History-dependent excitability as a single-cell substrate of transient memory for information discrimination

PLoS ONE

Volumn 5, Issue 12, 2010, Pages

  Baroni, Fabiano ^a   Torres, Joaquín J ^b   Varona, Pablo ^a  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^b UNIVERSITY OF GRANADA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CELL FUNCTION; CELL TYPE; CONTROLLED STUDY; DISCRIMINATIVE STIMULUS; HISTORY DEPENDENT EXCITABILITY; MATHEMATICAL MODEL; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NERVE EXCITABILITY; NERVE STIMULATION; OSCILLATION; QUANTITATIVE ANALYSIS; SENSITIVITY ANALYSIS; SIGNAL TRANSDUCTION; ACTION POTENTIAL; ANIMAL; ARTIFICIAL NEURAL NETWORK; BIOLOGICAL MODEL; BIOPHYSICS; COMPUTER SIMULATION; HUMAN; MEMORY; METABOLISM; METHODOLOGY; NERVE CELL; OSCILLOMETRY; PHYSIOLOGY; STATISTICAL MODEL; THEORETICAL MODEL; TIME;

ACTION POTENTIALS; ANIMALS; BIOPHYSICS; COMPUTER SIMULATION; HUMANS; LINEAR MODELS; MEMORY; MODELS, NEUROLOGICAL; MODELS, THEORETICAL; NERVE NET; NEURAL NETWORKS (COMPUTER); NEURONS; OSCILLOMETRY; TIME FACTORS;

EID: 78650839708     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0015023     Document Type: Article

References (109)

1. Cooper S, Adrian ED (1923) The frequency of discharge from the spinal cord in the frog. J Physiol 58: 209-229.
2. De Valois RLL, Jacobs GHH, Jones AEE (1962) Effects of increments and decrements of light on neural discharge rate. Science 136: 986-988.
3. Meister M, Lagnado L, Baylor DA (1995) Concerted signaling by retinal ganglion cells. Science 270: 1207-1210.
4. deCharms RC, Merzenich MM (1996) Primary cortical representation of sounds by the coordination of action-potential timing. Nature 381: 610-613.
5. Wehr M, Laurent G (1996) Odour encoding by temporal sequences of firing in oscillating neural assemblies. Nature 384: 162-166.
6. Ikegaya Y, Aaron G, Cossart R, Aronov D, Lampl I, et al. (2004) Synfire chains and cortical songs: temporal modules of cortical activity. Science 304: 559-564.
7. Luczak A, Barthó P, Marguet SL, Buzsáki G, Harris KD (2007) Sequential structure of neocortical spontaneous activity in vivo. Proc Natl Acad Sci U S A 104: 347-352.
8. Mao BQ, Hamzei-Sichani F, Aronov D, Froemke RC, Yuste R (2001) Dynamics of spontaneous activity in neocortical slices. Neuron 32: 883-898.
9. Cossart R, Aronov D, Yuste R (2003) Attractor dynamics of network up states in the neocortex. Nature 423: 283-288.
10. Oram MW, Wiener MC, Lestienne R, Richmond BJ (1999) Stochastic nature of precisely timed spike patterns in visual system neuronal responses. J Neurophysiol 81: 3021-3033.
11. Baker SN, Lemon RN (2000) Precise spatiotemporal repeating patterns in monkey primary and supplementary motor areas occur at chance levels. J Neurophysiol 84: 1770-1780.
12. Johnson HA, Buonomano DV (2007) Development and plasticity of spontaneous activity and up states in cortical organotypic slices. J Neurosci 27: 5915-5925.
13. Ripley SH, Wiersma CA (1953) The effect of spaced stimulation of excitatory and inhibitory axons of the crayfish. Physiol comp et oeco 3: 1-17.
14. Segundo JP, Moore GP, Stensaas LJ, Bullock TH (1963) Sensitivity of neurones in aplysia to temporal pattern of arriving impulses. J Exp Biol 40: 643-667.
15. Wiersma CA, Adams RT (1950) The influence of nerve impulse sequence on the contractions of different crustacean muscles. Physiol comp et oeco 2: 20-33.
16. Zhurov Y, Brezina V (2006) Variability of motor neuron spike timing maintains and shapes contractions of the accessory radula closer muscle of aplysia. J Neurosci 26: 7056-7070.
17. Hooper SL (1998) Transduction of temporal patterns by single neurons. Nat Neurosci 1: 720-726.
18. Abarbanel HD, Talathi SS (2006) Neural circuitry for recognizing interspike interval sequences. Phys Rev Lett 96: 148104.
19. Izhikevich EM, Desai NS, Walcott EC, Hoppensteadt FC (2003) Bursts as a unit of neural information: selective communication via resonance. Trends Neurosci 26: 161-167.
20. Thomson AM, Deuchars J (1994) Temporal and spatial properties of local circuits in neocortex. Trends Neurosci 17: 119-126.
21. 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.
22. Abbott LF, Varela JA, Sen K, Nelson SB (1997) Synaptic depression and cortical gain control. Science 275: 220-224.
23. Zucker RS, Regehr WG (2002) Short-term synaptic plasticity. Annu Rev Physiol 64: 355-405.
24. Kavalali ET (2007) Multiple vesicle recycling pathways in central synapses and their impact on neurotransmission. J Physiol 585: 669-679.
25. Fuhrmann G, Segev I, Markram H, Tsodyks M (2002) Coding of temporal information by activity-dependent synapses. J Neurophysiol 87: 140-148.
26. Kleppe IC, Robinson HP (2006) Correlation entropy of synaptic input-output dynamics. Phys Rev E Stat Nonlin Soft Matter Phys 74: 041909.
27. Zhang W, Linden DJ (2003) The other side of the engram: experience-driven changes in neuronal intrinsic excitability. Nat Rev Neurosci 4: 885-900.
28. Llinás RR (1988) The intrinsic electrophysiological properties of mammalian neurons: insights into central nervous system function. Science 242: 1654-1664.
29. Hutcheon B, Yarom Y (2000) Resonance, oscillation and the intrinsic frequency preferences of neurons. Trends Neurosci 23: 216-222.
30. Buzsáki G (2006) Rhythms of the Brain. USA: Oxford University Press.
31. Richardson MJ, Brunel N, Hakim V (2003) From subthreshold to firing-rate resonance. J Neurophysiol 89: 2538-2554.
32. Schreiber S, Erchova I, Heinemann U, Herz AV (2004) Subthreshold resonance explains the frequency-dependent integration of periodic as well as random stimuli in the entorhinal cortex. J Neurophysiol 92: 408-415.
33. Baroni F, Varona P (2007) Subthreshold oscillations and neuronal input-output relationships. Neurocomputing 70: 1611-1614.
34. Turrigiano GG, Marder E, Abbott LF (1996) Cellular short-term memory from a slow potassium conductance. J Neurophysiol 75: 963-966.
35. Marder E, Abbott LF, Turrigiano G, Liu Z, Golowasch J (1996) Memory from the dynamics of intrinsic membrane currents. Proc Natl Acad Sci U S A 93: 13481-13486.
36. Egorov AV, Hamam BN, Fransén E, Hasselmo ME, Alonso AA (2002) Graded persistent activity in entorhinal cortex neurons. Nature 420: 173-178.
37. Nayak TK, Sikdar SK (2007) Time-dependent molecular memory in single voltage-gated sodium channel. J Membr Biol 219: 19-36.
38. Winograd M, Destexhe A, Sanchez-Vives MV (2008) Hyperpolarizationactivated graded persistent activity in the prefrontal cortex. Proc Natl Acad Sci U S A 105: 7298-7303.
39. Loewenstein Y, Sompolinsky H (2003) Temporal integration by calcium dynamics in a model neuron. Nat Neurosci 6: 961-967.
40. Teramae JN, Fukai T (2005) A cellular mechanism for graded persistent activity in a model neuron and its implications in working memory. J Comput Neurosci 18: 105-121.
41. Seung HS, Lee DD, Reis BY, Tank DW (2000) The autapse: a simple illustration of short-term analog memory storage by tuned synaptic feedback. J Comput Neurosci 9: 171-185.
42. Branco T, Clark BA, Hausser M (2010) Dendritic Discrimination of Temporal Input Sequences in Cortical Neurons. Science 329: 1671-1675.
43. Lapicque L (1907) Recherches quantitatives sur l'excitation electrique des nerfs traitee comme une polarization. J Physiol Pathol Gen 9: 620-635.
44. Hill AV (1936) Excitation and Accommodation in Nerve. Proc R Soc Lond B Biol Sci 119: 305-355.
45. Cole KS (1932) Electric phase angle of cell membranes. J Gen Physiol 15: 641-649.
46. Cole KS (1941) Rectification and inductance in the squid giant axon. J Gen Physiol 25: 29-51.
47. Song S, Sjöström PJ, Reigl M, Nelson S, Chklovskii DB (2005) Highly nonrandom features of synaptic connectivity in local cortical circuits. PLoS Biol 3: e68.
48. Sherman SM, Guillery RW (1998) On the actions that one nerve cell can have on another: distinguishing "drivers" from "modulators". Proc Natl Acad Sci U S A 95: 7121-7126.
49. Lefort S, Tomm C, Floyd Sarria JCC, Petersen CC (2009) The excitatory neuronal network of the c2 barrel column in mouse primary somatosensory cortex. Neuron 61: 301-316.
50. Salinas E, Sejnowski TJ (2001) Correlated neuronal activity and the flow of neural information. Nat Rev Neurosci 2: 539-550.
51. Moreno R, de la Rocha J, Renart A, Parga N (2002) Response of spiking neurons to correlated inputs. Phys Rev Lett 89: 288101.
52. Bruno RM, Sakmann B (2006) Cortex is driven by weak but synchronously active thalamocortical synapses. Science 312: 1622-1627.
53. Shadlen MN, Newsome WT (1998) The variable discharge of cortical neurons: implications for connectivity, computation, and information coding. J Neurosci 18: 3870-3896.
54. Fusi S, Drew PJ, Abbott LF (2005) Cascade models of synaptically stored memories. Neuron 45: 599-611.
55. Gilboa G, Chen R, Brenner N (2005) History-dependent multiple-time-scale dynamics in a single-neuron model. J Neurosci 25: 6479-6489.
56. Anderson RB (2001) The power law as an emergent property. Mem Cognit 29: 1061-1068.
57. Sikström S (2002) Forgetting curves: implications for connectionist models. Cognit Psychol 45: 95-152.
58. Prinz AA, Abbott LF, Marder E (2004) The dynamic clamp comes of age. Trends Neurosci 27: 218-224.
59. Fellous JM, Rudolph M, Destexhe A, Sejnowski TJ (2003) Synaptic background noise controls the input/output characteristics of single cells in an in vitro model of in vivo activity. Neuroscience 122: 811-829.
60. Wolf DM, Fontaine-Bodin L, Bischofs I, Price G, Keasling J, et al. (2008) Memory in microbes: quantifying history-dependent behavior in a bacterium. PLoS ONE 3: e1700.
61. Stern EA, Kincaid AE, Wilson CJ (1997) Spontaneous subthreshold membrane potential fluctuations and action potential variability of rat corticostriatal and striatal neurons in vivo. J Neurophysiol 77: 1697-1715.
62. Lampl I, Reichova I, Ferster D (1999) Synchronous membrane potential fluctuations in neurons of the cat visual cortex. Neuron 22: 361-374.
63. Destexhe A, Rudolph M, Paré D (2003) The high-conductance state of neocortical neurons in vivo. Nat Rev Neurosci 4: 739-751.
64. Fourcaud-Trocmé N, Hansel D, van Vreeswijk C, Brunel N (2003) How spike generation mechanisms determine the neuronal response to fluctuating inputs. J Neurosci 23: 11628-11640.
65. Schaefer AT, Angelo K, Spors H, Margrie TW (2006) Neuronal oscillations enhance stimulus discrimination by ensuring action potential precision. PLoS Biol 4: e163+.
66. Li C, Chen L, Aihara K (2006) Transient resetting: A novel mechanism for synchrony and its biological examples. PLoS Comput Biol 2: e103.
67. Arnold L (2003) Random Dynamical Systems (Springer Monographs in Mathematics). Springer.
68. Tateno T, Pakdaman K (2004) Random dynamics of the morris-lecar neural model. Chaos 14: 511-530.
69. Pakdaman K (2002) The reliability of the stochastic active rotator. Neural Comput 14: 781-792.
70. Legenstein R, Maass W (2007) Edge of chaos and prediction of computational performance for neural circuit models. Neural Netw 20: 323-334.
71. van Vreeswijk C, Sompolinsky H (1996) Chaos in neuronal networks with balanced excitatory and inhibitory activity. Science 274: 1724-1726.
72. Izhikevich EM, Edelman GM (2008) Large-scale model of mammalian thalamocortical systems. Proc Natl Acad Sci U S A 105: 3593-3598.
73. Rudolph M, Pospischil M, Timofeev I, Destexhe A (2007) Inhibition determines membrane potential dynamics and controls action potential generation in awake and sleeping cat cortex. J Neurosci 27: 5280-5290.
74. Saideman SR, Blitz DM, Nusbaum MP (2007) Convergent motor patterns from divergent circuits. J Neurosci 27: 6664-6674.
75. Proekt A, Brezina V, Weiss KR (2004) Dynamical basis of intentions and expectations in a simple neuronal network. Proc Natl Acad Sci U S A 101: 9447-9452.
76. Nadim F, Brezina V, Destexhe A, Linster C (2008) State dependence of network output: Modeling and experiments. J Neurosci 28: 11806-11813.
77. Kintos N, Nusbaum MP, Nadim F (2008) A modeling comparison of projection neuron- and neuromodulator-elicited oscillations in a central pattern generating network. J Comput Neurosci 24: 374-397.
78. Fontanini A, Katz DB (2008) Behavioral states, network states, and sensory response variability. J Neurophysiol 100: 1160-1168.
79. Steriade M (2004) Neocortical cell classes are flexible entities. Nat Rev Neurosci 5: 121-134.
80. Klausberger T, Somogyi P (2008) Neuronal diversity and temporal dynamics: The unity of hippocampal circuit operations. Science 321: 53-57.
81. Wolfe J, Houweling AR, Brecht M (2010) Sparse and powerful cortical spikes. Curr Opin Neurobiol 20: 306-312.
82. Voogd J, Glickstein M (1998) The anatomy of the cerebellum. Trends Neurosci 21: 370-375.
83. Szücs A, Pinto RD, Rabinovich MI, Abarbanel HDI, Selverston AI (2003) Synaptic modulation of the interspike interval signatures of bursting pyloric neurons. J Neurophysiol 89: 1363-1377.
84. Zeck, Gunther M, Masland, Richard H (2007) Spike train signatures of retinal ganglion cell types. Eur J Neurosci 26: 367-380.
85. Latorre R, Rodríguez FB, Varona P (2006) Neural signatures: multiple coding in spiking-bursting cells. Biol Cybern 95: 169-183.
86. Hopfield JJ (1982) Neural networks and physical systems with emergent collective computational abilities. Proc Natl Acad Sci U S A 79: 2554-2558.
87. Quintana J, Fuster JM (1992) Mnemonic and predictive functions of cortical neurons in a memory task. Neuroreport 3: 721-724.
88. Quintana J, Fuster JM (1999) From perception to action: temporal integrative functions of prefrontal and parietal neurons. Cereb Cortex 9: 213-221.
89. Rainer G, Rao SC, Miller EK (1999) Prospective coding for objects in primate prefrontal cortex. J Neurosci 19: 5493-5505.
90. Takeda K, Funahashi S (2002) Prefrontal task-related activity representing visual cue location or saccade direction in spatial working memory tasks. J Neurophysiol 87: 567-588.
91. Baeg EH, Kim YB, Huh K, Mook-Jung I, Kim HT, et al. (2003) Dynamics of population code for working memory in the prefrontal cortex. Neuron 40: 177-188.
92. Scheich H, Ohl FW, Schulze H, Hess A, Brechmann A (2005) 23 Problems in Systems Neuroscience, Oxford University Press, USA, chapter What is reflected in sensory neocortical activity: External stimuli or what the cortex does with them? Computational Neuroscience Series. pp 343-366.
93. Buonomano DVV, Maass W (2009) State-dependent computations: spatiotemporal processing in cortical networks. Nat Rev Neurosci 10: 113-125.
94. Rabinovich MI, Huerta R, Varona P, Afraimovich VS (2008) Transient cognitive dynamics, metastability, and decision making. PLoS Comput Biol 4: e1000072.
95. Rabinovich MI, Varona P, Selverston AI, Abarbanel HDI (2006) Dynamical principles in neuroscience. Rev Mod Phys 78: 1213.
96. Durstewitz D, Deco G (2008) Computational significance of transient dynamics in cortical networks. Eur J Neurosci 27: 217-227.
97. Destexhe A, Contreras D (2006) Neuronal computations with stochastic network states. Science 314: 85-90.
98. Tsuda I (2001) Toward an interpretation of dynamic neural activity in terms of chaotic dynamical systems. Behav Brain Sci 24: 793-810.
99. Maass W, Natschläger T, Markram H (2002) Real-time computing without stable states: a new framework for neural computation based on perturbations. Neural Comput 14: 2531-2560.
100. Buonomano DV (2000) Decoding temporal information: A model based on short-term synaptic plasticity. J Neurosci 20: 1129-1141.
101. Karmarkar UR, Buonomano DV (2007) Timing in the absence of clocks: encoding time in neural network states. Neuron 53: 427-438.
102. Bertschinger N, Natschläger T (2004) Real-time computation at the edge of chaos in recurrent neural networks. Neural Comput 16: 1413-1436.
103. Soltesz I (2005) Diversity in the Neuronal Machine: Order and Variability in Interneuronal Microcircuits. USA: Oxford University Press.
104. Brunel N (2000) Dynamics of sparsely connected networks of excitatory and inhibitory spiking neurons. J Comput Neurosci 8: 183-208.
105. Shamir M, Sompolinsky H (2006) Implications of neuronal diversity on population coding. Neural Comput 18: 1951-1986.
106. Chelaru MI, Dragoi V (2008) Efficient coding in heterogeneous neuronal populations. Proc Natl Acad Sci U S A 105: 16344-16349.
107. White JA, Chow CC, Ritt J, Soto-Treviño C, Kopell N (1998) Synchronization and oscillatory dynamics in heterogeneous, mutually inhibited neurons. J Comput Neurosci 5: 5-16.
108. Baroni F, Varona P (2010) Spike timing-dependent plasticity is affected by the interplay of intrinsic and network oscillations. J Physiol Paris 104: 91-98.
109. Izhikevich EM (2001) Resonate-and-fire neurons. Neural Netw 14: 883-894.