistry. Brain Res. 171:11-28. (Pubitemid 9211579)
70. Woolsey TA, Van der Loos H. 1970. The structural organization of layer IV in the somatosensory region (SI) of mouse cerebral cortex. The description of a cortical field composed of discrete cytoarchitec-tonic units. Brain Res. 17:205-242.
71. Yu C, Derdikman D, Haidarliu S, Ahissar E. 2006. Parallel thalamic pathways for whisking and touch signals in the rat. PLoS Biol. 4:e124.
72. Zhang ZW, 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. (Pubitemid 27329909)