Ionic and neuromodulatory regulation of burst discharge controls frequency tuning

Journal of Physiology Paris

Volumn 102, Issue 4-6, 2008, Pages 195-208

  Mehaffey, W Hamish ^a   Ellis, Lee D ^b   Krahe, Rüdiger ^b   Dunn, Robert J ^b   Chacron, Maurice J ^b  

^a UNIVERSITY OF CALGARY   (Canada)

^b MCGILL UNIVERSITY   (Canada)

Author keywords

Acetylcholine; Bursting; Calcium dynamics; Information theory; Neuromodulation; Weakly electric fish

Indexed keywords

AMPLITUDE MODULATION; ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR CONTROL; BRAIN REGION; CELL TYPE; CONTROLLED STUDY; ELECTRIC CURRENT; ELECTRIC FISH; ELECTRIC ORGAN; NERVE CELL NETWORK; NERVE CONDUCTION; NEUROMODULATION; NONHUMAN; PYRAMIDAL NERVE CELL; SENSORY STIMULATION; SENSORY SYSTEM;

ACTION POTENTIALS; ANIMALS; BIOPHYSICAL PROCESSES; ELECTRIC FISH; ELECTRIC STIMULATION; ION CHANNELS; MODELS, NEUROLOGICAL; NEUROTRANSMITTER AGENTS; PYRAMIDAL CELLS; RHOMBENCEPHALON; TIME FACTORS;

EID: 58649085245     PISSN: 09284257     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jphysparis.2008.10.019     Document Type: Article

References (101)

1. Abbott L.F. Where are the switches on this thing?. In: van Hemmen J.L., and Sejnowski T.J. (Eds). 23 Problems in Systems Neuroscience (2005), Oxford University Press 423-431
2. Andermann M.L., Ritt J., Neimark M.A., and Moore C.I. Neural correlates of vibrissa resonance; band-pass and somatotopic representation of high-frequency stimuli. Neuron 42 (2004) 451-463
3. Bair W., Koch C., Newsome W., and Britten K. Power spectrum analysis of bursting cells in area MT in the behaving monkey. J. Neurosci. 14 (1994) 2870-2892
4. Bastian J. Electrolocation II. The effects of moving objects and other electrical stimuli on the activities of two categories of posterior lateral line lobe cells in Apteronotus albifrons. J. Comp. Physiol. [A] 144 (1981) 481-494
5. Bastian J. Plasticity of feedback inputs in the apteronotid electrosensory system. J. Exp. Biol. 202 Pt 10 (1999) 1327-1337
6. Bastian J., and Courtright J. Morphological correlates of pyramidal cell adaption rate in the electrosensory lateral line lobe of weakly electric fish. J. Comp. Physiol. 168 (1991) 393-407
7. Bastian J., and Nguyenkim J. Dendritic modulation of burst-like firing in sensory neurons. J. Neurophysiol. 85 (2001) 10-22
8. Bastian J., Chacron M.J., and Maler L. Receptive field organization determines pyramidal cell stimulus-encoding capability and spatial stimulus selectivity. J. Neurosci. 22 (2002) 4577-4590
9. Bastian J., Chacron M.J., and Maler L. Plastic and nonplastic pyramidal cells perform unique roles in a network capable of adaptive redundancy reduction. Neuron 41 (2004) 767-779
10. Benda J., Longtin A., and Maler L. Spike-frequency adaptation separates transient communication signals from background oscillations. J. Neurosci. 25 (2005) 2312-2321
11. Benda J., Longtin A., and Maler L. A synchronization-desynchronization code for natural communication signals. Neuron 52 (2006) 347-358
12. Berman N.J., and Maler L. Distal versus proximal inhibitory shaping of feedback excitation in the electrosensory lateral line lobe: implications for sensory filtering. J. Neurophysiol. 80 (1998) 3214-3232
13. Berman N.J., and Maler L. Inhibition evoked from primary afferents in the electrosensory lateral line lobe of the weakly electric fish (Apteronotus leptorhynchus). J. Neurophysiol. 80 (1998) 3173-3196
14. Berman N.J., and Maler L. Interaction of GABAB-mediated inhibition with voltage-gated currents of pyramidal cells: computational mechanism of a sensory searchlight. J. Neurophysiol. 80 (1998) 3197-3213
15. Berman N., Dunn R.J., and Maler L. Function of NMDA receptors and persistent sodium channels in a feedback pathway of the electrosensory system. J. Neurophysiol. 86 (2001) 1612-1621
16. Butts D.A., Weng C., Jin J., Yeh C.I., Lesica N.A., Alonso J.M., and Stanley G.B. Temporal precision in the neural code and the timescales of natural vision. Nature 449 (2007) 92-95
17. Cai X., Liang C.W., Muralidharan S., Kao J.P., Tang C.M., and Thompson S.M. Unique roles of SK and Kv4.2 potassium channels in dendritic integration. Neuron 44 (2004) 351-364
18. Carr C.E. Time coding in electric fish and barn owls. Brain Behav. Evol. 28 (1986) 122-133
19. Chacron M.J. Nonlinear information processing in a model sensory system. J. Neurophysiol. 95 (2006) 2933-2946
20. Chacron M.J., and Bastian J.A. Population coding by electrosensory neurons. J. Neurophysiol. 100 (2008) 852-867
21. Chacron M.J., Doiron B., Maler L., Longtin A., and Bastian J. Non-classical receptive field mediates switch in a sensory neuron's frequency tuning. Nature 423 (2003) 77-81
22. Chacron M.J., Longtin A., and Maler L. The effects of spontaneous activity, background noise, and the stimulus ensemble on information transfer in neurons. Network 14 (2003) 803-824
23. Chacron M.J., Longtin A., and Maler L. Delayed excitatory and inhibitory feedback shape neural information transmission. Phys. Rev. E. Stat. Nonlin. Soft. Matter. Phys. 72 (2005) 051917
24. Chacron M.J., Maler L., and Bastian J. Feedback and feed forward control of frequency tuning to naturalistic stimuli. J. Neurosci. 25 (2005) 5521-5532
25. + channels in dendrites of CA1 pyramidal neurones of rat hippocampus. J. Physiol. 559 (2004) 187-203
26. + current and enhances induction of long-term potentiation in hippocampal CA1 pyramidal neurons. J. Neurosci. 26 (2006) 12143-12151
27. Connor J.A., and Stevens C.F. Voltage clamp studies of a transient outward membrane current in gastropod neural somata. J. Physiol. 213 (1971) 21-30
28. Delgado-Lezama R., Perrier J.F., Nedergaard S., Svirskis G., and Hounsgaard J. Metabotropic synaptic regulation of intrinsic response properties of turtle spinal motoneurones. J. Physiol. 504 Pt 1 (1997) 97-102
29. Deng Q., Rashid A.J., Fernandez F.R., Turner R.W., Maler L., and Dunn R.J. A C-terminal domain directs Kv3.3 channels to dendrites. J. Neurosci. 25 (2005) 11531-11541
30. Doiron B., Chacron M.J., Maler L., Longtin A., and Bastian J. Inhibitory feedback required for network oscillatory responses to communication but not prey stimuli. Nature 421 (2003) 539-543
31. Doiron B., Laing C., Longtin A., and Maler L. Ghostbursting: a novel neuronal burst mechanism. J. Comput. Neurosci. 12 (2002) 5-25
32. Doiron B., Oswald A.M., and Maler L. Interval coding. II. Dendrite-dependent mechanisms. J. Neurophysiol. 97 (2007) 2744-2757
33. Elhilali M., Fritz J.B., Klein D.J., Simon J.Z., and Shamma S.A. Dynamics of precise spike timing in primary auditory cortex. J. Neurosci. 24 (2004) 1159-1172
34. Ellis L.D., Krahe R., Bourque C.W., Dunn R.J., and Chacron M.J. Muscarinic receptors control frequency tuning through the downregulation of an A-type potassium current. J. Neurophysiol. 98 (2007) 1526-1527
35. Ellis L.D., Maler L., and Dunn R.J. Differential distribution of SK channel subtypes in the brain of the weakly electric fish Apteronotus leptorhynchus. J. Comp. Neurol. 507 (2008) 1964-1978
36. Ellis L.D., Mehaffey W.H., Harvey-Girard E., Turner R.W., Maler L., and Dunn R.J. SK Channels provide a novel mechanism for the control of frequency tuning in electrosensory neurons. J. Neurosci. 27 (2007) 9491-9502
37. Faber E.S., Delaney A.J., and Sah P. SK channels regulate excitatory synaptic transmission and plasticity in the lateral amygdala. Nat. Neurosci. 8 (2005) 635-641
38. + current. J. Neurosci. 25 (2005) 363-371
39. + current inactivation can increase cell excitability by delaying a somatic depolarizing afterpotential. J. Neurophysiol. 94 (2005) 3836-3848
40. Finger T.E. Efferent neurons of the teleost cerebellum. Brain Res. 153 (1978) 608-614
41. Frank, K., Becker, M.C., 1964. Physical techniques in biological research. In: Nastuk, W.L. (Ed.), vol. 5, Pt. A. Academic Press, New York, pp. 23-87 and 239-243.
42. Goldberg J.M., Smith C.E., and Fernandez C. Relation between discharge regularity and responses to externally applied galvanic currents in vestibular nerve afferents of the squirrel monkey. J. Neurophysiol. 51 (1984) 1236-1256
43. Harvey-Girard E., Dunn R.J., and Maler L. Regulated expression of N-methyl-d-aspartate receptors and associated proteins in teleost electrosensory system and telencephalon. J. Comp. Neurol. 505 (2007) 644-668
44. Heiligenberg W. Neural Nets in Electric Fish (1991), MIT Press, Cambridge, Mass
45. + channel regulation of signal propagation in dendrites of hippocampal pyramidal neurons. Nature 387 (1997) 869-875
46. Izhikevich E.M. Dynamical Systems in Neuroscience: The Geometry of Excitability and Bursting (2007), MIT Press, Cambridge, MA
47. Jarvis M.R., and Mitra P.P. Sampling properties of the spectrum and coherency of sequences of action potentials. Neural. Comput. 13 (2001) 717-749
48. Johnston D., Magee J.C., Colbert C.M., and Cristie B.R. Active properties of neuronal dendrites. Annu. Rev. Neurosci. 19 (1996) 165-186
49. Johnston S.A., Maler L., and Tinner B. The distribution of serotonin in the brain of Apteronotus leptorhynchus: an immunohistochemical study. J. Chem. Neuroanat. 3 (1990) 429-465
50. Kohler M., Hirschberg B., Bond C.T., Kinzie J.M., Marrion N.V., Maylie J., and Adelman J.P. Small-conductance, calcium-activated potassium channels from mammalian brain. Science 273 (1996) 1709-1714
51. Krahe R., and Gabbiani F. Burst firing in sensory systems. Nat. Rev. Neurosci. 5 (2004) 13-23
52. Krahe R., Kreiman G., Gabbiani F., Koch C., and Metzner W. Stimulus encoding and feature extraction by multiple sensory neurons. J. Neurosci. 22 (2002) 2374-2382
53. Lemon N., and Turner R.W. Conditional spike backpropagation generates burst discharge in a sensory neuron. J. Neurophysiol. 84 (2000) 1519-1530
54. Lesica N.A., and Stanley G.B. Encoding of natural scene movies by tonic and burst spikes in the lateral geniculate nucleus. J. Neurosci. 24 (2004) 10731-10740
55. Li W., Kaczmarek L.K., and Perney T.M. Localization of two high-threshold potassium channel subunits in the rat central auditory system. J. Comp. Neurol. 437 (2001) 196-218
56. MacLeod K.M., and Carr C.E. Beyond timing in the auditory brainstem: intensity coding in the avian cochlear nucleus angularis. Prog. Brain. Res. 165 (2007) 123-133
57. Maler L. The posterior lateral line lobe of certain gymnotoid fish: quantitative light microscopy. J. Comp. Neurol. 183 (1979) 323-363
58. Maler L., and Ellis W.G. Inter-male aggressive signals in weakly electric fish are modulated by monoamines. Behav. Brain. Res. 25 (1987) 75-81
59. Maler L., Sas E.K., and Rogers J. The cytology of the posterior lateral line lobe of high-frequency weakly electric fish (Gymnotidae): dendritic differentiation and synaptic specificity in a simple cortex. J. Comp. Neurol. 195 (1981) 87-139
60. Marder E., and Goaillard J.M. Variability, compensation and homeostasis in neuron and network function. Nat. Rev. Neurosci. 7 (2006) 563-574
61. Mathieson W.B., and Maler L. Morphological and electrophysiological properties of a novel in vitro preparation: the electrosensory lateral line lobe brain slice. J. Comp. Physiol. [A] 163 (1988) 489-506
62. McCormick D.A. Functional properties of a slowly inactivating potassium current in guinea pig dorsal lateral geniculate relay neurons. J. Neurophysiol. 66 (1991) 1176-1189
63. Mehaffey W.H., Doiron B., Maler L., and Turner R.W. Deterministic multiplicative gain control with active dendrites. J. Neurosci. 25 (2005) 9968-9977
64. Mehaffey W.H., Fernandez F.R., Rashid A.J., Dunn R.J., and Turner R.W. Distribution and function of potassium channels in the electrosensory lateral line lobe of weakly electric apteronotid fish. J. Comp. Physiol. A. Neuroethol. Sens. Neural. Behav. Physiol. 192 (2006) 637-648
65. Mehaffey W.H., Fernandez F.R., Doiron B., and Turner R.W. Synaptic and dynamic regulation of pyramidal cell firing dynamics mediated by backpropating spikes. J. Physiol. Paris (2008)
66. Mehaffey W.H., Fernandez F.R., Maler L., and Turner R.W. Regulation of burst dynamics improves differential encoding of stimulus frequency by spike train segregation. J. Neurophysiol. 98 (2007) 939-951
67. Mehaffey W.H., Maler L., and Turner R.W. Regulation of intrinsic frequency tuning of ELL pyramidal cells across electrosensory maps. J. Neurophysiol. (2008)
68. Metzner W., and Juranek J. A sensory brain map for each behavior?. Proc. Natl. Acad. Sci. USA 94 (1997) 14798-14803
69. Metzner W., Koch C., Wessel R., and Gabbiani F. Feature extraction by burst-like spike patterns in multiple sensory maps. J. Neurosci. 18 (1998) 2283-2300
70. Middleton J.W., Longtin A., Benda J., and Maler L. The cellular basis for parallel neural transmission of a high-frequency stimulus and its low-frequency envelope. Proc. Natl. Acad. Sci. USA 103 (2006) 14596-14601
71. Nelson M.E., and MacIver M.A. Prey capture in the weakly electric fish Apteronotus albifrons: sensory acquisition strategies and electrosensory consequences. J. Exp. Biol. 202 (1999) 1195-1203
72. 2+mediated feedback loop in dendritic spines. Nat. Neurosci. 8 (2005) 642-649
73. Noonan L., Doiron B., Laing C., Longtin A., and Turner R.W. A dynamic dendritic refractory period regulates burst discharge in the electrosensory lobe of weakly electric fish. J. Neurosci. 23 (2003) 1524-1534
74. Oswald A.M., Chacron M.J., Doiron B., Bastian J., and Maler L. Parallel processing of sensory input by bursts and isolated spikes. J. Neurosci. 24 (2004) 4351-4362
75. Oswald A.M., Doiron B., and Maler L. Interval coding. I. Burst interspike intervals as indicators of stimulus intensity. J. Neurophysiol. 97 (2007) 2731-2743
76. Pedarzani P., McCutcheon J.E., Rogge G., Jensen B.S., Christophersen P., Hougaard C., Strobaek D., and Stocker M. Specific enhancement of SK channel activity selectively potentiates the afterhyperpolarizing current I(AHP) and modulates the firing properties of hippocampal pyramidal neurons. J. Biol. Chem. 280 (2005) 41404-41411
77. Perney T.M., and Kaczmarek L.K. Localization of a high threshold potassium channel in the rat cochlear nucleus. J. Comp. Neurol. 386 (1997) 178-202
78. Phan M., and Maler L. Distribution of muscarinic receptors in the caudal cerebellum and electrosensory lateral line lobe of gymnotiform fish. Neurosci. Lett. 42 (1983) 137-143
79. Priebe N.J., Lisberger S.G., and Movshon J.A. Tuning for spatiotemporal frequency and speed in directionally selective neurons of macaque striate cortex. J. Neurosci. 26 (2006) 2941-2950
80. + channels in electrosensory and cerebellar neurons. J. Comp. Neurol. 441 (2001) 234-247
81. + channels to burst threshold in a sensory neuron. J. Neurosci. 21 (2001) 125-135
82. Roddey J.C., Girish B., and Miller J.P. Assessing the performance of neural encoding models in the presence of noise. J. Comput. Neurosci. 8 (2000) 95-112
83. Sah P., and Faber E.S. Channels underlying neuronal calcium-activated potassium currents. Prog. Neurobiol. 66 (2002) 345-353
84. Sarter M., Hasselmo M.E., Bruno J.P., and Givens B. Unraveling the attentional functions of cortical cholinergic inputs: interactions between signal-driven and cognitive modulation of signal detection. Brain. Res. Brain. Res. Rev. 48 (2005) 98-111
85. Saunders J., and Bastian J. The physiology and morphology of two types of electrosensory neurons in the weakly electric fish, Apteronotus leptorhynchus. J. Comp. Physiol. [A] 154 (1984) 199-209
86. Schoppa N.E., and Westbrook G.L. Regulation of synaptic timing in the olfactory bulb by an A-type potassium current. Nat. Neurosci. 2 (1999) 1106-1113
87. Shumway C.A. Multiple electrosensory maps in the medulla of weakly electric gymnotiform fish. I. Physiological differences. J. Neurosci. 9 (1989) 4388-4399
88. Shumway C.A. Multiple electrosensory maps in the medulla of weakly electric gymnotiform fish. II. Anatomical differences. J. Neurosci. 9 (1989) 4400-4415
89. Simoncelli E.P., and Olshausen B.A. Natural image statistics and neural representation. Annu. Rev. Neurosci. 24 (2001) 1193-1216
90. Smith G.T., Unguez G.A., and Weber C.M. Distribution of Kv1-like potassium channels in the electromotor and electrosensory systems of the weakly electric fish Apteronotus leptorhynchus. J. Neurobiol. 66 (2006) 1011-1031
91. Softky W.R., and Koch C. The highly irregular firing of cortical cells is inconsistent with temporal integration of random EPSPs. J. Neurosci. 13 (1993) 334-350
92. + current in hippocampal pyramidal neurons. Proc. Natl. Acad. Sci. USA 96 (1999) 4662-4667
93. Troyer T.W., and Miller K.D. Physiological gain leads to high ISI variability in a simple model of a cortical regular spiking cell. Neural. Comput. 9 (1997) 971-983
94. Turner R.W., and Maler L. Oscillatory and burst discharge in the apteronotid electrosensory lateral line lobe. J. Exp. Biol. 202 (1999) 1255-1265
95. Turner R.W., Maler L., Deerinck T., Levinson S.R., and Ellisman M.H. TTX-sensitive dendritic sodium channels underlie oscillatory discharge in a vertebrate sensory neuron. J. Neurosci. 14 (1994) 6453-6471
96. Turner R.W., Plant J.R., and Maler L. Oscillatory and burst discharge across electrosensory topographic maps. J. Neurophysiol. 76 (1996) 2364-2382
97. von Hehn C.A., Bhattacharjee A., and Kaczmarek L.K. Loss of Kv3.1 tonotopicity and alterations in cAMP response element-binding protein signaling in central auditory neurons of hearing impaired mice. J. Neurosci. 24 (2004) 1936-1940
98. Wang X., Wei Y., Vaingankar V., Wang Q., Koepsell K., Sommer F.T., and Hirsch J.A. Feedforward excitation and inhibition evoke dual modes of firing in the cat's visual thalamus during naturalistic viewing. Neuron 55 (2007) 465-478
99. Wässle H. Parallel processing in the mammalian retina. Nat. Rev. Neurosci. 5 (2004) 747-757
100. Wilbur W.J., and Rinzel J. A theoretical basis for large coefficient of variation and bimodality in neuronal interspike interval distributions. J. Theor. Biol. 105 (1983) 345-368
101. Zupanc G.K., Sirbulescu R.F., Nichols A., and Ilies I. Electric interactions through chirping behavior in the weakly electric fish, Apteronotus leptorhynchus. J. Comp. Physiol. A. Neuroethol. Sens. Neural. Behav. Physiol. 192 (2006) 159-173