Intrinsic morphological diversity of thick-tufted layer 5 pyramidal neurons ensures robust and invariant properties of in silico synaptic connections

Journal of Physiology

Volumn 590, Issue 4, 2012, Pages 737-752

  Ramaswamy, Srikanth ^a   Hill, Sean L ^a   King, James G ^a   Schürmann, Felix ^a   Wang, Yun ^b,c   Markram, Henry ^a  

^a EPFL   (Switzerland)

^b TUFTS UNIVERSITY   (United States)

^c WENZHOU MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ALGORITHM; ARTICLE; BRAIN FUNCTION; CELL STRUCTURE; COMPUTER MODEL; COMPUTER SIMULATION; DENDRITE; EXCITATORY POSTSYNAPTIC POTENTIAL; JUVENILE ANIMAL; NEOCORTEX; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NERVE FIBER; NEUROANATOMY; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; SOMATOSENSORY CORTEX; STOCHASTIC MODEL; SYNAPSE; SYNAPTIC TRANSMISSION; THICK TUFTED LAYER 5 PYRAMIDAL NEURON; THREE DIMENSIONAL IMAGING;

ACTION POTENTIALS; ANIMALS; COMPUTER SIMULATION; MODELS, BIOLOGICAL; PYRAMIDAL CELLS; RATS; RATS, WISTAR; SOMATOSENSORY CORTEX; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 84863116366     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2011.219576     Document Type: Article

References (57)

1. Anwar H, Riachi I, Hill S, Schürmann F & Markram H (2009). An approach to capturing neuron morphological diversity. In Computational Neuroscience: Realistic Modeling for Experimentalists, ed. Schutter ED, pp. 211-232. The MIT Press, Cambridge
2. Braitenberg V & Schüz A (1998). In Cortex : Statistics and Geometry of Neuronal Connectivity, ed. Braitenberg V. Springer, London
3. Bush P & Sejnowski T (1996). Inhibition synchronizes sparsely connected cortical neurons within and between columns in realistic network models. J Comput Neurosci 3, 91-110.
4. DeFelipe J & Fariñas I (1992). The pyramidal neuron of the cerebral cortex: morphological and chemical characteristics of the synaptic inputs. Prog Neurobiol 39, 563-607.
5. Del Castillo J & Katz B (1954). Quantal components of the end-plate potential. J Physiol 124, 560-573.
6. Druckmann S, Banitt Y, Gidon A, Schürmann F, Markram H & Segev I (2007). A novel multiple objective optimization framework for constraining conductance-based neuron models by experimental data. Front Neurosci 1, 7-18.
7. Druckmann S, Berger TK, Hill S, Schürmann F, Markram H & Segev (2008). Evaluating automated parameter constraining procedures of neuron models by experimental and surrogate data. Biol Cybern 99, 371-379.
8. Fares T & Stepanyants A (2009). Cooperative synapse formation in the neocortex. Proc Natl Acad Sci U S A 106, 16463-16468.
9. Feldmeyer D, Lübke 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.
10. Fuhrmann G, Segev I, Markram H & Tsodyks M (2002). Coding of temporal information by activity-dependent synapses. J Neurophysiol 87, 140-148.
11. Garcia Alvarez S, Perin R & Markram H (2006). Quantitative analysis of neuron numbers, densities and distributions in the neocortical column. FENS Abstr., vol. 3, A109.15.
12. Gilbert CD & Wiesel TN (1979). Morphology and intracortical projections of functionally characterised neurones in the cat visual cortex. Nature 280, 120-125.
13. Hausser M & Roth A (1997). Estimating the time course of the excitatory synaptic conductance in neocortical pyramidal cells using a novel voltage jump method. J Neurosci 17, 7606-7625.
14. Hay E, Hill S, Schürmann F, Markram H & Segev I (2011). Models of neocortical layer 5b pyramidal cells capturing a wide range of dendritic and perisomatic active properties. PLoS Comput Biol 7, e1002107.
15. Hines ML & Carnevale NT (1997). The NEURON simulation environment. Neural Comput 9, 1179-1209.
16. Jahr CE & Stevens CF (1990). A quantitative description of NMDA receptor-channel kinetic behavior. J Neurosci 10, 1830-1837.
17. Kalisman N, Silberberg G & Markram H (2005). The neocortical microcircuit as a tabula rasa. Proc Natl Acad Sci U S A 102, 880-885.
18. Kasper EM, Lübke J, Larkman AU & Blakemore C (1994). Pyramidal neurons in layer 5 of the rat visual cortex. III. Differential maturation of axon targeting, dendritic morphology, and electrophysiological properties. J Comp Neurol 339, 495-518.
19. Korn H & Faber DS (1991). Quantal analysis and synaptic efficacy in the CNS. Trends Neurosci 14, 439-445.
20. Kozloski J, Sfyrakis K, Hill S, Schürmann F, Peck C & Markram H (2008). Identifying, tabulating, and analyzing contacts between branched neuron morphologies. IBM J Res Dev 52, 43-55.
21. Larkman AU (1991). Dendritic morphology of pyramidal neurones of the visual cortex of the rat: I. Branching patterns. J Comp Neurol 306, 307-319.
22. Larkum ME, Zhu JJ & Sakmann B (1999). A new cellular mechanism for coupling inputs arriving at different cortical layers. Nature 398, 338-341.
23. Le Bé JV & Markram H (2006). Spontaneous and evoked synaptic rewiring in the neonatal neocortex. Proc Natl Acad Sci U S A 103, 13214-13219.
24. Lübke J, Markram H, Frotscher M & Sakmann B (1996). Frequency and dendritic distribution of autapses established by layer 5 pyramidal neurons in the developing rat neocortex: comparison with synaptic innervation of adjacent neurons of the same class. J Neurosci 16, 3209-3218.
25. Lübke 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.
26. Markram H (1997). A network of tufted layer 5 pyramidal neurons. Cereb Cortex 7, 523-533.
27. Markram H (2008). Fixing the location and dimensions of functional neocortical columns. HFSP J 2, 132-135.
28. Markram H, Lübke J, Frotscher M, Roth A & Sakmann B (1997). Physiology and anatomy of synaptic connections between thick tufted pyramidal neurones in the developing rat neocortex. J Physiol 500, 409-440.
29. Meyer HS, Wimmer VC, Oberlaender M, de Cock 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.
30. Mountcastle VB (1997). The columnar organization of the neocortex. Brain 120, 701-722.
31. Myme CI, Sugino K, Turrigiano GG & Nelson SB (2003). The NMDA-to-AMPA ratio at synapses onto layer 2/3 pyramidal neurons is conserved across prefrontal and visual cortices. J Neurophysiol 90, 771-779.
32. Perin R, Berger TK & Markram H (2011). A synaptic organizing principle for cortical neuronal groups. Proc Natl Acad Sci U S A 108, 5419-5424.
33. Peters A (1979). Thalamic input to the cerebral-cortex. Trends Neurosci 2, 183-185.
34. Peters A (1987). Number of neurons and synapses in primary visual cortex. In Cerebral Cortex, ed. Jones EG & Peters A, pp. 267-294. Plenum, New York
35. Petersen CC (2007). The functional organization of the barrel cortex. Neuron 56, 339-355.
36. Rinaldi T, Silberberg G & Markram H (2008). Hyperconnectivity of local neocortical microcircuitry induced by prenatal exposure to valproic acid. Cereb Cortex 18, 763-770.
37. 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, 1-27.
38. Sarid L, Bruno R, Sakmann B, Segev I & Feldmeyer D (2007). Modeling a layer 4-to-layer 2/3 module of a single column in rat neocortex: interweaving in vitro and in vivo experimental observations. Proc Natl Acad Sci U S A 104, 16353-16358.
39. Shepherd GM, Stepanyants A, Bureau I, Chklovskii D & Svoboda K (2005). Geometric and functional organization of cortical circuits. Nat Neurosci 8, 782-790.
40. Silva LR, Amitai Y & Connors BW (1991). Intrinsic oscillations of neocortex generated by layer 5 pyramidal neurons. Science 251, 432-435.
41. Silver RA, Lübke J, Sakmann B & Feldmeyer D (2003). High-probability uniquantal transmission at excitatory synapses in barrel cortex. Science 302, 1981-1984.
42. Simkus CR & Stricker C (2002). Properties of mEPSCs recorded in layer II neurones of rat barrel cortex. J Physiol 545, 509-520.
43. Song S, Sjostrom PJ, Reigl M, Nelson S & Chklovskii DB (2005). Highly nonrandom features of synaptic connectivity in local cortical circuits. PLoS Biol 3, e68.
44. Spruston N (2008). Pyramidal neurons: dendritic structure and synaptic integration. Nat Rev Neurosci 9, 206-221.
45. Stepanyants A & Chklovskii DB (2005). Neurogeometry and potential synaptic connectivity. Trends Neurosci 28, 387-394.
46. Stepanyants A, Hof PR & Chklovskii DB (2002). Geometry and structural plasticity of synaptic connectivity. Neuron 34, 275-288.
47. Stuart G & Sakmann B (1995). Amplification of EPSPs by axosomatic sodium channels in neocortical pyramidal neurons. Neuron 15, 1065-1076.
48. Stuart G, Schiller J & Sakmann B (1997). Action potential initiation and propagation in rat neocortical pyramidal neurons. J Physiol 505, 617-632.
49. Thomson AM & Deuchars J (1994). Temporal and spatial properties of local circuits in neocortex. Trends Neurosci 17, 119-126.
50. Thomson AM, Deuchars J & West DC (1993). Large, deep layer pyramid-pyramid single axon EPSPs in slices of rat motor cortex display paired pulse and frequency-dependent depression, mediated presynaptically and self-facilitation, mediated postsynaptically. J Neurophysiol 70, 2354-2369.
51. Thomson AM, West DC, Wang Y & Bannister AP (2002). Synaptic connections and small circuits involving excitatory and inhibitory neurons in layers 2-5 of adult rat and cat neocortex: triple intracellular recordings and biocytin labelling in vitro. Cereb Cortex 12, 936-953.
52. Traub RD, Miles R & Buzsaki G (1992). Computer simulation of carbachol-driven rhythmic population oscillations in the CA3 region of the in vitro rat hippocampus. J Physiol 451, 653-672.
53. Tsodyks MV & Markram H (1997). The neural code between neocortical pyramidal neurons depends on neurotransmitter release probability. Proc Natl Acad Sci U S A 94, 719-723.
54. Wang Z & McCormick DA (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.
55. Yoshimura Y, Kimura F & Tsumoto T (1999). Estimation of single channel conductance underlying synaptic transmission between pyramidal cells in the visual cortex. Neuroscience 88, 347-352.
56. Yu YC, Bultje RS, Wang X & Shi SH (2009). Specific synapses develop preferentially among sister excitatory neurons in the neocortex. Nature 458, 501-504.
57. 2+ accumulations in dendrites of neocortical pyramidal neurons: an apical band and evidence for two functional compartments. Neuron 13, 23-43.