Cited by 548Ion channel regulation and functionNeuroscience and Neuropharmacology ResearchCardiac electrophysiology and arrhythmias

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Calcium-dependent current generating the afterhyperpolarization of hippocampal neurons

Lancaster, B., Adams, P. R.·1986·Journal of Neurophysiology

DOI 10.1152/jn.1986.55.6.1268

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Abstract

A single-electrode voltage-clamp technique was employed on in vitro hippocampal slices to examine the membrane current responsible for the slow afterhyperpolarization (AHP) in CA1 pyramidal cells. This was achieved by using conventional procedures to evoke an AHP in current clamp, followed rapidly by a switch into voltage clamp (hybrid clamp). The AHP current showed a dependence on extracellular K+, which was close to that predicted for a K+ current by the Nernst equation. The AHP current could be blocked by Cd2+ or norepinephrine. Although the AHP current showed a requirement for voltage-dependent Ca2+ entry, the current did not show any clear intrinsic voltage dependence. Once activated, AHP current is not turned off by hyperpolarizing the membrane potential. The effects of norepinephrine, Cd2+, and tetraethylammonium (TEA) were used to identify an AHP current component to the outward current evoked by depolarizing voltage commands from holding potentials that approximate to the resting potential for these cells. The AHP current can contribute significantly to the outward current during the depolarizing command. Upon repolarization it is evident as a slow outward tail current. This slow tail current had the same time constant as AHP currents evoked by hybrid clamp. Fast components to the tail currents were also observed. These were sensitive to Cd2+ and TEA. They probably represent a voltage-sensitive gKCa, sometimes termed C-current. The strong sensitivity to voltage and TEA displayed by the conventionally described gKCa (IC) are properties inconsistent with the AHP. It seems likely that the AHP current (IAHP) represents a Ca2+-activated K+ current separate from IC and that these two currents coexist in the same cell.

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Background
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Method
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Background
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Background
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Background
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Background
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Background
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BackgroundResult
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Background
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Method
The transient potassium current, the A-current, is involved in spike frequency adaptation in rat amygdala neurons
Gean, P., & Shinnick‐Gallagher, P. (1989) · Brain Research · doi:10.1016/0006-8993(89)91578-3 · Cited by 39
The Molecular Basis for the Calcium-Dependent Slow Afterhyperpolarization in CA1 Hippocampal Pyramidal Neurons
Sahu, G., & Turner, R. W. (2021) · Frontiers in Physiology · doi:10.3389/fphys.2021.759707 · Cited by 39
Network Excitability Dysfunction in Alzheimer's Disease: Insights from In Vitro and In Vivo Models
Santos, S. F., Pierrot, N., & Octave, J. (2010) · Reviews in the Neurosciences · doi:10.1515/revneuro.2010.21.3.153 · Cited by 37
Metrifonate Decreases sI AHP in CA1 Pyramidal Neurons In Vitro
POWER, J. M., Oh, M. M., & Disterhoft, J. F. (2001) · Journal of Neurophysiology · doi:10.1152/jn.2001.85.1.319 · Cited by 38
“Metrifonate Decreases sIAHP in CA1 Pyramidal Neurons In Vitro”
BackgroundMethod
Properties of Single Calcium‐activated Potassium Channels of Large Conductance in Rat Hippocampal Neurons in Culture
Wann, K. T., & Richards, C. D. (1994) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1994.tb00305.x · Cited by 38
“, 1985), and in central hippocampal neurons (Lancaster and Adams, 1986; Segal and Barker, 1986).”
Background
Caffeine response in pyramidal neurons freshly dissociated from rat hippocampus
Uneyama, H., Munakata, M., & Akaike, N. (1993) · Brain Research · doi:10.1016/0006-8993(93)90348-q · Cited by 37
Presynaptic localization of the small conductance calcium-activated potassium channel SK3 at the neuromuscular junction
Roncarati, R., Chio, M. D., Sava, A., Terstappen, G. C., & Fumagalli, G. F. (2001) · Neuroscience · doi:10.1016/s0306-4522(01)00066-5 · Cited by 37
Transient Hypoxemia Disrupts Anatomical and Functional Maturation of Preterm Fetal Ovine CA1 Pyramidal Neurons
McClendon, E., Wang, K., Degener-O’Brien, K., Hagen, M. W., Gong, X., Nguyen, T. D., Wu, W., Maylie, J., & Back, S. A. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.1364-19.2019 · Cited by 36
“Due to its long-lasting nature, the sAHP exerts the predominant influence on limiting repetitive firing in response to a sustained depolarization (Madison and Nicoll, 1984; Lancaster and Adams, 1986; Hille, 1992; Sah, 1996).”
Background
The afterhyperpolarization conductance exerts the same control over the gain and variability of motoneurone firing in anaesthetized cats
Manuel, M., Meunier, C., Donnet, M., et al. (2006) · The Journal of Physiology · doi:10.1113/jphysiol.2006.117002 · Cited by 36
“Email: daniel.zytnicki@univ-paris5.fr In many types of neurones, action potentials trigger a slow calcium-dependent potassium current that provokes an afterhyperpolarization (AHP) (Llinas & Yarom, 1981; Lancaster & Adams, 1986; Schwindt et al. 1988; Wilson et al. 2004).”
Background
Modulation of a Slowly Inactivating Potassium Current,ID, by Metabotropic Glutamate Receptor Activation in Cultured Hippocampal Pyramidal Neurons
Wu, R.-L., & Barish, M. E. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-16-06825.1999 · Cited by 36
“…IAHP and IM after mGluR activation by quisqualate was described by Charpak et al. (1990), but neither IAHP nor IM is blocked by 4-AP or TEA (Brown and Adams, 1980; Lancaster and Adams, 1986), both of which affect ID, and the kinetics of IM is quite different from that of ID (Brown and Adams, 1980).”
Background
Long-lasting enhancement of synaptic excitability of CA1/subiculum neurons of the rat ventral hippocampus by vasopressin and vasopressin(4–8)
Chepkova, A. N., French, P. J., de Wied, D., Ontskul, A. H., Ramakers, G. M. J., Skrebitski, V. G., Gispen, W. H., & Urban, I. J. A. (1995) · Brain Research · doi:10.1016/0006-8993(95)01006-7 · Cited by 36
“Although antidromic stimulation was not used to identify the neurons tested, the average R~N) and the appearance of after-hyperpolarization following an action potential in response to depolarizing current were similar to those observed in pyramidal neurons by others [7,37], suggesting that the majority of these neuro…”
BackgroundResult
Cholinergic Modulation of the Action Potential in Rat Hippocampal Neurons
Figenschou, A. N., Hu, G., & Storm, J. F. (1996) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1996.tb01182.x · Cited by 35
Novel action of BAPTA series chelators on intrinsic K+ currents in rat hippocampal neurones
Lancaster, B., & Batchelor, A. M. (2000) · The Journal of Physiology · doi:10.1111/j.1469-7793.2000.t01-1-00231.x · Cited by 32
“Although these experiments were executed without K¤ channel blockers and are comparable to IsAHP recorded following brief spike trains (Lancaster & Adams, 1986), supranormal IsAHP can be evoked in the presence of tetraethylammonium which causes spike broadening by blocking BK channels so Ca¥ influx…”
MethodResultSelf-citation
Space-rate coding in an adaptive silicon neuron
Hynna, K. M., & Boahen, K. A. (2001) · Neural Networks · doi:10.1016/s0893-6080(01)00082-x · Cited by 34
Electrophysiological changes in rat hippocampal pyramidal neurons produced by cholecystokinin octapeptide
Shinohara, S., & Kawasaki, K. (1997) · Neuroscience · doi:10.1016/s0306-4522(96)00653-7 · Cited by 34
Somato-dendritic mechanisms underlying the electrophysiological properties of hypothalamic magnocellular neuroendocrine cells: A multicompartmental model study
Komendantov, A. O., Trayanova, N. A., & Tasker, J. G. (2007) · Journal of Computational Neuroscience · doi:10.1007/s10827-007-0024-z · Cited by 32
“…action potentials and the generation of the fast afterhyperpolarizing potential (AHP) or hyperpolarizing afterpotential in many types of neurons (Lancaster and Adams 1986; Lancaster and Nicoll 1987; MacDermott and Weight 1982; Womack and Khodakhah 2002), including MNCs (Dopico et al. 1999), SK…”
BackgroundInfluential
Age-induced changes in electrophysiological responses of neostriatal neurons recorded in vitro
Cepeda, C., Lee, N., Buchwald, N. A., Radisavljevic, Z., & Levine, M. S. (1992) · Neuroscience · doi:10.1016/0306-4522(92)90325-v · Cited by 32
A slowly activating Ca(2+)‐dependent K+ current that plays a role in termination of swimming in Xenopus embryos.
Wall, M. J., & Dale, N. (1995) · The Journal of Physiology · doi:10.1113/jphysiol.1995.sp020900 · Cited by 33
Activity-Dependent [Ca2+]i Changes in Guinea Pig Vagal Motoneurons: Relationship to the Slow Afterhyperpolarization
Lasser‐Ross, N., Ross, W. N., & Yarom, Y. (1997) · Journal of Neurophysiology · doi:10.1152/jn.1997.78.2.825 · Cited by 33
Individual and additive effects of neuromodulators on the slow components of afterhyperpolarization currents in layer V pyramidal cells of the rat medial prefrontal cortex
Satake, T., Mitani, H., Nakagome, K., & Kaneko, K. (2008) · Brain Research · doi:10.1016/j.brainres.2008.06.098 · Cited by 34
“…currents largely result from calciumactivated conductances, 2) that they could be distinguished based upon their different sensitivity to apamin (Lancaster and Adams, 1986; Faber and Sah, 2002), and 3) that ImAHP contributes little to spike frequency modulation in layer V pyramidal cells of the…”
Functional significance of the apamin-sensitive conductance in rat locus coeruleus neurons
Osmanovic, S. S., Shefner, S. A., & Brodie, M. S. (1990) · Brain Research · doi:10.1016/0006-8993(90)91296-s · Cited by 32
The Cortical Neuron as an Electrophysiological Unit
Gutnick, M. J., & Crill, W. E. (1995) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780195083309.003.0003 · Cited by 32
Effects of vasopressin and related peptides on neurons of the rat lateral septum and ventral hippocampus
Urban, I. J. A. (1999) · Progress in brain research · doi:10.1016/s0079-6123(08)61576-9 · Cited by 31
Alterations in Ca2+-Buffering in Prion-Null Mice: Association with Reduced Afterhyperpolarizations in CA1 Hippocampal Neurons
Powell, A. D., Toescu, E. C., Collinge, J., & Jefferys, J. G. R. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.0675-08.2008 · Cited by 31
“The slow AHP is a property found in many neurons, which is evoked by repetitive action potentials, can last for several seconds and reduces the likelihood of subsequent action potential firing (Lancaster and Adams, 1986).”
Background
Control of IsAHP in mouse hippocampus CA1 pyramidal neurons by RyR3-mediated calcium-induced calcium release
van de Vrede, Y., Fossier, P., Baux, G., Joëls, M., & Chameau, P. J. P. (2007) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-007-0277-4 · Cited by 31
“The sAHP current (IsAHP) has slow kinetics, is mostly evoked after a train of action potentials, and induces accommodation of cell firing [22, 23, 26].”
Background
1-Ethyl-2-benzimidazolinone (EBIO) suppresses epileptiform activity in in vitro hippocampus
Garduño, J., Galván, E. J., de Sevilla, D. F., & Buño, W. (2005) · Neuropharmacology · doi:10.1016/j.neuropharm.2005.03.021 · Cited by 31
Activation kinetics of the slow afterhyperpolarization in hippocampal CA1 neurons
Maylie, J., Adelman, J. P., & Gerlach, A. C. (2004) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-003-1237-2 · Cited by 31
“10-fold slower than the medium component [8, 19].”
BackgroundResultInfluential

Authors: Lancaster, B., & Adams, P. R.
ORCID: Adams, P. R.
Venue: Journal of Neurophysiology
Publisher: American Physiological Society
Published: 1986-06-01
Volume: 55
Issue: 6
Pages: 1268-1282
ISSN: 0022-3077 (ISSN-L)
1522-1598
DOI: 10.1152/jn.1986.55.6.1268
OpenAlex: W1876408798
Cited by: 547
References: 0
Citations by year: 2026: 1 · 2025: 1 · 2024: 4 · 2023: 4 · 2022: 2 · 2021: 5 · 2020: 4 · 2019: 8 · 2018: 6 · 2017: 5 · 2016: 4 · 2015: 3 · 2014: 1 · 2013: 7 · 2012: 11
FWCI: 9.16
Type: journal article
Language: en
Open access: closed
Locations: Journal of Neurophysiology (publishedVersion)
PubMed (publishedVersion)
Funders: National Institute of Neurological Disorders and Stroke (NS18579)
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
Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Cardiac electrophysiology and arrhythmias
Keywords: afterhyperpolarization, calcium-activated potassium current, CA1 pyramidal neurons, tetraethylammonium sensitivity, cadmium block, norepinephrine, voltage-gated potassium channels
MeSH terms: Action Potentials, Animals, Calcium, Hippocampus, Ion Channels, Kinetics, Neural Conduction, Synaptic Transmission, Potassium, Rats, In Vitro Techniques

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Calcium-dependent current generating the afterhyperpolarization of hippocampal neurons

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