Intrinsic Neuronal Properties Switch the Mode of Information Transmission in Networks

PLoS Computational Biology

Volumn 10, Issue 12, 2014, Pages

  Gjorgjieva, Julijana ^a   Mease, Rebecca A ^b   Moody, William J ^c   Fairhall, Adrienne L ^c  

^a HARVARD UNIVERSITY   (United States)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^c UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOPHYSICS; BRAIN; NETWORK LAYERS;

BIOPHYSICAL PROPERTIES; DEVELOPMENTAL CHANGES; IN NETWORKS; INFORMATION TRANSMISSION; INTRINSIC NEURONAL PROPERTIES; INTRINSIC PROPERTY; ION CHANNEL; NETWORK FUNCTIONS; PROPERTY; SINGLE NEURON;

NEURONS;

ARTICLE; BRAIN CORTEX; BRAIN DEVELOPMENT; CALCULATION; CELL POPULATION; ELECTRIC ACTIVITY; ENTROPY; INFORMATION PROCESSING; MATHEMATICAL MODEL; NERVE CELL; NERVE CELL NETWORK; NEUROTRANSMISSION; PROBABILITY; SYNAPSE; SYNAPTIC TRANSMISSION; ACTION POTENTIAL; ANIMAL; BIOLOGICAL MODEL; BIOLOGY; CYTOLOGY; METABOLISM; PHYSIOLOGY; RAT;

ION CHANNEL;

ACTION POTENTIALS; ANIMALS; CEREBRAL CORTEX; COMPUTATIONAL BIOLOGY; ION CHANNELS; MODELS, NEUROLOGICAL; NERVE NET; NEURONS; RATS; SYNAPTIC TRANSMISSION;

EID: 84919663288     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1003962     Document Type: Article

References (77)

1. Brenner N, Bialek W, de Ruyter van Steveninck R, (2000) Adaptive rescaling maximizes information transmission. Neuron 26: 695–702.
2. Laughlin S, (1981) A simple coding procedure enhances a neuron's information capacity. Zeitschrift für Naturforschung 36C: 910–912.
3. Fairhall AL, Lewen GD, Bialek W, de Ruyter Van Steveninck R, (2001) Efficiency and ambiguity in an adaptive neural code. Nature 412: 787–792.
4. Kim K, Rieke F, (2001) Temporal contrast adaptation in the input and output signals of salamander retinal ganglion cells. J Neurosci 21: 287–99.
5. Nagel K, Doupe A, (2006) Temporal processing and adaptation in the songbird auditory forebrain. Neuron 51: 845–59.
6. Maravall M, Petersen RS, Fairhall AL, Arabzadeh E, Diamond ME, (2007) Shifts in coding properties and maintenance of information transmission during adaptation in barrel cortex. PLoS Biol 5: e19.
7. Wark B, Lundstrom B, Fairhall A, (2007) Sensory adaptation. Curr Opin Neurobiol 17: 423–429.
8. Mease RA, Famulare M, Gjorgjieva J, Moody WJ, Fairhall AL, (2013) Emergence of efficient encoding by single neurons in the developing cortex. J Neurosci 33: 12154–12170.
9. Díaz-Quesada M, Maravall M, (2008) Intrinsic mechanisms for adaptive gain rescaling in barrel cortex. J Neurosci 28: 696–710.
10. Lundstrom BN, Fairhall AL, Maravall M, (2010) Multiple timescale encoding of slowly varying whisker stimulus envelope in cortical and thalamic neurons in vivo. J Neurosci 30: 5071–5077.
11. Ermentrout B, (1998) Linearization of F-I curves by adaptation. Neural Comp 10: 1721–1729.
12. Lischalk JW, Easton CR, Moody WJ, (2009) Bilaterally propagating waves of spontaneous activity arising from discrete pacemakers in the neonatal mouse cerebral cortex. Devel Neurobiol 69: 407–414.
13. Conhaim J, Cedarbaum ER, Barahimi M, Moore JG, Becker MI, et al. (2010) Bimodal septal and cortical triggering and complex propagation patterns of spontaneous waves of activity in the developing mouse cerebral cortex. Devel Neurobiol 70: 679–92.
14. Conhaim J, Easton CR, Becker MI, Barahimi M, Cedarbaum ER, et al. (2011) Developmental changes in propagation patterns and transmitter dependence of waves of spontaneous activity in the mouse cerebral cortex. J Physiol 589: 2529–2541.
15. Ben-Ari Y, (2002) Excitatory actions of GABA during development: the nature of the nurture. Nat Rev Neurosci 3: 728–739.
16. McCabe AK, Easton CR, Lischalk JW, Moody WJ, (2007) Roles of glutamate and GABA receptors in setting the developmental timing of spontaneous synchronized activity in the developing mouse cortex. Dev Neurobiol 67: 1574–1588.
17. Kumar A, Rotter S, Aertsen A, (2010) Spiking activity propagation in neuronal networks: reconciling different perspectives on neural coding. Nat Rev Neurosci 11: 615–627.
18. Hunter I, Korenberg M, (1986) The identification of nonlinear biological systems: Wiener and Hammerstein cascade models. Biol Cybern 55: 135–144.
19. Meister M, Berry MJ, (1999) The neural code of the retina. Neuron 22: 435–450.
20. Chance FS, Abbott L, Reyes AD, (2002) Gain modulation from background synaptic input. Neuron 35: 773–82.
21. Higgs M, Slee S, Spain W, (2006) Diversity of gain modulation by noise in neocortical neurons: regulation by the slow afterhyperpolarization conductance. J Neurosci 26: 8787–99.
22. Corlew R, Bosma MM, Moody WJ, (2004) Spontaneous, synchronous electrical activity in neonatal mouse cortical neurones. J Physiol 560: 377–390.
23. Simoncelli E (2004) Characterization of neural responses with stochastic stimuli. In: Gazzaniga M, editor, The New Cognitive Neurosciences, MIT Press. pp.327–338.
24. Rieke F, Warland D, de Ruyter van Stivenick R, Bialek W (1996) Spikes: Exploring the Neural Code. Cambridge, MA: MIT Press.
25. Wiesenfeld K, Moss F, (1995) Stochastic resonance and the benefits of noise: from ice ages to cray fish and SQUIDs. Nature 373: 33–36.
26. Levin JE, Miller JP, (1996) Broadband neural encoding in the cricket cercal sensory system enchances by stochastic resonance. Nature 380: 165–168.
27. McDonnell MD, Abbott D, (2009) What is stochastic resonance? definitions, misconceptions, debates, and its relevance to biology. PLoS Comp Biol 5: e1000348.
28. Garaschuk O, Hanse E, Konnerth A, (1998) Developmental profile and synaptic origin of early network oscillations in the CA1 region of rat neonatal hippocampus. J Physiol 507: 219–236.
29. Moody WJ, Bosma MM, (2005) Ion channel development, spontaneous activity, and activity-dependent development in nerve and muscle cells. Physiol Rev 85: 883–941.
30. Brody CD, Romo R, Kepecs A, (2003) Basic mechanisms for graded persistent activity: discrete attractors, continuous attractors, and dynamic representations. Curr Opin Neurobiol 13: 204–211.
31. van Rossum MCW, Turrigiano GG, Nelson SB, (2002) Fast propagation of firing rates through layered networks of noisy neurons. J Neurosci 22: 1956–1966.
32. Reyes AD, (2003) Synchrony-dependent propagation of firing rate in iteratively constructed networks in vitro. Nat Neurosci 6: 593–599.
33. Wang S, Wang W, Liu F, (2006) Propagation of firing rate in a feed-forward neuronal network. Phys Rev Lett 96: 018103.
34. Barnett HM, Gjorgjieva J, Weir K, Comfort CE, Fairhall AL, et al. (2014) Relationship between individual neuron and network spontaneous activity in developing mouse cortex. J Neurophysiol [epub ahead of print] doi: 10.1152/jn.00349.2014
35. Abbott LF, Kepler T (1990) Model neurons: From Hodgkin-Huxley to Hopfield. In: Garrido L, editor, Statistical Mechanics of Neural Networks, Springer-Verlag, Berlin. pp.5–18.
36. Cayco-Gajic NA, Shea-Brown E, (2013) Neutral stability, rate propagation, and critical branching in feedforward networks. Neural Comput 25: 1768–1806.
37. Vogels T, Abbott LF, (2005) Signal propagation and logic gating in networks of integrate-and-fire neurons. J Neurosci 25: 10786–10795.
38. Kumar A, Rotter S, Aertsen A, (2008) Conditions for propagating synchronous spiking and asynchronous firing rates in a cortical network model. J Neurosci 20: 5268–5280.
39. Garaschuk O, Linn J, Eilers J, Konnerth A, (2000) Large-scale oscillatory calcium waves in the immature cortex. Nat Neurosci 3: 452–459.
40. Namiki S, Noromoto H, Kobayashi C, Nakatani K, Matsuki N, et al. (2013) Layer III neurons control synchronized waves in the immature cerebral cortex. J Neurosci 33: 987–1001.
41. Blankenship AG, Feller MB, (2010) Mechanisms underlying spontaneous patterned activity in developing neural circuits. Nat Rev Neurosci 11: 18–29.
42. Spitzer NC, (2006) Electrical activity in early neuronal development. Nature 444: 707–712.
43. Watari H, Tose AJ, Bosma MM, (2013) Hyperpolarization of resting membrane potential causes retraction of spontaneous Cai2+ transients during mouse embryonic circuit development. J Physiol 591: 973–983.
44. Diesmann M, Gewaltig MO, Aertsen A, (1999) Stable propagation of synchronous spiking activity in cortical neural networks. Nature 402: 529–533.
45. Shadlen M, Newsome W, (1998) The variable discharge of cortical neurons: implications for connectivity, computation and information coding. J Neurosci 18: 3870–3896.
46. Agüera y Arcas B, Fairhall AL, Bialek W, (2003) Computation in a single neuron: Hodgkin and Huxley revisited. Neural Comput 15: 1715–1749.
47. Hong S, Lundstrom B, Fairhall A, (2008) Intrinsic gain modulation and adaptive neural coding. PLoS Comput Biol 4: e1000119.
48. Barreiro A, Thilo EL, Shea-Brown E, (2012) A-current and type I/type II transition determine collective spiking from common input. J Neurophysiol 108: 1631–1645.
49. Hong S, Ratté S, Prescott S, de Schutter E, (2012) Single neuron firing properties impact correlation-based population coding. J Neurosci 32: 1413–28.
50. Lundstrom B, Hong S, Higgs M, Fairhall A, (2008) Two computational regimes of a single-compartment neuron separated by a planar boundary in conductance space. Neural Comp 20: 1239–1260.
51. Prescott SA, Ratté S, De Koninck Y, Sejnowski TJ, (2006) Nonlinear interaction between shunting and adaptation controls a switch between integration and coincidence detection in pyramidal neurons. J Neurosci 26: 9084–9097.
52. Prescott S, de Koninck Y, Sejnowski T, (2008) Biophysical basis for three distinct dynamical mechanisms of action potential initiation. PLoS Comput Biol 4: e1000198.
53. Ratté S, Hong S, De Schutter E, Prescott S, (2013) Impact of neuronal properties on network coding: Roles of spike initiation dynamics and robust synchrony transfer. Neuron 78: 758–772.
54. Yazdanbakhsh A, Babadi B, Rouhani S, Arabzadeh E, Abbassi A, (2002) New attractor states for synchronous activity in synfire chains with excitatory and inhibitory coupling. Biol Cybern 86: 367–378.
55. Litvak V, Sompolinsky H, Segev I, Abeles M, (2003) On the transmission of rate code in long feedforward networks with excitatory-inhibitory balance. J Neurosci 23: 3006–3015.
56. de la Rocha J, Doiron B, Shea-Brown E, Josić K, Reyes A, (2007) Correlation between neural spike trains increases with firing rate. Nature 448: 802–806.
57. Nowotny T, Huerta R, (2003) Explaining synchrony in feed-forward networks. Biol Cybern 89: 237–241.
58. Mehring C, Hehl U, Kubo M, Diesmann M, Aertsen A, (2003) Activty dynamics and propagation of synchronous spiking in locally connected random networks. Biol Cybern 88: 395–408.
59. Marsálek P, Koch C, Maunsell J, (1997) On the relationship between synaptic input and spike output jitter in individual neurons. Proc Natl Acad Sci USA 94: 735–740.
60. Burkitt AN, Clark GM, (1999) Analysis of integrate-and-fire neurons: synchronization of synaptic input and spike output. Neural Comput 11: 871–901.
61. Sanchez-Vives MV, McCormick DA, (2000) Cellular and network mechanisms of rhythmic recurrent activity in neocortex. Nat Neurosci 3: 1027–1034.
62. Rubino D, Robbins KA, Hatsopoulos NG, (2006) Propagating waves mediate information transfer in the motor cortex. Nat Neurosci 9: 1549–1557.
63. Luczak A, Barthó P, Marguet SL, G GB, Harris KD, (2007) Sequential structure of neocortical spontaneous activity in vivo. Proc Natl Sci 104: 347–352.
64. Chauvette S, Seigneur J, Timofeev I, (2012) Sleep oscillations in the thalamocortical system induce long-term neuronal plasticity. Neuron 75: 1105–1113.
65. Vyazovskiy VV, Cirelli C, Pfister-Genskow M, Faraguna U, Tononi G, (2008) Molecular and electrophysiological evidence for net synaptic potentiation in wake and depression in sleep. Nat Neurosci 11: 200–208.
66. Hille B (2001) Ion Channels of Excitable Membranes. Sunderland, MA: Sinauer Associates, Inc.
67. Sah P, Faber ES, (2002) Channels underlying neuronal calcium-activated potassium current. Prog Neurobiol 66: 345–353.
68. Mease RA, Lee S, Moritz AT, Powers RK, Binder MD, et al. (2014) Context-dependent coding in single neurons. J Comp Neurosci DOI 10.1007/s10827-014-0513-9
69. Miles GB, Dai Y, Brownstone RM, (2005) Mechanisms underlying the early phase of spike frequency adaptation in mouse spinal motoneurones. J Physiol 566: 519–532.
70. Kim KJ, Rieke F, (2003) Slow Na+ inactivation and variance adaptation in salamander retinal ganglion cells. J Neurosci 23: 1506–1516.
71. Lundstrom B, Higgs M, Spain WJ, Fairhall A, (2008) Fractional differentiation by neocortical pyramidal neurons. Nat Neurosci 11: 1335–1342.
72. Brockmann MD, Poöschel, Cichon N, Hanganu-Opatz IL, (2011) Coupled oscillations mediate directed interactions between prefrontal cortex and hippocampus of the neonatal rat. Neuron 71: 332–347.
73. Minlebaev M, Colonnese M, Tsintsadze T, Sirota A, Khazipov R, (2011) Early gamma oscillations synchronize developing thalamus and cortex. Science 334: 226–229.
74. Colonnese MT, Kaminska A, Minlebaev M, Milh M, Bloem B, et al. (2010) A conserved switch in sensory processing prepares developing neocortex for vision. Neuron 67: 480–498.
75. Mainen ZF, Joerges J, Huguenard JR, Sejnowski TJ, (1995) A model of spike initiation in neocortical pyramidal neurons. Neuron 15: 1427–1439.
76. Risken H (1996) The Fokker-Planck equation: materials and methods of solution and applications. Berlin, Germany: Springer.
77. Borst A, Theunissen FE, (1999) Information theory and neural coding. Nat Neurosci 2: 947–957.