Sub- and suprathreshold adaptation currents have opposite effects on frequency tuning

Journal of Physiology

Volumn 590, Issue 19, 2012, Pages 4839-4858

  Deemyad, Tara ^a   Kroeger, Jens ^a   Chacron, Maurice J ^a  

^a MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM CHANNEL; POTASSIUM CHANNEL KCNQ;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CALCIUM CURRENT; CELLULAR DISTRIBUTION; CHANNEL GATING; COMPUTER ANALYSIS; COMPUTER PREDICTION; CONTROLLED STUDY; EVOLUTIONARY ADAPTATION; FEMALE; FREQUENCY MODULATION; MALE; MATHEMATICAL MODEL; NERVE CELL PLASTICITY; NERVE CELL STIMULATION; NEUROTRANSMISSION; NONHUMAN; PERCEPTIVE THRESHOLD; POTASSIUM CURRENT; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PYRAMIDAL NERVE CELL; SPIKE WAVE; STIMULUS RESPONSE;

ADAPTATION, PHYSIOLOGICAL; ALKANES; ANIMALS; ANTHRACENES; FEMALE; FISHES; KCNQ POTASSIUM CHANNELS; MALE; MODELS, NEUROLOGICAL; POTASSIUM CHANNEL BLOCKERS; POTASSIUM CHANNELS, CALCIUM-ACTIVATED; PYRAMIDAL CELLS; QUINOLINIUM COMPOUNDS;

EID: 84866878418     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2012.234401     Document Type: Article

References (105)

1. Adams PR, Brown DA & Constanti A (1982). Pharmacological inhibition of the M-current. J Physiol 332, 223-262.
2. Adorjan P, Piepenbrock C & Obermayer K (1999). Contrast adaptation and infomax in visual cortical neurons. Rev Neurosci 10, 181-200.
3. Avila Akerberg O & Chacron MJ (2011). In vivo conditions influence the coding of stimulus features by bursts of action potentials. J Comput Neurosci 31, 369-383.
4. Barlow HB (1961). Possible principles underlying the transformation of sensory messages. In Sensory Communication, ed. Rosenblith W. MIT Press, Cambridge, MA, USA.
5. Bastian J, Chacron MJ & Maler L (2002). Receptive field organization determines pyramidal cell stimulus-encoding capability and spatial stimulus selectivity. J Neurosci 22, 4577-4590.
6. Bell C & Maler L (2005). Central neuroanatomy of electrosensory systems in fish. In Electroreception, ed. Bullock TH, Hopkins CD, Popper AN & Fay RR, pp. 68-111. Springer, New York.
7. Benda J & Hennig RM (2008). Spike-frequency adaptation generates intensity invariance in a primary auditory interneuron. J Computat Neurosci 24, 113-136.
8. Benda J & Herz AV (2003). A universal model for spike-frequency adaptation. Neural Computation 15, 2523-2564.
9. Benda J, Longtin A & Maler L (2005). Spike-frequency adaptation separates transient communication signals from background oscillations. J Neurosci 25, 2312-2321.
10. Berman NJ & Maler L (1998). Distal versus proximal inhibitory shaping of feedback excitation in the electrosensory lateral line lobe: implications for sensory filtering. J Neurophysiol 80, 3214-3232.
11. Borst A & Theunissen F (1999). Information theory and neural coding. Nat Neurosci 2, 947-957.
12. Brenner N, Bialek W & de Ruyter van Steveninck R (2000). Adaptive rescaling maximizes information transmission. Neuron 26, 695-702.
13. Brette R & Gerstner W (2005). Adaptive exponential integrate-and-fire model as an effective description of neuronal activity. J Neurophysiol 94, 3637-3642.
14. Brunel N, Hakim V & Richardson MJ (2003). Firing-rate resonance in a generalized integrate-and-fire neuron with subthreshold resonance. Phys Rev E Stat Nonlin Soft Matter Phys 67, 051916.
15. Carr CE & Maler L (1986). Electroreception in gymnotiform fish. Central anatomy and physiology. In Electroreception, ed. Bullock TH & Heiligenberg W, pp. 319-373. Wiley, New York.
16. Chacron MJ, Doiron B, Maler L, Longtin A & Bastian J (2003a). Non-classical receptive field mediates switch in a sensory neuron's frequency tuning. Nature 423, 77-81.
17. Chacron MJ, Longtin A & Maler L (2001a). Negative interspike interval correlations increase the neuronal capacity for encoding time-varying stimuli. J Neurosci 21, 5328-5343.
18. Chacron MJ, Longtin A & Maler L (2001b). Simple models of bursting and non-bursting electroreceptors. Neurocomputing 38, 129-139.
19. Chacron MJ, Longtin A & Maler L (2003b). The effects of spontaneous activity, background noise, and the stimulus ensemble on information transfer in neurons. Network 14, 803-824.
20. Chacron MJ, Longtin A & Maler L (2005a). Delayed excitatory and inhibitory feedback shape neural information transmission. Phys Rev E Stat Nonlin Soft Matter Phys 72, 051917.
21. Chacron MJ, Longtin A & Maler L (2011). Efficient computation via sparse coding in electrosensory neural networks. Curr Opin Neurobiol 21, 752-760.
22. Chacron MJ, Maler L & Bastian J (2005b). Electroreceptor neuron dynamics shape information transmission. Nat Neurosci 8, 673-678.
23. Chance FS, Nelson SB & Abbott LF (1998). Synaptic depression and the temporal response characteristics of V1 cells. J Neurosci 18, 4785-4799.
24. Deemyad T, Maler L & Chacron MJ (2011). Inhibition of SK and M channel mediated currents by 5-HT enables parallel processing by bursts and isolated spikes. J Neurophysiol 105, 1276-1294.
25. Destexhe A, Rudolph M & Pare D (2003). The high-conductance state of neocortical neurons in vivo. Nat Rev Neurosci 4, 739-751.
26. Dragoi V, Sharma J, Miller EK & Sur M (2002). Dynamics of neuronal sensitivity in visual cortex and local feature discrimination. Nat Neurosci 5, 883-891.
27. Ellis LD, Krahe R, Bourque CW, Dunn RJ & Chacron MJ (2007a). Muscarinic receptors control frequency tuning through the downregulation of an A-type potassium current. J Neurophysiol 98, 1526-1537.
28. Ellis LD, Maler L & Dunn RJ (2008). Differential distribution of SK channel subtypes in the brain of the weakly electric fish Apteronotus leptorhynchus. J Com Neurol 507, 1964-1978.
29. Ellis LD, Mehaffey WH, Harvey-Girard E, Turner RW, Maler L & Dunn RJ (2007b). SK channels provide a novel mechanism for the control of frequency tuning in electrosensory neurons. J Neurosci 27, 9491-9502.
30. Ermentrout B, Pascal M & Gutkin B (2001). The effects of spike frequency adaptation and negative feedback on the synchronization of neural oscillators. Neural Comput 13, 1285-1310.
31. Faber ES & Sah P (2003). Calcium-activated potassium channels: multiple contributions to neuronal function. Neuroscientist 9, 181-194.
32. Faber ESL & Sah P (2002). Physiological role of calcium-activated potassium currents in the rat lateral amygdala. J Neurosci 22, 1618-1628.
33. Fairhall AL, Lewen GD, Bialek W & de Ruyter van Steveninck RR (2001). Efficiency and ambiguity in an adaptive neural code. Nature 412, 787-792.
34. French AS, Hoger U, Sekizawa S & Torkkeli PH (2001). Frequency response functions and information capacities of paired spider mechanoreceptor neurons. Biol Cybern 85, 293-300.
35. Fuhrmann G, Segev I, Markram H & Tsodyks M (2002). Coding of temporal information by activity-dependent synapses. J Neurophysiol 87, 140-148.
36. Gabbiani F, Krapp HG, Hatsopoulos N, Mo CH, Koch C & Laurent G (2004). Multiplication and stimulus invariance in a looming-sensitive neuron. J Physiol (Paris) 98, 19-34.
37. Gelfand S (2004). Hearing: An Introduction to Psychological and Physiological Acoustics. Informa Healthcare, Colchester.
38. Glantz RM & Schroeter JP (2004). Analysis and simulation of gain control and precision in crayfish visual interneurons. J Neurophysiol 92, 2747-2761.
39. + channels to hyperpolarizing after-potentials and discharge pattern in rat supraoptic neurones. J Neuroendocrinol 16, 577-588.
40. Gu N, Hu H, Vervaeke K & Storm JF (2008). SK (KCa2) channels do not control somatic excitability in CA1 pyramidal neurons but can be activated by dendritic excitatory synapses and regulate their impact. J Neurophysiol 100, 2589-2604.
41. Guan D, Higgs MH, Horton LR, Spain WJ & Foehring RC (2011). Contributions of Kv7-mediated potassium current to sub- and suprathreshold responses of rat layer II/III neocortical pyramidal neurons. J Neurophysiol 106, 1722-1733.
42. Halliwell JV & Adams PR (1982). Voltage-clamp analysis of muscarinic excitation in hippocampal neurons. Brain research 250, 71-92.
43. Hallworth NE, Wilson CJ & Bevan MD (2003). Apamin-sensitive small conductance calcium-activated potassium channels, through their selective coupling to voltage-gated calcium channels, are critical determinants of the precision, pace, and pattern of action potential generation in rat subthalamic nucleus neurons in vitro. J Neurosci 23, 7525-7542.
44. Hitschfeld ÉM, Stamper SA, Vonderschen K, Fortune ES & Chacron MJ (2009). Effects of restraint and immobilization on electrosensory behaviors of weakly electric fish. ILAR J 50, 361-372.
45. Kawasaki M (2005). Central neuroanatomy of electrosensory systems in fish. In Electroreception, ed. Bullock TH, Hopkins CD, Popper AN & Fay RR, pp. 154-194. Springer, New York.
46. Koyama S & Appel SB (2006). Characterization of M-current in ventral tegmental area dopamine neurons. J Neurophysiol 96, 535-543.
47. Krahe R, Bastian J & Chacron MJ (2008). Temporal processing across multiple topographic maps in the electrosensory system. J Neurophysiol 100, 852-867.
48. Laughlin SB (1989). The role of sensory adaptation in the retina. J Exp Biol 146, 39-62.
49. Lindner B, Gangloff D, Longtin A & Lewis JE (2009). Broadband coding with dynamic synapses. J Neurosci 29, 2076-2087.
50. Lindner B, Schimansky-Geier L & Longtin A (2002). Maximizing spike train coherence or incoherence in the leaky integrate-and-fire model. Phys Rev E Stat Nonlin Soft Matter Phys 66, 031916.
51. Livingstone MS & Hubel DH (1987). Psychophysical evidence for separate channels for the perception of form, color, movement, and depth. J Neurosci 7, 3416-3468.
52. Madamba SG, Schweitzer P & Siggins GR (1999). Dynorphin selectively augments the M-current in hippocampal CA1 neurons by an opiate receptor mechanism. J Neurophysiol 82, 1768-1775.
53. Maler L (1979). The posterior lateral line lobe of certain gymnotiform fish. Quantitative light microscopy. J Comp Neurol 183, 323-363.
54. Maler L (2009). Receptive field organization across multiple electrosensory maps. I. Columnar organization and estimation of receptive field size. J Comp Neurol 516, 376-393.
55. Maler L, Sas EK & Rogers J (1981). The cytology of the posterior lateral line lobe of high frequency weakly electric fish (Gymnotidae): Differentiation and synaptic specificity in a simple cortex. J Comp Neurol 195, 87-139.
56. 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.
57. Marr D (1982). Vision. Freeman, New York.
58. Mathieson WB & Maler L (1988). Morphological and electrophysiological properties of a novel in vitro preparation: the electrosensory lateral line lobe brain slice. J Comp Physiol A 163, 489-506.
59. McGillivray P, Vonderschen K, Fortune ES & Chacron MJ (2012). Parallel coding of first and second order stimulus attributes by midbrain electrosensory neurons. J Neurosci 32, 5510-5524.
60. Mehaffey WH, Doiron B, Maler L & Turner RW (2005). Deterministic multiplicative gain control with active dendrites. J Neurosci 25, 9968-9977.
61. Mehaffey WH, Ellis LD, Krahe R, Dunn RJ & Chacron MJ (2008a). Ionic and neuromodulatory regulation of burst discharge controls frequency tuning. J Physiol (Paris) 102, 195-208.
62. Mehaffey WH, Maler L & Turner RW (2008b). Intrinsic frequency tuning in ELL pyramidal cells varies across electrosensory maps. J Neurophysiol 99, 2641-2655.
63. Merigan WH & Maunsell JH (1993). How parallel are the primate visual pathways? Annu Rev Neurosci 16, 369-402.
64. Muller JR, Metha AB, Krauskopf J & Lennie P (1999). Rapid adaptation in visual cortex to the structure of images. Science 285, 1405-1408.
65. Naud R, Marcille N, Clopath C & Gerstner W (2008). Firing patterns in the adaptive exponential integrate-and-fire model. Biol Cybernet 99, 335-347.
66. Nelson ME & MacIver MA (1999). Prey capture in the weakly electric fish Apteronotus albifrons: sensory acquisition strategies and electrosensory consequences. J Exp Biol 202, 1195-1203.
67. Nelson ME, Xu Z & Payne JR (1997). Characterization and modeling of P-type electrosensory afferent responses to amplitude modulations in a wave-type electric fish. J Comp Physiol A 181, 532-544.
68. Oertel D (1999). The role of timing in the brain stem auditory nuclei of vertebrates. Annu Rev Physiol 61, 497-519.
69. Oswald AMM, Chacron MJ, Doiron B, Bastian J & Maler L (2004). Parallel processing of sensory input by bursts and isolated spikes. J Neurosci 24, 4351-4362.
70. Park TJ, Klug A, Holinstat M & Grothe B (2004). Interaural level difference processing in the lateral superior olive and the inferior colliculus. J Neurophysiol 92, 289-301.
71. AHP and modulates the firing properties of hippocampal pyramidal neurons. J Biol Chem 280, 41404-41411.
72. Peron S & Gabbiani F (2009a). Spike frequency adaptation mediates looming stimulus selectivity in a collision-detecting neuron. Nat Neurosci 12, 318-326.
73. Peron SP & Gabbiani F (2009b). Role of spike-frequency adaptation in shaping neuronal response to dynamic stimuli. Biol Cybernet 100, 505-520.
74. + channels determines cholinergic action on firing properties of basolateral amygdala projection neurons. J Neurosci 28, 3209-3220.
75. Prescott SA & Sejnowski TJ (2008). Spike-rate coding and spike-time coding are affected oppositely by different adaptation mechanisms. J Neurosci 28, 13649-13661.
76. Prole DL, Lima PA & Marrion NV (2003). Mechanisms underlying modulation of neuronal KCNQ2/KCNQ3 potassium channels by extracellular protons. J Gen Physiol 122, 775-793.
77. Regev N, Degani-Katzav N, Korngreen A, Etzioni A, Siloni S, Alaimo A, Chikvashvili D, Villarroel A, Attali B & Lotan I (2009). Selective interaction of syntaxin 1A with KCNQ2: possible implications for specific modulation of presynaptic activity. PLoS One 4, e6586.
78. Richardson MJ, Brunel N & Hakim V (2003). From subthreshold to firing-rate resonance. J Neurophysiol 89, 2538-2554.
79. Rieke F, Warland D, de Ruyter van Steveninck RR & Bialek W (1996). Spikes: Exploring the Neural Code. MIT Press, Cambridge, MA, USA.
80. Sadeghi SG, Chacron MJ, Taylor MC & Cullen KE (2007). Neural variability, detection thresholds, and information transmission in the vestibular system. J Neurosci 27, 771-781.
81. Sah P & Faber ES (2002). Channels underlying neuronal calcium-activated potassium currents. Prog Neurobiol 66, 345-353.
82. Santini E & Porter JT (2010). M-type potassium channels modulate the intrinsic excitability of infralimbic neurons and regulate fear expression and extinction. J Neurosci 30, 12379-12386.
83. Schneider AD, Cullen KE & Chacron MJ (2011). In vivo conditions induce faithful encoding of stimuli by reducing nonlinear synchronization in vestibular sensory neurons. PLoS Comp Biol 7, e1002120.
84. Shah MM, Mistry M, Marsh SJ, Brown DA & Delmas P (2002). Molecular correlates of the M-current in cultured rat hippocampal neurons. J Physiol 544, 29-37.
85. Sharpee TO, Sugihara H, Kurgansky AV, Rebrik SP, Stryker MP & Miller KD (2006). Adaptive filtering enhances information transmission in visual cortex. Nature 439, 936-942.
86. Smith MR, Nelson AB & Du Lac S (2002). Regulation of firing response gain by calcium-dependent mechanisms in vestibular nucleus neurons. J Neurophysiol 87, 2031-2042.
87. 2+ dynamics in a cricket auditory neuron: an example of chemical computation. Science 263, 823-826.
88. Sogaard R, Ljungstrom T, Pedersen KA, Olesen SP & Jensen BS (2001). KCNQ4 channels expressed in mammalian cells: functional characteristics and pharmacology. Am J Physiol Heart Circ Physiol 280, C859-866.
89. Stamper SA, Carrera GE, Tan EW, Fugere V, Krahe R & Fortune ES (2010). Species differences in group size and electrosensory interference in weakly electric fishes: implications for electrosensory processing. Behav Brain Res 207, 368-376.
90. + channels: molecular determinants and function of the sk family. Nat Rev Neurosci 5, 758-770.
91. Tabak J, Rinzel J & Bertram R (2011). Quantifying the relative contributions of divisive and subtractive feedback to rhythm generation. PLoS Comp Biol 7, e1001124.
92. Takahashi T, Moiseff A & Konishi M (1984). Time and intensity cues are processed independently in the auditory system of the owl. J Neurosci 4, 1781-1786.
93. Tan EW, Nizar JM, Carrera GE & Fortune ES (2005). Electrosensory interference in naturally occurring aggregates of a species of weakly electric fish, Eigenmannia virescens. Behav Brain Res 164, 83-92.
94. Toporikova N & Chacron MJ (2009). Dendritic SK channels gate information processing in vivo by regulating an intrinsic bursting mechanism seen in vitro. J Neurophysiol 102, 2273-2287.
95. Ulanovsky N, Las L & Nelken I (2003). Processing of low-probability sounds by cortical neurons. Nat Neurosci 6, 391-398.
96. Vandecasteele M, Deniau JM & Venance L (2011). Spike frequency adaptation is developmentally regulated in substantia nigra pars compacta dopaminergic neurons. Neuroscience 192, 1-10.
97. Wainwright ML, Zhang H, Byrne JH & Cleary LJ (2002). Localized neuronal outgrowth induced by long-term sensitization training in aplysia. J Neurosci 22, 4132-4141.
98. Walcott EC, Higgins EA & Desai NS (2011). Synaptic and intrinsic balancing during postnatal development in rat pups exposed to valproic acid in utero. J Neurosci 31, 13097-13109.
99. Wang XJ (1998). Calcium coding and adaptive temporal computation in cortical pyramidal neurons. J Neurophysiol 79, 1549-1566.
100. Wark B, Lundstrom BN & Fairhall A (2007). Sensory adaptation. Curr Opin Neurobiol 17, 423-429.
101. Waroux O, Massotte L, Alleva L, Graulich A, Thomas E, Liegeois JF, Scuvee-Moreau J & Seutin V (2005). SK channels control the firing pattern of midbrain dopaminergic neurons in vivo. Eur J Neurosci 22, 3111-3121.
102. Williams S, Serafin M, Muhlethaler M & Bernheim L (1997). Distinct contributions of high- and low-voltage-activated calcium currents to afterhyperpolarizations in cholinergic nucleus basalis neurons of the guinea pig. J Neurosci 17, 7307-7315.
103. Wiskott L (2003). Slow feature analysis: a theoretical analysis of optimal free responses. Neural Comput 15, 2147-2177.
104. Yue C & Yaari Y (2004). KCNQ/M channels control spike afterdepolarization and burst generation in hippocampal neurons. J Neurosci 24, 4614-4624.
105. Zupanc GKH & Maler L (1993). Evoked chirping in the weakly electric fish Apteronotus leptorhynchus: a quantitative biophysical analysis. Can J Zool 71, 2301-2310.