Top

Journal of Computational Neuroscience

Published in:

01-04-2011

Phase-resetting curve determines how BK currents affect neuronal firing

Authors: Cheng Ly, Tamar Melman, Alison L. Barth, G. Bard Ermentrout

Published in: Journal of Computational Neuroscience | Issue 2/2011

Activate our intelligent search to find suitable subject content or patents.

search-config

AI-assisted search

Off

Abstract

BK channels are large conductance potassium channels gated by calcium and voltage. Paradoxically, blocking these channels has been shown experimentally to increase or decrease the firing rate of neurons, depending on the neural subtype and brain region. The mechanism for how this current can alter the firing rates of different neurons remains poorly understood. Using phase-resetting curve (PRC) theory, we determine when BK channels increase or decrease the firing rates in neural models. The addition of BK currents always decreases the firing rate when the PRC has only a positive region. When the PRC has a negative region (type II), BK currents can increase the firing rate. The influence of BK channels on firing rate in the presence of other conductances, such as I _m and I _h, as well as with different amplitudes of depolarizing input, were also investigated. These results provide a formal explanation for the apparently contradictory effects of BK channel antagonists on firing rates.

next article Dual oscillator model of the respiratory neuronal network generating quantal slowing of respiratory rhythm

Dont have a licence yet? Then find out more about our products and how to get one now:

Springer Professional "Wirtschaft+Technik"

Online-Abonnement

Mit Springer Professional "Wirtschaft+Technik" erhalten Sie Zugriff auf:

über 102.000 Bücher
über 537 Zeitschriften

aus folgenden Fachgebieten:

Automobil + Motoren
Bauwesen + Immobilien
Business IT + Informatik
Elektrotechnik + Elektronik
Energie + Nachhaltigkeit
Finance + Banking
Management + Führung
Marketing + Vertrieb
Maschinenbau + Werkstoffe
Versicherung + Risiko

Jetzt Wissensvorsprung sichern!

inform now

Springer Professional "Wirtschaft"

Online-Abonnement

Mit Springer Professional "Wirtschaft" erhalten Sie Zugriff auf:

über 67.000 Bücher
über 340 Zeitschriften

aus folgenden Fachgebieten:

Bauwesen + Immobilien
Business IT + Informatik
Finance + Banking
Management + Führung
Marketing + Vertrieb
Versicherung + Risiko

Jetzt Wissensvorsprung sichern!

inform now

Springer Professional "Technik"

Online-Abonnement

Mit Springer Professional "Technik" erhalten Sie Zugriff auf:

über 67.000 Bücher
über 390 Zeitschriften

aus folgenden Fachgebieten:

Automobil + Motoren
Bauwesen + Immobilien
Business IT + Informatik
Elektrotechnik + Elektronik
Energie + Nachhaltigkeit
Maschinenbau + Werkstoffe

Jetzt Wissensvorsprung sichern!

inform now

Adams, P., & Brown, D. (1982). Synaptic inhibition of the M-current: Slow excitatory post-synaptic potential mechanism in bullfrog sympathetic neurones. The Journal of Physiology, 332, 263.PubMed

Aradi, I., & Holmes, W. (1999). Role of multiple calcium and calcium-dependent conductances in regulation of hippocampal dentate granule cell excitability. Journal of Computational Neuroscience, 6, 215–235.PubMedCrossRef

Borg-Graham, L. (1987). Master’s thesis: Modelling the somatic electrical behavior of hippocampal pyramidal neurons. PhD thesis, Massachusetts Institute of Technology.

Borg-Graham, L. (1998). The surf-hippo neuron simulation system. http://www.cnrs-gif.fr/iaf/iaf9/surf-hippo.html, v2.8.

Borg-Graham, L. (1999), Interpretations of data and mechanisms for hippocampal pyramidal cell models. In E. Jones, P. Ulinski, & A. Peters (Eds.), Cerebral cortex (Vol. 13, pp. 19–138). Plenum Publishing Corporation.

Borg-Graham, L., & Schramm, A. (2009). In vivo dynamic clamp: The functional impact of synaptic and intrinsic conductances in visual cortex. In A. Destexhe, & T. Bal (Eds.), In dynamic clamp: From principles to applications (Vol. 13, pp. 19–138). Springer.

Brenner, R., Chen, Q., Vilaythong, A., Toney, G., Noebels, J., & Aldrich, R. (2005). BK channel β4 subunit reduces dentate gyrus excitability and protects against temporal lobe seizures. Nature Neuroscience, 8, 1752–1759.PubMedCrossRef

De Schutter, E., & Bower, J. (1994). An active membrane model of the cerebellar Purkinje cell. I. Simulation of current clamps in slice. Journal of Neurophysiology, 71, 375–400.PubMed

Destexhe, A., & Pare, D. (1999). Impact of network activity on the integrative properties of neocortical pyramidal neurons in vivo. Journal of Neurophysiology, 81, 1531–1547.PubMed

Du, W., Bautista, J., Yang, H., Diez-Sampedro, A., You, S., Wang, L., et al. (2005). Calcium-sensitive potassium channelopathy in human epilepsy and paroxysmal movement disorder. Nature Genetics, 37, 733–738.PubMedCrossRef

Ermentrout, G. B. (1996). Type I membranes, phase-resetting curves, and synchrony. Neural Computation, 8, 979–1001.PubMedCrossRef

Ermentrout, G. B. (2002). Simulating, analyzing, and animating dynamical systems: A guide to XPPAUT for researchers and students. Society for Industrial and Applied Mathematics (SIAM).

Ermentrout, G. B., Pascal, M., & Gutkin, B. (2001). The effects of spike frequency adaptation and negative feedback on the synchronization of neural oscillators. Neural Computation, 13, 1285–1310.PubMedCrossRef

Goldberg, J., Deister, C., & Wilson, C. (2007). Response properties and synchronization of rhythmically firing dendritic neurons. Journal of Neurophysiology, 97, 208.PubMedCrossRef

Gu, N., Vervaeke, K., & Storm, J. (2007). BK potassium channels facilitate high-frequency firing and cause early spike frequency adaptation in rat CA1 hippocampal pyramidal cells. The Journal of Physiology, 580, 859.PubMedCrossRef

Jin, W., Sugaya, A., Tsuda, T., Ohguchi, H., & Sugaya, E. (2000). Relationship between large conductance calcium-activated potassium channel and bursting activity. Brain Research, 860, 21–28.PubMedCrossRef

Kuramoto, Y. (1984). Chemical oscillations, waves and turbulence. New York: Springer.

Lee, U., & Cui, J. (2009). β subunit-specific modulations of BK channel function by a mutation associated with epilepsy and dyskinesia. The Journal of Physiology, 587, 1481–1498.PubMedCrossRef

Luthi, A., Bal, T., & McCormick, D. (1998). Periodicity of thalamic spindle waves is abolished by ZD7288, a blocker of Ih. Journal of Neurophysiology, 79, 3284–3289.PubMed

Maccaferri, G., & McBain, C. (1996). The hyperpolarization-activated current (Ih) and its contribution to pacemaker activity in rat CA1 hippocampal stratum oriens-alveus interneurones. Journal of Physiology, 497, 119–130.PubMed

Matthews, E., Weible, A., Shah, S., & Disterhoft, J. (2008). The BK-mediated fAHP is modulated by learning a hippocampus-dependent task. Proceedings of the National Academy of Sciences of the United States of America, 105, 15,154.CrossRef

Meredith, A., Wiler, S., Miller, B., Takahashi, J., Fodor, A., Ruby, N., et al. (2006). BK calcium-activated potassium channels regulate circadian behavioral rhythms and pacemaker output. Nature Neuroscience, 9, 1041–1049.PubMedCrossRef

Moczydlowski, E., & Latorre, R. (1983). Gating kinetics of Ca2 +-activated K+ channels from rat muscle incorporated into planar lipid bilayers. Evidence for two voltage-dependent Ca2 + binding reactions. Journal of General Physiology, 82, 511–542.PubMedCrossRef

Narayanan, R., & Johnston, D. (2008) The h channel mediates location dependence and plasticity of intrinsic phase response in rat hippocampal neurons. Journal of Neuroscience, 28, 5846–5860.PubMedCrossRef

Nelson, A., Gittis, A., & du Lac, S. (2005). Decreases in CaMKII activity trigger persistent potentiation of intrinsic excitability in spontaneously firing vestibular nucleus neurons. Neuron, 46, 623–631.PubMedCrossRef

Nelson, A., Krispel, C., Sekirnjak, C., & du Lac, S. (2003). Long-lasting increases in intrinsic excitability triggered by inhibition. Neuron, 40, 609–620.PubMedCrossRef

Netoff, T., Acker, C., Bettencourt, J., & White, J. (2005a). Beyond two-cell networks: Experimental measurement of neuronal responses to multiple synaptic inputs. Journal of Computational Neuroscience, 18, 287–295.PubMedCrossRef

Netoff, T., Banks, M., Dorval, A., Acker, C., Haas, J., Kopell, N., et al. (2005b). Synchronization in hybrid neuronal networks of the hippocampal formation. Journal of Neurophysiology, 93, 1197–1208.PubMedCrossRef

Pfeuty, B., Mato, G., Golomb, D., & Hansel, D. (2003). Electrical synapses and synchrony: The role of intrinsic currents. Journal of Neuroscience, 23, 6280.PubMed

Pitts, G., Ohta, H., & McMahon, D. (2006). Daily rhythmicity of large-conductance Ca2 +-activated K+ currents in suprachiasmatic nucleus neurons. Brain Research, 1071(1), 54–62.PubMedCrossRef

Rinzel, J., & Ermentrout, G. B. (1989). Analysis of neural excitability and oscillations. In I. Segev (Ed.), Methods in neuronal modeling: From synapses to networks (pp. 135–169). MIT Press.

Shao, L., Halvorsrud, R., Borg-Graham, L., & Storm, J. (1999). The role of BK-type Ca2 +-dependent K+ channels in spike broadening during repetitive firing in rat hippocampal pyramidal cells. The Journal of Physiology, 521, 135–146.PubMedCrossRef

Sheehan, J., Benedetti, B., & Barth, A. (2009). Anticonvulsant effects of the BK-channel antagonist paxilline. Epilepsia, 50, 711–720.PubMedCrossRef

Shruti, S., Clem, R., & Barth, A. (2008). A seizure-induced gain-of-function in BK channels is associated with elevated firing activity in neocortical pyramidal neurons. Neurobiology of Disease, 30, 323–330.PubMedCrossRef

Stiefel, K., Gutkin, B., & Sejnowski, T. (2008). Cholinergic neuromodulation changes phase response curve shape and type in cortical pyramidal neurons. PLoS One 3.

Stiefel, K., Gutkin, B., & Sejnowski, T. (2009). The effects of cholinergic neuromodulation on neuronal phase-response curves of modeled cortical neurons. Journal of Computational Neuroscience, 26, 289–301.PubMedCrossRef

Storm, J. (1985). Calcium-dependent spike repolarization, and three kinds of after-hyperpolarization (AHP) in hippocampal pyramidal cells. Society for Neuroscience, 11, 1183.

Storm, J. (1986a). A-current and ca-dependent transient outward current control the initial repetitive ring in hippocampal neurons. Biophysical Journal, 49, 369a.

Storm, J. (1986b). Evidence that C-current and A-current contribute to repolarization of the action potential in CA1 hippocampal pyramidal cells of rat hippocampus. Society for Neuroscience, 12, 764.

Storm, J. (1987). Action potential repolarization and a fast after-hyperpolarization in rat hippocampal pyramidal cells. The Journal of Physiology, 385, 733.PubMed

Sun, L., Xiong, Y., Zeng, X., Wu, Y., Pan, N., Lingle, C., et al. (2009). Differential regulation of action potentials by inactivating and noninactivating BK channels in rat adrenal chromaffin cells. Biophysical Journal, 97, 1832–1842.PubMedCrossRef

Traub, R., Wong, R., Miles, R., & Michelson, H. (1991). A model of a CA3 hippocampal pyramidal neuron incorporating voltage-clamp data on intrinsic conductances. Journal of Neurophysiology, 66, 635–650.PubMed

Tsubo, Y., Takada, M., Reyes, A., & Fukai, T. (2007). Layer and frequency dependencies of phase response properties of pyramidal neurons in rat motor cortex. European Journal of Neuroscience, 25, 3429.PubMedCrossRef

Wang, B., Rothberg, B., & Brenner, R. (2006). Mechanism of β4 subunit modulation of BK channels. Journal of General Physiology, 127, 449–465.PubMedCrossRef

Winfree, A. (1974). Patterns of phase compromise in biological cycles. Journal of Mathematical Biology, 1, 73–93.CrossRef

Title: Phase-resetting curve determines how BK currents affect neuronal firing
Authors: Cheng Ly
Tamar Melman
Alison L. Barth
G. Bard Ermentrout
Publication date: 01-04-2011
Publisher: Springer US
Published in: Journal of Computational Neuroscience / Issue 2/2011
Print ISSN: 0929-5313
Electronic ISSN: 1573-6873
DOI: https://doi.org/10.1007/s10827-010-0246-3

Springer Professional

Abstract

Please log in to get access to your license.

Dont have a licence yet? Then find out more about our products and how to get one now:

Springer Professional "Wirtschaft+Technik"

Springer Professional "Wirtschaft"

Springer Professional "Technik"

Other articles of this Issue 2/2011

A mathematical modeling study of inter-segmental coordination during stick insect walking

Frequency switching in a two-compartmental model of the dopaminergic neuron

Effects of heterogeneity in synaptic conductance between weakly coupled identical neurons

Can homeostatic plasticity in deafferented primary auditory cortex lead to travelling waves of excitation?

Dual oscillator model of the respiratory neuronal network generating quantal slowing of respiratory rhythm

Sharpening of directional selectivity from neural output of rabbit retina

Premium Partner