Norepinephrine selectively reduces slow Ca2+- and Na+-mediated K+ currents in cat neocortical neurons
Abstract
1. The effects of norepinephrine (NE) and related agonists and antagonists were examined on large neurons from layer V of cat sensorimotor cortex ("Betz cells") were examined in a brain slice preparation using intracellular recording, constant current stimulation and single microelectrode voltage clamp. 2. Application of NE (0.1-100 microM) usually caused a small depolarization from resting potential; hyperpolarizations were rare. Application of NE reversibly reduced rheobase and both the Ca2+- and Na+-dependent portions of the slow afterhyperpolarization (sAHP) that followed sustained firing evoked by constant current injection. The faster Ca2+-dependent medium afterhyperpolarization (mAHP), the fast afterhyperpolarization (fAHP), the action potential, and input resistance were unaffected. 3. The changes in excitability produced by NE application were most apparent during prolonged stimulation. The cells exhibited steady repetitive firing to currents that were formerly ineffective. The slow phase of spike frequency adaptation was reduced selectively and less habituation occurred during repeated long-lasting stimuli. The relation between firing rate and injected current became steeper if firing rate was averaged over several hundred milliseconds. 4. During voltage clamp in TTX, NE application selectively reduced the slow component of Ca2+-mediated K+ current. The faster Ca2+-mediated K+ current was unaffected, as were two voltage-dependent, transient K+ currents, the anomalous rectifier and leakage conductance measured at resting potential. Depolarizing voltage steps in the presence of Cd2+ revealed an apparent time- and voltage-dependent increase of the persistent Na+ current after NE application. The voltage-clamp results suggested ionic mechanisms for all effects seen during constant current stimulation except the depolarization from resting potential. The latter was insensitive to Cd2+ and TTX and occurred without a detectable change in membrane conductance. 5. NE application did not alter Ca2+ spikes evoked in the presence of TTX and 10 mM TEA. Inward Ca2+ currents examined during voltage clamp in TTX (with K+ currents reduced) became slightly larger after NE application. We conclude that NEs reduction of the slow Ca2+-mediated K+ current is not caused by reduction of Ca2+ influx. 6. Effects on membrane potential, rheobase, and the sAHP were mimicked by the beta-adrenergic agonist isoproterenol, but not by the alpha-adrenergic agonists clonidine or phenylephrine at higher concentrations.(ABSTRACT TRUNCATED AT 400 WORDS)
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Noradrenaline increases excitability of neurons that express β-adrenergic receptors.
“Noradrenaline increases the excitability of neurons that express β-adrenergic receptors187–189 and reduces excitatory synaptic transmission by acting on α-adrenergic receptors190,191”
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Harris, K. D., & Thiele, A. (2011) · Nature reviews. Neuroscience · doi:10.1038/nrn3084 · Cited by 871 · see citing works
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McCormick, D. A. (1989) · Trends in Neurosciences · doi:10.1016/0166-2236(89)90125-2 · Cited by 488 · see citing works
Mason, A., & Larkman, A. U. (1990) · Journal of Neuroscience · doi:10.1523/jneurosci.10-05-01415.1990 · Cited by 490 · see citing works
Gu, N., Vervaeke, K., Hu, H., & Storm, J. F. (2005) · The Journal of Physiology · doi:10.1113/jphysiol.2005.086835 · Cited by 363 · see citing works
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Bevan, M. D., & Wilson, C. J. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-17-07617.1999 · Cited by 343 · see citing works
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Pedarzani, P., & Storm, J. F. (1993) · Neuron · doi:10.1016/0896-6273(93)90216-e · Cited by 272 · see citing works
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Origin of Active States in Local Neocortical Networks during Slow Sleep Oscillation
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Kawaguchi, Y., & Shindou, T. (1998) · The Journal of Neuroscience · doi:10.1523/jneurosci.18-17-06963.1998 · Cited by 230 · see citing works
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McCormick, D. A., Pape, H.-C., & Williamson, A. (1991) · Progress in Brain Research · doi:10.1016/s0079-6123(08)63817-0 · Cited by 209 · see citing works
The role of metaplasticity mechanisms in regulating memory destabilization and reconsolidation
Finnie, P. S. B., & Nader, K. (2012) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2012.03.008 · Cited by 189 · see citing works
Séguéla, P., Watkins, K. C., Geffard, M., & Descarries, L. (1990) · Neuroscience · doi:10.1016/0306-4522(90)90079-j · Cited by 196 · see citing works
Slack, Slick, and Sodium-Activated Potassium Channels
Kaczmarek, L. K. (2013) · ISRN Neuroscience · doi:10.1155/2013/354262 · Cited by 150 · see citing works
Gu, Q., & Singer, W. (1993) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1993.tb00514.x · Cited by 137 · see citing works
“This agrees with the fact that noradrenalin, through P-receptor-rnediated processes, also reduces various K+ conductances in cortical neurons (Foehring et al., 1989).”
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Dryer, S. E. (1994) · Trends in Neurosciences · doi:10.1016/0166-2236(94)90093-0 · Cited by 139 · see citing works
Corner, M. A., van Pelt, J., Wolters, P. S., Baker, R. E., & Nuytinck, R. H. (2002) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(01)00062-8 · Cited by 132 · see citing works
SK channels and the varieties of slow after‐hyperpolarizations in neurons
Vogalis, F., Storm, J. F., & Lancaster, B. (2003) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2003.03040.x · Cited by 122 · see citing works
Higgs, M. H., Slee, S. J., & Spain, W. J. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.1792-06.2006 · Cited by 124 · see citing works
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Thomas, T. M., Smith, Y., Levey, A. I., & Hersch, S. M. (2000) · Synapse · doi:10.1002/1098-2396(20000915)37:4 · Cited by 81 · see citing works
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Sheets, P. L., Suter, B. A., Kiritani, T., Chan, C. S., Surmeier, D. J., & Shepherd, G. M. (2011) · Journal of Neurophysiology · doi:10.1152/jn.00232.2011 · Cited by 117 · see citing works
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Meintzschel, F., & Ziemann, U. (2006) · Cerebral Cortex · doi:10.1093/cercor/bhj052 · Cited by 119 · see citing works
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Manunta, Y., & Edeline, J. (1997) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1997.tb01433.x · Cited by 113 · see citing works
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Steriade, M. (2001) · Cambridge University Press eBooks · doi:10.1017/cbo9780511541711 · Cited by 116 · see citing works
Abel, H. J., Lee, J. C. F., Callaway, J. C., & Foehring, R. C. (2004) · Journal of Neurophysiology · doi:10.1152/jn.00583.2003 · Cited by 110 · see citing works
Self-citationHaug, T. M., & Storm, J. F. (2000) · Journal of Neurophysiology · doi:10.1152/jn.2000.83.4.2071 · Cited by 110 · see citing works
“…norepinephrine, serotonin, dopamine, and histamine all suppressIsAHP, thus increasing the excitability of the target cells (Constanti and Sim 1987; Foehring et al. 1989; Haas and Konnerth 1983; Haas and Rose 1987; Madison and Nicoll 1982, 1984, 1986a,b; McCormick 1989; for reviews, see Nicoll…”
BackgroundPineda, J. C., Waters, R. S., & Foehring, R. C. (1998) · Journal of Neurophysiology · doi:10.1152/jn.1998.79.5.2522 · Cited by 109 · see citing works
“Possible ters (e.g., Araneda and Andrade 1991; Foehring et al. 1989;reasons for coexpression include, but are not limited to, difLorenzon and Foehring 1992, 1993; McCormick and Princeferential modulation of specific channel subtypes by trans1986; McCormick and Williamson 1989; Schwindt et…”
BackgroundSelf-citationSchwindt, P. C., Spain, W. J., & Crill, W. E. (1992) · Neuroscience · doi:10.1016/0306-4522(92)90166-y · Cited by 109 · see citing works
Self-citationMouradian, R. D., Sessler, F. M., & Waterhouse, B. D. (1991) · Brain Research · doi:10.1016/0006-8993(91)91162-t · Cited by 108 · see citing works
Huang, C., Hsu, K., & Pw, G. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-03-01026.1996 · Cited by 108 · see citing works
“Intracellular studies with both hippocampal and neocortical slices also showed that postsynaptic P-adrenergic receptors mediated the reduction of Ca’+- and Na’-dependent K+ currents (Madison and Nicoll, 1982; Foehring et al., 1989).”
ResultManunta, Y., & Edeline, J. (1999) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.1999.00633.x · Cited by 104 · see citing works
“The in vitro studies do not clarify the pharmacological pro®le of these inhibitory effects, as many authors focused on excitatory effects (Constanti & Sim, 1987; Foehring et al., 1989; Pape & McCormick, 1989; Mouradian et al., 1991; McCormick, 1992).”
BackgroundActions of noradrenaline on neocortical neurons in vitro
Dodt, H.-U., Pawelzik, H., & Zieglga¨nsberger, W. (1991) · Brain Research · doi:10.1016/0006-8993(91)91303-i · Cited by 104 · see citing works
The calcium-activated slow AHP: cutting through the Gordian knot
Andrade, R., Foehring, R. C., & Tzingounis, A. V. (2012) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2012.00047 · Cited by 101 · see citing works
“It should also be mentioned that the latter part of the sAHP in cat neocortical pyramidal neurons was not Ca2+-dependent but rather appeared due to a Na+-dependent potassium conductance (Foehring et al., 1989; Schwindt et al., 1989).”
BackgroundSelf-citationKim, U., & McCormick, D. A. (1998) · Journal of Neurophysiology · doi:10.1152/jn.1998.80.3.1222 · Cited by 95 · see citing works
“After preparation, slices vated K/ currents (Foehring et al. 1989; Schwindt et al. were placed in an interface-style recording chamber (Fine Sciences Tools) and allowed ¢2 h to recover.”
BackgroundMethodBistability, Causality, and Complexity in Cortical Networks: An In Vitro Perturbational Study
D’Andola, M., Rebollo, B., Casali, A. G., Weinert, J. F., Pigorini, A., Villa, R., Massimini, M., & Sanchez-Vives, M. V. (2017) · Cerebral Cortex · doi:10.1093/cercor/bhx122 · Cited by 92 · see citing works
“ability reflected in the emergent SOs, (2) in an “awake-like” state where neuronal bistability is reduced by bath application of norepinephrine (NE) and carbachol (CCh), drugs with effects largely mediated through blockade of K channels (Foehring et al. 1989; Schwindt et al. 1989), and (3) after bath application of ka…”
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Fung, S. J., Manzoni, D., Chan, J. Y. H., Pompeiano, O., & Barnes, C. D. (1991) · Progress in brain research · doi:10.1016/s0079-6123(08)63825-x · Cited by 91 · see citing works
Neuroplasticity Regulation by Noradrenaline in Mammalian Brain
Marzo, A., Bai, J., & Otani, S. (2009) · Current Neuropharmacology · doi:10.2174/157015909790031193 · Cited by 86 · see citing works
“This inhibition of potassium conductance may underlie the blockade of the slow after-hyperpolarization (AHP) current in the cortex [33], the thalamus (paratenial thalamic nucleus; [75, 76]), and the hippocampus [41, 42, 57, 65, 66].”
Spain, W. J., Schwindt, P. C., & Crill, W. E. (1991) · The Journal of Physiology · doi:10.1113/jphysiol.1991.sp018489 · Cited by 87 · see citing works
Self-citationBrown, M. R., Kronengold, J., Gazula, V., Spilianakis, C. G., Flavell, R. A., von Hehn, C. A. A., Bhattacharjee, A., & Kaczmarek, L. K. (2008) · The Journal of Physiology · doi:10.1113/jphysiol.2008.160861 · Cited by 81 · see citing works
Gain modulation by serotonin in pyramidal neurones of the rat prefrontal cortex
Zhang, Z., & Arsenault, D. (2005) · The Journal of Physiology · doi:10.1113/jphysiol.2005.086066 · Cited by 82 · see citing works
“Indeed, both ACh and NA have been shown to increase spike frequency and attenuate spike accommodation (Benardo & Prince, 1982; Madison & Nicoll, 1982; McCormick & Prince, 1987, 1988; Foehring et al. 1989).”
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McLean, J., & Waterhouse, B. D. (1994) · Brain Research · doi:10.1016/0006-8993(94)91716-7 · Cited by 79 · see citing works
Chapter 3: Catecholaminergic-cholinergic interaction in the basal forebrain
Záborszky, L., Cullinan, W. E., & Luine, V. N. (1993) · Progress in brain research · doi:10.1016/s0079-6123(08)62379-1 · Cited by 77 · see citing works
Adaptive changes in the developing brain during intrauterine stress
Amiel‐Tison, C., & Pettigrew, A. G. (1991) · Brain and Development · doi:10.1016/s0387-7604(12)80109-4 · Cited by 78 · see citing works
Noradrenergic Regulation of Fear and Drug-Associated Memory Reconsolidation
Otis, J. M., Werner, C. T., & Mueller, D. T. (2014) · Neuropsychopharmacology · doi:10.1038/npp.2014.243 · Cited by 74 · see citing works
“Similarly, b-AR activation decreases the conductance of ion-gated Kþ channels, reducing the slow and fast afterhyperpolarization that contribute to spike-frequency adaptation (Foehring et al, 1989; Mueller et al, 2008; Otis et al, 2013).”
BackgroundMethylphenidate facilitates and disinhibits the motor cortex in intact humans
Ilic, T. V., Korchounov, A., & Ziemann, U. (2003) · Neuroreport · doi:10.1097/00001756-200304150-00023 · Cited by 74 · see citing works
Kaczorowski, C. C., Disterhoft, J. F., & Spruston, N. (2006) · The Journal of Physiology · doi:10.1113/jphysiol.2006.124586 · Cited by 73 · see citing works
“Next, we set out to examine whether the action of NA was specific to blockade of a Ca2+-dependent K+ current (Madison & Nicoll, 1984, 1986), as opposed to inhibition of the Na+-mediated K+ current shown to underlie a late AHP in neocortical neurons (Foehring et al. 1989).”
MethodLayer- and area-specific actions of norepinephrine on cortical synaptic transmission
Salgado, H., Treviño, M., & Atzori, M. (2016) · Brain Research · doi:10.1016/j.brainres.2016.01.033 · Cited by 71 · see citing works
Actions of norepinephrine in the rat hippocampus
Segal, M., Markram, H., & Richter‐Levin, G. (1991) · Progress in brain research · doi:10.1016/s0079-6123(08)63819-4 · Cited by 71 · see citing works
Dryer, S. E. (1991) · The Journal of Physiology · doi:10.1113/jphysiol.1991.sp018522 · Cited by 70 · see citing works
Optimality and Robustness of a Biophysical Decision-Making Model under Norepinephrine Modulation
Eckhoff, P. A., Wong‐Lin, K., & Holmes, P. J. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.5024-08.2009 · Cited by 67 · see citing works
“Higher NE levels reduce membrane leak conductances, allowing cells to further depolarize (Foehring et al., 1989; McCormick and Pape, 1990).”
BackgroundGu, N., Hu, H., Vervaeke, K., & Storm, J. F. (2008) · Journal of Neurophysiology · doi:10.1152/jn.90433.2008 · Cited by 65 · see citing works
Norepinephrine effects on spinal motoneurons
White, S. R., Fung, S. J., & Barnes, C. D. (1991) · Progress in brain research · doi:10.1016/s0079-6123(08)63821-2 · Cited by 66 · see citing works
Law-Tho, D., Crépel, F., & Hirsch, J. C. (1993) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1993.tb00217.x · Cited by 65 · see citing works
“These results are similar to those reported in cells from the sensorimotor cortex (Foehring et al., 1989), the motor cortex (Dodt et al.”
BackgroundResultInfluentialChen, D., & Fetz, E. E. (2005) · Journal of Neurophysiology · doi:10.1152/jn.00024.2005 · Cited by 63 · see citing works
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MethodLecas, J.-C. (2004) · European Journal of Neuroscience · doi:10.1111/j.0953-816x.2004.03341.x · Cited by 63 · see citing works
Windhorst, U. (1990) · Progress in Neurobiology · doi:10.1016/0301-0082(90)90020-h · Cited by 61 · see citing works
Slow Adaptation in Fast-Spiking Neurons of Visual Cortex
Descalzo, V. F., Nowak, L. G., Brumberg, J. C., McCormick, D. A., & Sanchez-Vives, M. V. (2004) · Journal of Neurophysiology · doi:10.1152/jn.00658.2004 · Cited by 59 · see citing works
Herrero, I., & Sánchez‐Prieto, J. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.48.30554 · Cited by 59 · see citing works
Cortical Auditory Adaptation in the Awake Rat and the Role of Potassium Currents
Abolafia, J. M., Vergara, R. O., ARNOLD, M. M., Reig, R., & Sanchez-Vives, M. V. (2010) · Cerebral Cortex · doi:10.1093/cercor/bhq163 · Cited by 58 · see citing works
“The modulation of K + channels through adrenergic or cholinergic neurotransmitters (Foehring et al. 1989; Schwindt et al. 1989) could”
BackgroundInfluentialThe ontogeny of repetitive firing and its modulation by norepinephrine in rat neocortical neurons
Lorenzon, N. M., & Foehring, R. C. (1993) · Developmental Brain Research · doi:10.1016/0165-3806(93)90141-v · Cited by 58 · see citing works
Self-citationNa+-activated K+ channels are widely distributed in rat CNS and in Xenopus oocytes
Egan, T. M., Dagan, D., Kupper, J., & Levitan, I. B. (1992) · Brain Research · doi:10.1016/0006-8993(92)90913-t · Cited by 58 · see citing works
Moxon, K. A., Devilbiss, D. M., Chapin, J. K., & Waterhouse, B. D. (2007) · Brain Research · doi:10.1016/j.brainres.2007.02.006 · Cited by 56 · see citing works
“adrenoceptors and second-messenger cascades (Cheun & Yeh, 1992; 1996; Foehring et al., 1989; Madison & Nicoll, 1986b; Mouradian et al., 1991; Sessler et al., 1989; 1995; Waterhouse et al., 1981; 1982).”
BackgroundInfluentialAdrenergic Modulation of GABAAReceptor-Mediated Inhibition in Rat Sensorimotor Cortex
Bennett, B. D., Huguenard, J. R., & Prince, D. A. (1998) · Journal of Neurophysiology · doi:10.1152/jn.1998.79.2.937 · Cited by 56 · see citing works
“Epinephrine (Foehring et al. 1989; Madison and Nicoll 1986) and reduces(EPI; 10 mM) reversibly altered the amplitude of evoked IPSCs slow afterhyperpolarizations, thereby altering spike fre-(eIPSCs) in slices from postnatal day 9–12 (P9–12) and P15– quency accommodation (Dodt et al. 1991; Foehring…”
BackgroundEgo‐Stengel, V., Bringuier, V., & Shulz, D. E. (2002) · Neuroscience · doi:10.1016/s0306-4522(02)00011-8 · Cited by 53 · see citing works
“…of a facilitatory e¡ect of the iontophoresis of NE observed in this study while recording cortical cells extracellularly is di⁄cult to reconcile with the very well-documented increase in excitability to intracellular current injection observed in in vitro experiments (e.g. Foehring et al., 1989).”
BackgroundInfluentialBassant, M. H., Ennouri, K., & Lamour, Y. (1990) · Neuroscience · doi:10.1016/0306-4522(90)90279-d · Cited by 51 · see citing works
Paton, J. F. R., Foster, W. R., & Schwaber, J. S. (1993) · Brain Research · doi:10.1016/0006-8993(93)90358-t · Cited by 51 · see citing works
Koyanagi, Y., Yamamoto, K., Oi, Y., Koshikawa, N., & Kobayashi, M. (2010) · Journal of Neurophysiology · doi:10.1152/jn.00972.2009 · Cited by 50 · see citing works
“Isoproterenol effectively enhances repetitive firing frequency and decreases spike adaptation (Dodt et al. 1991; Foehring et al. 1989; Kobayashi et al. 2008a; Nowicky et al. 1992).”
BackgroundGuan, D., Armstrong, W. E., & Foehring, R. C. (2015) · Journal of Neurophysiology · doi:10.1152/jn.00524.2014 · Cited by 47 · see citing works
“The initial Ca2 - sensitive portion of the sAHP lasts 1–2 s and is mediated by unknown channels that are negatively modulated by transmitters that activate PKA (e.g., NE through -receptors; Andrade et al. 2012; Foehring et al. 1989).”
BackgroundInfluentialSelf-citationChanges of the EPSP Waveform Regulate the Temporal Window for Spike-Timing-Dependent Plasticity
Fuenzalida, M., de Sevilla, D. F., & Buño, W. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.0900-07.2007 · Cited by 47 · see citing works
Waterhouse, B. D., Mouradian, R., Sessler, F. M., & Lin, R. C. S. (2000) · Brain Research · doi:10.1016/s0006-8993(00)02261-7 · Cited by 45 · see citing works
Ionic conductance mechanisms contributing to the electrophysiological properties of neurons
Baxter, D. A., & Byrne, J. H. (1991) · Current Opinion in Neurobiology · doi:10.1016/0959-4388(91)90017-2 · Cited by 45 · see citing works
Ionic Currents Governing Input–Output Relations of Betz Cells
Schwindt, P. C. (1992) · Elsevier eBooks · doi:10.1016/b978-0-12-484815-3.50016-5 · Cited by 45 · see citing works
Self-citationHaimann, C., Magistretti, J., & Pozzi, B. (1992) · Pflügers Archiv · doi:10.1007/bf00376215 · Cited by 31 · see citing works
Sessler, F. M., Liu, W., Kirifides, M. L., Mouradian, R., Lin, R. C. S., & Waterhouse, B. D. (1995) · Brain Research · doi:10.1016/0006-8993(95)00060-4 · Cited by 39 · see citing works
Kobayashi, M., Kojima, M., Koyanagi, Y., Adachi, K., Imamura, K., & Koshikawa, N. (2008) · Synapse · doi:10.1002/syn.20604 · Cited by 36 · see citing works
“…other hand, several intracellular recording studies have demonstrated that activation of postsynaptic badrenoceptors increases firing frequency in response to intracellular depolarizing current pulse injection (Dodt et al., 1991; Foehring et al., 1989; Kobayashi et al., 2008; Nowicky et al., 1992).”
The mechanism of noradrenergic alpha 1 excitatory modulation of pontine reticular formation neurons
Stevens, D. R., McCarley, R. W., & Greene, R. (1994) · Journal of Neuroscience · doi:10.1523/jneurosci.14-11-06481.1994 · Cited by 37 · see citing works
“Similar action of p agonists have been reported in thalamus (McCormick and Prince, 1988) and cortex (Foehring et al., 1989).”
BackgroundSaar, D., & Barkai, E. (2009) · Molecular Neurobiology · doi:10.1007/s12035-009-8060-5 · Cited by 36 · see citing works
Lu, S., Das, P., Fadool, D. A., et al. (2010) · Journal of Neurophysiology · doi:10.1152/jn.00607.2009 · Cited by 36 · see citing works
Slow Synaptic Inhibition in Nucleus HVc of the Adult Zebra Finch
Schmidt, M. F., & Perkel, D. J. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-03-00895.1998 · Cited by 36 · see citing works
Learning-Induced Reversal of the Effect of Noradrenalin on the Postburst AHP
Brosh, I., Rosenblum, K., & Barkai, E. (2006) · Journal of Neurophysiology · doi:10.1152/jn.00376.2006 · Cited by 34 · see citing works
Warren, R. A., & Dykes, R. W. (1996) · Canadian Journal of Physiology and Pharmacology · doi:10.1139/y95-225 · Cited by 33 · see citing works
Hormigo, S., Horta‐Júnior, J. D. A. C., Gómez‐Nieto, R., & López, D. E. (2012) · Frontiers in Neural Circuits · doi:10.3389/fncir.2012.00041 · Cited by 33 · see citing works
“Modulators like NA might participate in stimulus-specific adaption given that NA blocks both Ca2+- and Na+-dependent K+ currents (Foehring et al., 1989).”
BackgroundWang, S.-J. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.04.053 · Cited by 32 · see citing works
Existence of glutamate in noradrenergic locus coeruleus neurons of rodents
Fung, S. J., Reddy, V. K., Liu, R.-H., Wang, Z., & Barnes, C. D. (1994) · Brain Research Bulletin · doi:10.1016/0361-9230(94)90164-3 · Cited by 32 · see citing works
Satake, T., Mitani, H., Nakagome, K., & Kaneko, K. (2008) · Brain Research · doi:10.1016/j.brainres.2008.06.098 · Cited by 31 · see citing works
“A defining feature of IsAHP is its regulation by a range of neuromodulators including NA (Foehring et al., 1989), muscarinic agonist (Schwindt et al., 1988b) and 5-HT (Villalobos et al., 2005), all of which potently block the slow currents (for a review see Nicoll, 1988; Vogalis et al., 2003).”
α2-Adrenergic receptor-mediated modulation of calcium current in neocortical pyramidal neurons
Timmons, S. D., Geisert, E. E., Stewart, A. E., Lorenzon, N. M., & Foehring, R. C. (2004) · Brain Research · doi:10.1016/j.brainres.2004.04.025 · Cited by 31 · see citing works
Self-citationKobayashi, M. (2007) · Neuroscience · doi:10.1016/j.neuroscience.2007.04.001 · Cited by 31 · see citing works
Wang, S. J., & Sihra, T. S. (2003) · Neuropharmacology · doi:10.1016/s0028-3908(03)00045-5 · Cited by 31 · see citing works
“These include modulation of ion-channel activities involved in nerve terminal excitability (Dunwiddie et al., 1992; Foehring et al., 1989; Madison and Nicoll, 1986), voltage-dependent Ca2+-channels (VDCCs) (Catterall, 2000), as well as direct effects on processes leading up to and including the secretory process itsel…”
InfluentialLee, S., Beak, S. K., Park, S. H., Waterhouse, B. D., & Lee, H. S. (2009) · The Journal of Comparative Neurology · doi:10.1002/cne.22012 · Cited by 31 · see citing works
“Despite continuous debate (Fritschy and Grzanna, 1990), the involvement of the LC in various motor functions has been repeatedly reported (Foehring et al., 1989; Fung et al., 1991; Pompeiano et al., 1991).”
Background
- Authors
- Foehring, R. C., Schwindt, P. C., & Crill, W. E.
- Affiliations
- University of Washington (US)
- ORCID
- Foehring, R. C.
- Venue
- Journal of Neurophysiology
- Publisher
- American Physiological Society
- Published
- 1989-02-01
- Volume
- 61
- Issue
- 2
- Pages
- 245-256
- ISSN
- 0022-3077 (ISSN-L)
- 1522-1598
- OpenAlex
- W2403611111
- Cited by
- 178
- References
- 0
- Citations by year
- 2026: 1 · 2025: 2 · 2022: 1 · 2021: 3 · 2020: 2 · 2019: 1 · 2018: 5 · 2017: 1 · 2016: 1 · 2015: 4 · 2014: 6 · 2013: 1 · 2012: 9
- FWCI
- 4.43
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Neurophysiology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute of Neurological Disorders and Stroke (NS16972, NS-22410, NS-70907)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ion channel regulation and function
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Keywords
- norepinephrine, Betz cells, neocortical neurons, slow afterhyperpolarization, neuronal excitability, spike frequency adaptation, beta-adrenergic receptors, isoproterenol, alpha-adrenergic receptors, alpha2-adrenoceptors
- MeSH terms
- Animals, Calcium, Cats, Cerebral Cortex, Electrophysiology, Ions, Membrane Potentials, Neurons, Norepinephrine, Potassium, Receptors, Adrenergic, Sodium, Sympathomimetics
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