Estimation of thalamocortical and intracortical network models from joint thalamic single-electrode and cortical laminar-electrode recordings in the rat barrel system

PLoS Computational Biology

Volumn 5, Issue 3, 2009, Pages

  Blomquist, Patrick ^a   Devor, Anna ^b,c   Indahl, Ulf G ^a   Ulbert, Istvan ^d,e   Einevoll, Gaute T ^a   Dale, Anders M ^c  

^a NORWEGIAN UNIVERSITY OF LIFE SCIENCES   (Norway)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d INSTITUTE FOR PSYCHOLOGY   (Hungary)

^e PÁZMÁNY PÉTER CATHOLIC UNIVERSITY   (Hungary)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMICAL ACTIVATION; DIFFERENTIAL EQUATIONS; ELECTRODES; INTEGRAL EQUATIONS; POPULATION STATISTICS; STRUCTURAL OPTIMIZATION;

ACTIVATION FUNCTIONS; BARREL SYSTEM; FEED FORWARD; FIRING RATE MODELS; FIRING RATES; LINEAR-PARABOLIC; NETWORK MODELS; SIGNAL TRANSFER; SINGLE ELECTRODE RECORDING; SINGLE ELECTRODES;

RATS;

ANIMAL EXPERIMENT; ARTICLE; BRAIN FUNCTION; BRAIN REGION; CONTROLLED STUDY; MALE; MATHEMATICAL MODEL; NERVE CELL NETWORK; NONHUMAN; RAT; SIGNAL PROCESSING; STIMULUS RESPONSE; THALAMOCORTICAL TRACT; THALAMUS; ANIMAL; BIOLOGICAL MODEL; COMPUTER SIMULATION; ELECTROENCEPHALOGRAPHY; EVOKED SOMATOSENSORY RESPONSE; INNERVATION; INSTRUMENTATION; METHODOLOGY; PHYSIOLOGY; SENSORY NERVE; SOMATOSENSORY CORTEX; TOUCH; VIBRISSA;

RATTUS;

AFFERENT PATHWAYS; ANIMALS; COMPUTER SIMULATION; ELECTROENCEPHALOGRAPHY; EVOKED POTENTIALS, SOMATOSENSORY; MODELS, NEUROLOGICAL; NERVE NET; RATS; SOMATOSENSORY CORTEX; THALAMUS; TOUCH; VIBRISSAE;

EID: 63549111803     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1000328     Document Type: Article

References (76)

1. Wilson HR, Cowan JD (1973) A mathematical theory of the functional dynamics of cortical and thalamic nervous tissue. Kybernetik 13: 55-80.
2. Amari S (1977) Dynamics of pattern formation in lateral-inhibition type neural fields. Biol Cybern 27: 77-87.
3. Deco G, Jirsa VK, Robinson PA, Breakspear M, Friston K (2008) The dynamic brain: From spiking neurons to neural masses and cortical fields. PLOS Comp Biol 4: e1000092. doi:10.1371/journal.pcbi.1000092.
4. Dayan P, Abbott LF (2001) Theoretical Neuroscience: Computational and Mathematical Modeling of Neural Systems. Cambridge MA: MIT Press.
5. Ermentrout B (1998) Neural networks as spatio-temporal pattern-forming systems. Rep Prog Phys 61: 353-430.
6. Coombes S (2005) Waves, bumps, and patterns in neural field theories. Biol Cybern 93: 91-108.
7. Kyriazi HT, Simons DJ (1993) Thalamocortical response transformations in simulated whisker barrels. J Neurosci 13: 1601-1615.
8. Pinto D, Brumberg JC, Simons JC, Ermentrout GB (1996) A quantitative population model of whisker barrels: Re-examining the Wilson-Cowan equations. J Comp Neuroscience 3: 247-264.
9. Pinto DJ, Hartings JA, Brumberg JC, Simons DJ (2003) Cortical damping: analysis of thalamocortical response transformations in rodent barrel cortex. Cereb Cort 13: 33-44.
10. Buzsaki G (2004) Large-scale recording of neuronal ensembles. Nat Neurosci 7: 446-451.
11. Einevoll GT, Pettersen KH, Devor A, Ulbert I, Halgren E, et al. (2007) Laminar Population Analysis: Estimating firing rates and evoked synaptic Activity from multielectrode recordings in rat barrel cortex. J Neurophysiol 97: 2174-2190.
12. Pettersen KH, Hagen E, Einevoll GT (2008) Estimation of population firing rates and current source densities from laminar electrode recordings. J Comp Neurosci 24: 291-313.
13. Pettersen KH, Einevoll GT (2008) Amplitude variability and extracellular lowpass filtering of neuronal spikes. Biophys J 94: 784-802.
14. Nordbø Ø, Wyller J, Einevoll GT (2007) Neural network firing-rate models on integral form: Effects of temporal coupling kernels on equilibrium-state stability. Biol Cybern 97: 195-209.
15. Pinto DJ, Brumberg JC, Simons DJ (2000) Circuit dynamics and coding strategies in rodent somatosensory cortex. J Neurophysiol 83: 1158-1166.
16. Wilent WB, Contreras D (2004) Synaptic responses to whisker deflections in rat barrel cortex as a function of cortical layer and stimulus intensity. J Neurosci 24: 3985-3998.
17. Blomquist P, Indahl UG, Devor A, Ulbert I, Einevoll GT, et al. (2006) Estimation of cortical microcircuit model from joint thalamic single-unit and cortical laminar-electrode recordings in rat whisker-barrel system. Soc Neurosci Abstr 53: 23.
18. Kyriazi HT, Carvell GE, Simons DJ (1994) OFF response transformations in the whisker/barrel system. J Neurophysiol 72: 392-401.
19. Beierlein M, Fall CP, Rinzel J, Yuste R (2002) Thalamocortical bursts trigger recurrent activity in neocortical networks: layer 4 as a frequency-dependent gate. J Neurosci 22: 9885-9894.
20. Feldmeyer D, Egger V, Lübke J, Sakmann B (1999) Reliable synaptic connections between pairs of excitatory layer 4 neurones within a single "barrel" of developing rat somatosensory cortex. J Physiol 521: 169-190.
21. Beierlein M, Gibson JR, Connors BW (2003) Two dynamically distinct inhibitory networks in layer 4 of the neocortex. J Neurophysiol 90: 2987-3000.
22. Swadlow HA, Gusev AG (2002) Receptive-field construction in cortical inhibitory interneurons. Nature Neurosci 5: 403-404.
23. Swadlow HA (2003) Fast-spike interneurons and feedforward inhibition in awake sensory neocortex. Cereb Cort 13: 25-32.
24. Sun Q-Q, Huguenard JR, Prince DA (2006) Barrel cortex microcircuits: thalamocortical feedforward inhibition in spiny stellate cells is mediated by a small number of fast-spiking interneurons. J Neurosci 26: 1219-1230.
25. Temereanca S, Simons DJ (2004) Functional topography of corticothalamic feedback enhances thalamic spatial response tuning in the somatosensory whisker/barrel system. Neuron 41: 639-651.
26. Tateno T, Harsch A, Robinson HPC (2004) Threshold firing frequency-current relationships of neurons in rat somatosensory cortex: Type 1 and type 2 dynamics. J Neurophysiol 92: 2283-2294.
27. Gutenkunst RN, Waterfall JJ, Casey FP, Brown KS, Myers CR, et al. (2007) Universally sloppy parameter sensitivities in systems biology models. PLoS Comp Biol 3: 1871-1878. doi:10.1371/journal.pcbi.0030189.
28. Wyller J, Blomquist P, Einevoll GT (2007) Turing instability and pattern formation in a two-population neuronal network model. Physica D 225: 75-93.
29. Brown KS, Sethna JP (2003) Statistical mechanical approaches to models with many poorly known parameters. Phys Rev E 68: 021904.
30. Oppenheim AW, Willsky AS (1996) Signals and Systems. 2nd ed. Upper Saddle River, New Jersey: Prentice.
31. Bracewell RN (1999) The Fourier transform and its applications. 3rd ed. Columbus, Ohio: McGraw-Hill.
32. Einevoll GT, Plesser HE (2002) Linear mechanistic models for the dorsal lateral geniculate nucleus of cat probed using drifting-grating stimuli. Network: Comp Neur Syst 13: 503-530.
33. Webber RM, Stanley GB (2004) Nonlinear encoding of tactile patterns in the barrel cortex. J Neurophysiol 91: 2010-2022.
34. Petersen CCH, Sakmann B (2001) Functionally independent columns of rat somatosensory barrel cortex revealed with voltage-sensitive dye imaging. J Neurosci 21: 8435-8446.
35. 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 538.3: 803-822.
36. Lübke J, Roth A, Feldmeyer D, Sakmann B (2003) Morphometric analysis of the columnar innervation domain of neurons connection layer 4 and layer 2/3 of juvenile rat barrel cortex. Cereb Cort 13: 1051-1063.
37. Thomson AM, Bannister AP (2003) Interlaminar connections in the neocortex. Cereb Cort 13: 5-14.
38. Helmstaedter M, de Kock CPJ, Feldmeyer D, Bruno RM, Sakmann B (2007) Reconstruction of an average cortical column in silico. Brain Res Rev 55: 193-203.
39. Lübke J, Feldmeyer D (2007) Excitatory signal flow and connectivity in a cortical column: focus on barrel cortex. Brain Struct Funct 212: 3-17.
40. Sarid L, Bruno R, Sakmann B, Segev I, Feldmeyer D (2007) Modeling a layer 4- to-layer 2/3 module of a singe column in rat neocortex: Interweaving in vitro and in vivo experimental observations. Proc Natl Acac Sci U S A 41: 16353-16358.
41. Thomson AM, Lamy C (2007) Functional maps in neocortical local circuitry. Front in Neurosci 1: 19-42.
42. Feldmeyer D, Lübke J, Sakmann B (2006) Efficacy and connectivity of intracolumnar pairs of layer 2/3 pyramidal cells in the barrel cortex of juvenile rats. J Physiol 575.2: 583-602.
43. Feldmeyer D, Roth A, Sakmann B (2005) Monosynaptic connections between pairs of spiny stellate cells in layer 4 and pyramidal cells in layer 5A indicate that lemniscal and paralemniscal afferent pathways converge in the infragranular somatosensory cortex. J Neurosci 25: 3423-3431.
44. Schubert D, Kö tter R, Luhmann HJ, Staiger JF (2006) Morphology, electrophysiology and functional input connectivity of pyramidal neurons characterizes a genuine layer Va in the primary somatosensory cortex. Cereb Cort 16: 223-236.
45. Bruno RM, Sakmann B (2006) Cortex is driven by weak and synchronously active thalamocortical synapses. Science 312: 1622-1627.
46. de Kock CPJ, Bruno RM, Spors H, Sakmann B (2007) Layer- and cell-type specific suprathreshold stimulus representation in rat primary sensory cortex. J Physiol 581: 139-154.
47. Shepherd GMG, Svoboda K (2005) Laminar and columnar organization of ascending excitatory projections to layer 2/3 pyramidal neurons in rat barrel cortex. J Neurosci 25: 5670-5679.
48. Schroeder CE, Lindsley RW, Specht C, Marcovici A, Smiley JF, Javitt DC (2001) Somatosensory input to auditory association cortex in the macaque monkey. J Neurophysiol 85: 1322-1327.
49. Ulbert I, Halgren E, Heit G, Karmos G (2001) Multiple microelectroderecording system for human intracortical applications. J Neurosci Meth 106: 69-79.
50. Covert RF, Scheriber MD, Leff AR, White SR, Munoz NM, et al. (1992) Oxygen metabolism and catecholamine secretion during chloralose anesthesia in lambs. J Dev Physiol 17: 125-132.
51. Lindauer U, Villringer A, Dirnagl U (1993) Characterization of CBF response to somatosensory stimulation: model and influence of anesthetics. Am J Physiol 264: H1223-1228.
52. Ueki M, Mies G, Hossmann KA (1992) Effect of alpha-chloralose, halothane, pentobarbital and nitrous oxide anesthesia on metabolic coupling in somatosensory cortex of rat. Acta Anaesthesiol Scand 36: 318-322.
53. Pinto D, Ermentrout B (2001) Spatially structured activity in synaptically coupled neuronal networks: II Lateral inhibition and standing pulses. SIAM J Appl Math 62: 226-243.
54. Shriki O, Hansel D, Sompolinsky H (2003) Rate models for conductance-based cortical neuronal networks. Neural Comp 15: 1809-1841.
55. Kriener B, Tetzlaff T, Aertsen A, Diesmann M, Rotter S (2008) Correlations and population dynamics in cortical networks. Neural Comp 20: 2133-2184.
56. Petreanu L, Huber D, Sobczyk A, Svoboda K (2007) Channelrhodopsin-2- assisted circuit mapping of long-range callosal projections. Nat Neurosci 10: 663-668.
57. Wise SP, Jones EG (1976) The organization and postnatal development of the commissural projection of the rat somatic sensory cortex. J Comp Neurol 168: 313-343.
58. White EL, DeAmicis RA (1977) Afferent and efferent projections of the region in mouse SmL cortex which contains the posteromedial barrel subfield. J Comp Neurol 175: 455-482.
59. Koralek KA, Olavarria J, Killackey HP (1990) Areal and laminar organization of corticocortical projections in the rat somatosensory cortex. J Comp Neurol 299: 133-150.
60. Li L, Ebner FF (2006) Balancing bilateral sensory activity: callosal processing modulates sensory transmission through the contralateral thalamus by altering the response threshold. Exp Brain Res 172: 397-415.
61. Vogt BA, Gorman AL (1982) Responses of cortical neurons to stimulation of corpus callosum in vitro. J Neurophysiol 48: 1257-1273.
62. Olavarria J, Van Sluyters RC, Killackey HP (1984) Evidence for the complementary organization of callosal and thalamic connections within rat somatosensory cortex. Brain Res 291: 364-368.
63. Derdikman D, Hildesheim R, Ahissar E, Arieli A, Grinvald A (2003) Imaging spatiotemporal dynamics of surround inhibition in the barrels somatosensory cortex. J Neurosci 23: 3100-3105.
64. Devor A, Tian P, Nishimura N, Teng IC, Hillman EM, et al. (2007) Suppressed neuronal activity and concurrent arteriolar vasoconstriction may explain negative blood oxygenation level-dependent signal. J Neurosci 27: 4452-4459.
65. Hlushchuk Y, Hari R (2006) Transient suppression of ipsilateral primary somatosensory cortex during tactile finger stimulation. J Neurosci 26: 5819-5824.
66. Ferbert A, Priori A, Rothwell JC, Day BL, Colebatch JG, et al. (1992) Interhemispheric inhibition of the human motor cortex. J Physiol 453: 525-546.
67. Ogawa S, Lee TM, Stepniski R, Chen W, Zhu XH, et al. (2000) An approach to probe some neural systems interaction by functional MRI at neural time scale down to milliseconds. Proc Natl Acad Sci U S A 97: 11026-11031.
68. Horwitz B, Tagamets MA, McIntosh AR (1999) Neural modeling, functional brain imaging, and cognition. Trends Cogn Sci 3: 91-98.
69. Buchel C, Friston KJ (2000) Assessing interactions among neuronal systems using functional neuroimaging. Neural Networks 13: 871-882 2000.
70. Friston KJ (2005) A theory of cortical responses. Philos Trans R Soc Lond B Biol Sci 360: 815-836.
71. Friston K (2008) Hierarchical models in the brain. PLOS Comp Biol 4: e1000211. doi:10.1371/journal.pcbi.1000211.
72. Dale AM, Sereno MI (1993) Improved localization of cortical activity by combining EEG and MEG with MRI cortical surface reconstruction: a linear approach. J Cog Neurosci 5: 162-176.
73. Dale AM, Halgren E (2001) Spatiotemporal mapping of brain activity by integration of multiple imaging modalities. Curr Opin Neurobiol 11: 202-208.
74. Ahissar E, Sosnik R, Baqdasarian K, Haidarliu S (2001) Temporal frequency of whisker movement. II. Laminar organization of cortical representations. J Neurophysiol 86: 354-367.
75. Dale AM (1999) Optimal experimental design of event-related fMRI. Hum Brain Map 8: 109-114.
76. Cushing JM (1977) Integrodifferential equations and delay models in population dynamics, lecture notes in biomathematics. Heidelberg: Springer.