Dynamic interaction of Ih and IK-LVA during trains of synaptic potentials in principal neurons of the medial superior olive

Journal of Neuroscience

Volumn 31, Issue 24, 2011, Pages 8936-8947

  Khurana, Sukant ^a   Remme, Michiel W H ^b   Rinzel, John ^b,c   Golding, Nace L ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^b NEW YORK UNIVERSITY   (United States)

^c NEW YORK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CATION CHANNEL; POTASSIUM CHANNEL; CARDIOTONIC AGENT; DENDROTOXIN K; ICI D2788; PEPTIDE; PYRIMIDINE DERIVATIVE; VOLTAGE GATED POTASSIUM CHANNEL;

ANIMAL TISSUE; ARTICLE; BRAIN SLICE; BRAIN STEM; CATION CURRENT; CONTROLLED STUDY; EXCITATORY POSTSYNAPTIC POTENTIAL; FEMALE; GERBIL; HYPERPOLARIZATION; ION CURRENT; MALE; MEDIAL SUPERIOR OLIVE; MEMBRANE STEADY POTENTIAL; NONHUMAN; PATCH CLAMP; POTASSIUM CURRENT; PRIORITY JOURNAL; SIMULATION; SUPERIOR OLIVARY NUCLEUS; SYNAPSE; ANIMAL; BIOLOGICAL MODEL; BIOPHYSICS; CHANNEL GATING; COMPUTER SIMULATION; CYTOLOGY; DRUG EFFECT; ELECTROSTIMULATION; IN VITRO STUDY; METHODOLOGY; NERVE CELL; NEWBORN; NONLINEAR SYSTEM; NORMAL DISTRIBUTION; OLIVARY NUCLEUS; PHYSIOLOGY; SYNAPTIC POTENTIAL; TIME;

ANIMALS; ANIMALS, NEWBORN; BIOPHYSICS; CARDIOTONIC AGENTS; COMPUTER SIMULATION; ELECTRIC STIMULATION; FEMALE; GERBILLINAE; ION CHANNEL GATING; MALE; MODELS, NEUROLOGICAL; NEURONS; NONLINEAR DYNAMICS; NORMAL DISTRIBUTION; OLIVARY NUCLEUS; PATCH-CLAMP TECHNIQUES; PEPTIDES; POTASSIUM CHANNELS, VOLTAGE-GATED; PYRIMIDINES; SYNAPTIC POTENTIALS; TIME FACTORS;

EID: 79959314864     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1079-11.2011     Document Type: Article

References (44)

1. Bal R, Oertel D (2000) Hyperpolarization-activated, mixed-cation current (Ih) in octopus cells of the mammalian cochlear nucleus. J Neurophysiol 84:806-817.
2. Bal R, Oertel D (2001) Potassium currents in octopus cells of the mammalian cochlear nucleus. J Neurophysiol 86:2299-2311.
3. Banks MI, Smith PH (1992) Intracellular recordings from neurobiotin-labeled cells in brain slices of the rat medial nucleus of the trapezoid body. J Neurosci 12:2819-2837.
4. Barnes-Davies M, Barker MC, Osmani F, Forsythe ID (2004) Kv1 currents mediate a gradient of principal neuron excitability across the tonotopic axis in the rat lateral superior olive. Eur J Neurosci 19:325-333.
5. Borst JG (2010) The low synaptic release probability in vivo. Trends Neurosci 33:259-266.
6. Cook DL, Schwindt PC, Grande LA, Spain WJ (2003) Synaptic depression in the localization of sound. Nature 421:66-70.
7. Couchman K, Grothe B, Felmy F (2010) Medial superior olivary neurons receive surprisingly few excitatory and inhibitory inputs with balanced strength and short-term dynamics. JNeurosci 30:17111-17121.
8. + channels. Nat Neurosci 12:577-584.
9. Golding NL, Robertson D, Oertel D (1995) Recordings from slices indicate that octopus cells of the cochlear nucleus detect coincident firing of auditory nerve fibers with temporal precision. JNeurosci 15:3138-3153.
10. Grande LA, Spain WJ (2005) Synaptic depression as a timing device. Physiology (Bethesda) 20:201-210.
11. Grothe B (2003) New roles for synaptic inhibition in sound localization. Nat Rev Neurosci 4:540-550.
12. Hassfurth B, Magnusson AK, Grothe B, Koch U (2009) Sensory deprivation regulates the development of the hyperpolarization-activated current in auditory brainstem neurons. Eur J Neurosci 30:1227-1238.
13. Joris P, Yin TC (2007) A matter of time: internal delays in binaural processing. Trends Neurosci 30:70-78.
14. Joris PX, Carney LH, Smith PH, Yin TC (1994) Enhancement of neural synchronization in the anteroventral cochlear nucleus. I. Responses to tones at the characteristic frequency. J Neurophysiol 71:1022-1036.
15. Kaczmarek LK, Bhattacharjee A, Desai R, Gan L, Song P, von Hehn CA, Whim MD, Yang B (2005) Regulation of the timing of MNTB neurons by short-term and long-term modulation of potassium channels. Hear Res 206:133-145.
16. Koch U, Grothe B (2003) Hyperpolarization-activated current (Ih) in the inferior colliculus: distribution and contribution to temporal processing. J Neurophysiol 90:3679-3687.
17. Kole MH, Hallermann S, Stuart GJ (2006) Single Ih channels in pyramidal neuron dendrites: properties, distribution, and impact on action potential output. J Neurosci 26:1677-1687.
18. Kuba H, Yamada R, Fukui I, Ohmori H (2005) Tonotopic specialization of auditory coincidence detection in nucleus laminaris of the chick. J Neurosci 25:1924-1934.
19. Kuznetsova MS, Higgs MH, Spain WJ (2008) Adaptation of firing rate and spike-timing precision in the avian cochlear nucleus. J Neurosci 28:11906-11915.
20. Leao KE, Leao RN, Sun H, Fyffe RE, Walmsley B (2006) Hyperpolarization-activated currents are differentially expressed in mice brainstem auditory nuclei. J Physiol 576:849-864.
21. Leao RN, Svahn K, Berntson A, Walmsley B (2005) Hyperpolarization-activated (Ih) currents in auditory brainstem neurons of normal and con-genitally deaf mice. Eur J Neurosci 22:147-157.
22. Lorincz A, Notomi T, Tamas G, Shigemoto R, Nusser Z (2002) Polarized and compartment-dependent distribution of HCN1 in pyramidal cell dendrites. Nat Neurosci 5:1185-1193.
23. Lorteije JA, Rusu SI, Kushmerick C, Borst JG (2009) Reliability and precision of the mouse calyx of Held synapse. J Neurosci 29:13770-13784.
24. MacLean JN, Zhang Y, Goeritz ML, Casey R, Oliva R, Guckenheimer J, Harris-Warrick RM (2005) Activity-independent coregulation ofIA and Ih in rhythmically active neurons. J Neurophysiol 94:3601-3617.
25. Magee JC (1998) Dendritic hyperpolarization-activated currents modify the integrative properties of hippocampal CA1 pyramidal neurons. J Neurosci 18:7613-7624.
26. Magee JC (1999) Dendritic Ih normalizes temporal summation in hippocampal CA1 neurons. Nat Neurosci 2:848.
27. Magnusson AK, Kapfer C, Grothe B, Koch U (2005) Maturation of glycin-ergic inhibition in the gerbil medial superior olive after hearing onset. J Physiol 568:497-512.
28. Mathews PJ, Jercog PE, Rinzel J, Scott LL, Golding NL (2010) Control of submillisecond synaptic timing in binaural coincidence detectors by Kv1 channels. Nat Neurosci 13:601-609.
29. Mo ZL, Davis RL (1997) Heterogeneous voltage dependence of inward rectifier currents in spiral ganglion neurons. J Neurophysiol 78:3019-3027.
30. + dynamics matter. J Physiol 586:2031.
31. Rathouz M, Trussell L (1998) Characterization of outward currents in neurons of the avian nucleus magnocellularis. J Neurophysiol 80:2824-2835.
32. Reyes AD, Rubel EW, Spain WJ (1994) Membrane properties underlying the firing of neurons in the avian cochlear nucleus. J Neurosci 14:5352-5364.
33. Rothman JS, Manis PB (2003a) Kinetic analyses of three distinct potassium conductances in ventral cochlear nucleus neurons. J Neurophysiol 89:3083-3096.
34. Rothman JS, Manis PB (2003b) The roles potassium currents play in regulating the electrical activity of ventral cochlear nucleus neurons. J Neurophysiol 89:3097-3113.
35. Scott LL, Mathews PJ, Golding NL (2005) Posthearing developmental refinement of temporal processing in principal neurons of the medial superior olive. J Neurosci 25:7887-7895.
36. Scott LL, Hage TA, Golding NL (2007) Weak action potential backpropaga-tion is associated with high-frequency axonal firing capability in principal neurons of the gerbil medial superior olive. J Physiol 583:647-661.
37. Scott LL, Mathews PJ, Golding NL (2010) Perisomatic voltage-gated sodium channels actively maintain linear synaptic integration in principal neurons of the medial superior olive. J Neurosci 30:2039-2050.
38. Smith AJ, Owens S, Forsythe ID (2000) Characterisation of inhibitory and excitatory postsynaptic currents of the rat medial superior olive. J Physiol 529:681-698.
39. Stuart G, Spruston N (1998) Determinants of voltage attenuation in neo-cortical pyramidal neuron dendrites. J Neurosci 18:3501-3510.
40. Svirskis G, Kotak V, Sanes DH, Rinzel J (2002) Enhancement of signal-to-noise ratio and phase locking for small inputs by a low-threshold outward current in auditory neurons. J Neurosci 22:11019-11025.
41. Svirskis G, Kotak V, Sanes DH, Rinzel J (2004) Sodium along with low-threshold potassium currents enhance coincidence detection of subthreshold noisy signals in MSO neurons. J Neurophysiol 91:2465-2473.
42. Wahl-Schott C, Biel M (2009) HCN channels: structure, cellular regulation and physiological function. Cell Mol Life Sci 66:470-494.
43. Willms AR (2002) NEUROFIT: software for fitting Hodgkin-Huxley models to voltage-clamp data. J Neurosci Methods 121:139-150.
44. Yamada R, Kuba H, Ishii TM, Ohmori H (2005) Hyperpolarization-activated cyclic nucleotide-gated cation channels regulate auditory coincidence detection in nucleus laminaris of the chick. J Neurosci 25:8867-8877.