Influence of anomalous rectifier activation on afterhyperpolarizations of neurons from cat sensorimotor cortex in vitro
Abstract
1. Large neurons from layer V of cat sensorimotor cortex (Betz cells) were studied to determine the influence of the anomalous rectifier current (IAR) on slow afterhyperpolarizations (AHPs). The neurons were examined using intracellular recording and single-microelectrode voltage clamp in an in vitro brain slice preparation. 2. A faster medium-duration AHP (mAHP) and slower AHP (sAHP) followed repetitive firing (22, 23). The amplitude of the mAHP often increased or remained constant during membrane potential hyperpolarization. The membrane potential trajectory resulting solely from IAR activation was similar to the mAHP. 3. Postrepetitive firing voltage clamp was used to measure directly slowly decaying K+ currents (IK) and IAR at different membrane potentials. IK exhibited both a fast and slow decay. The time constants of the fast decay of IK and IAR activation were similar. IAR increased with hyperpolarization or raised extracellular K+ concentration [( K+]o), whereas both the fast and slow components of IK reversed or nulled near -100 mV and behaved as pure K+ currents in response to raised [K+]o. 4. To determine the precise contribution of IK and IAR to the AHP waveform, theoretical AHPs were computed using a quantitative model based on voltage-clamp measurements. The calculated AHPs were qualitatively similar to measured AHPs. The amplitude of the mAHP showed little change with hyperpolarization because of the increasing dominance of IAR at more negative membrane potentials. The sAHP was little affected by IAR activation. 5. Several model parameters subject to biological variation among Betz cells were varied in the calculations to determine their importance in the AHP waveform. With IK parameters held constant, the amplitude and time course of the mAHP depended on resting potential, membrane time constant, the kinetics of the anomalous rectifier conductance (GAR), and the maximum value of GAR. IAR activation could result in a biphasic AHP even when the fast decay of IK was omitted from the calculations. 6. A wider variation of model parameters revealed behavior that may be relevant to other neurons. Certain values of membrane or IAR activation time constants resulted in a monophasic AHP even when the fast decay of IK was present. The decay of a biphasic AHP could reflect either the onset of IAR or the fast decay of IK, depending on the relative value of their time constants. Procedures are outlined to discriminate between these possibilities using current clamp methods.(ABSTRACT TRUNCATED AT 400 WORDS)
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Activation of mAChRs on cortical pyramidal neurons increases excitability via Ca2+-dependent potassium channels.
“increases excitability via Ca2+-dependent potassium channels177–179”
From Mechanisms underlying gain modulation in the cortex (2020) · cites this paper as [179]
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Lytton, W. W., & Sejnowski, T. J. (1991) · Journal of Neurophysiology · doi:10.1152/jn.1991.66.3.1059 · Cited by 432 · see citing works
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Bayliss, D. A., Viana, F., Bellingham, M. C., & Berger, A. J. (1994) · Journal of Neurophysiology · doi:10.1152/jn.1994.71.1.119 · Cited by 158 · see citing works
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Reyes, A. D., & Fetz, E. E. (1993) · Journal of Neurophysiology · doi:10.1152/jn.1993.69.5.1661 · Cited by 142 · see citing works
Larkman, P. M., & Kelly, J. S. (1992) · The Journal of Physiology · doi:10.1113/jphysiol.1992.sp019347 · Cited by 129 · see citing works
Electrophysiological classes of neocortical neurons.
Contreras, D. (2004) · Neural Networks · doi:10.1016/j.neunet.2004.04.003 · Cited by 124 · see citing works
Lopez-Garcia, J. A., & King, A. E. (1994) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1994.tb00594.x · Cited by 111 · see citing works
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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
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Ren, Y., Barnwell, L. F., Alexander, J. C., Lubin, F. D., Adelman, J. P., Pfaffinger, P. J., Schrader, L. A., & Anderson, A. E. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m513125200 · Cited by 103 · see citing works
Contribution of Outward Currents to Spike-Frequency Adaptation in Hypoglossal Motoneurons of the Rat
Sawczuk, A., Powers, R. K., & Binder, M. D. (1997) · Journal of Neurophysiology · doi:10.1152/jn.1997.78.5.2246 · Cited by 88 · see citing works
“One possibility is that the depolarization associated with the onset of repetitive discharge leads to the deactivation of an inward rectifier current (Ih) , that contributes to the early decline in firing rate (Schwindt et al. 1988a; Spain et al. 1987).”
BackgroundMethodResultInfluentialFranceschetti, S., Lavazza, T., Curia, G., Aracri, P., Panzica, F., Sancini, G., AVANZINI, G., & Magistretti, J. (2003) · Journal of Neurophysiology · doi:10.1152/jn.00695.2002 · Cited by 86 · see citing works
“rectifying currents) (Foehring and Waters 1991; Schwindt et al. 1988).”
InfluentialPasquale, E. D., Keegan, K. D., & Noebels, J. L. (1997) · Journal of Neurophysiology · doi:10.1152/jn.1997.77.2.621 · Cited by 75 · see citing works
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Electrophysiological properties of hypoglossal motoneurons of guinea-pigs studied in vitro
Laursen, A. M., & Rekling, J. C. (1989) · Neuroscience · doi:10.1016/0306-4522(89)90156-5 · Cited by 63 · see citing works
van Brederode, J. F. M., & Snyder, G. L. (1992) · Neuroscience · doi:10.1016/0306-4522(92)90426-3 · Cited by 55 · see citing works
Potassium currents in motoneurones
McLarnon, J. G. (1995) · Progress in Neurobiology · doi:10.1016/0301-0082(95)00032-1 · Cited by 54 · see citing works
Guan, D., Armstrong, W. E., & Foehring, R. C. (2015) · Journal of Neurophysiology · doi:10.1152/jn.00524.2014 · Cited by 47 · see citing works
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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
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Pape, H. (1994) · Neuroscience · doi:10.1016/0306-4522(94)90602-5 · Cited by 44 · see citing works
Ping, H., & Shepard, P. D. (1999) · Journal of Neurophysiology · doi:10.1152/jn.1999.81.3.977 · Cited by 41 · see citing works
Zhu, J., Uhlrich, D. J., & Lytton, W. W. (1999) · Neuroscience · doi:10.1016/s0306-4522(98)00759-3 · Cited by 33 · see citing works
The role of L-type calcium channels in neuronal excitability and aging
Moore, S. J., & Murphy, G. G. (2020) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2020.107230 · Cited by 31 · see citing works
A TTX-sensitive conductance underlying burst firing in isolated pyramidal neurons from rat neocortex
Guatteo, E., Franceschetti, S., Bacci, A., et al. (1996) · Brain Research · doi:10.1016/s0006-8993(96)00866-9 · Cited by 31 · see citing works
“TTX-sensitive shoulder spikes [12,16,36] can also be recorded in slices in the presence of intracellular Cs + and by blocking Ca 2+ con-”
BackgroundResultPostsynaptic depression induced by isoflurane and Althesin in neocortical neurons
El‐Beheiry, H., & Puil, E. (1989) · Experimental Brain Research · doi:10.1007/bf00247942 · Cited by 29 · see citing works
Electrophysiological Roles of L-Type Channels in Different Classes of Guinea Pig Sympathetic Neuron
Davies, P., Ireland, D. R., Martínez‐Pinna, J., et al. (1999) · Journal of Neurophysiology · doi:10.1152/jn.1999.82.2.818 · Cited by 24 · see citing works
Evidence for a persistent sodium conductance in neurons from the nucleus prepositus hypoglossi
Reckling, J. C., & Laursen, A. M. (1989) · Brain Research · doi:10.1016/0006-8993(89)90323-5 · Cited by 24 · see citing works
Computer model of ethosuximide's effect on a thalamic neuron
Lytton, W. W., & B, T. J. S. A. (1992) · Annals of Neurology · doi:10.1002/ana.410320204 · Cited by 23 · see citing works
Schlichter, R., Bader, C. R., & Bernheim, L. (1991) · The Journal of Physiology · doi:10.1113/jphysiol.1991.sp018786 · Cited by 22 · see citing works
The burst firing in the layer III and V pyramidal neurons of the cat sensorimotor cortex in vitro
Nishimura, Y., Kitagawa, H., Saitoh, K., et al. (1996) · Brain Research · doi:10.1016/0006-8993(96)00505-7 · Cited by 21 · see citing works
Preferential Inhibition of I h in Rat Trigeminal Ganglion Neurons by an Organic Blocker
Janigro, D., Martenson, M. E., & Baumann, T. (1997) · The Journal of Membrane Biology · doi:10.1007/s002329900299 · Cited by 19 · see citing works
“Cesium ions have been extensively used as a tool for suppressing mixed Na /K currents in neurons [24, 25, 36], but due to their poor specificity and steep voltage-dependence, Cs + blocking actions have been difficult to interpret.”
McCarren, M., Potter, B. V. L., & Miller, R. J. (1989) · Neuron · doi:10.1016/0896-6273(89)90205-5 · Cited by 18 · see citing works
Shibuya, H., & Yamamoto, T. (1998) · Neuroscience · doi:10.1016/s0306-4522(97)00609-x · Cited by 17 · see citing works
Boucetta, S., Crochet, S., Chauvette, S., Seigneur, J., & Timofeev, I. (2012) · Experimental Neurology · doi:10.1016/j.expneurol.2012.12.001 · Cited by 15 · see citing works
Delayed and prolonged effects of a near threshold EPSP on the firing time of human α‐motoneurones
Mattei, B., & Schmied, A. (2002) · The Journal of Physiology · doi:10.1113/jphysiol.2001.012701 · Cited by 12 · see citing works
Hwa, G. G. C., & Avoli, M. (1991) · Epilepsia · doi:10.1111/j.1528-1157.1991.tb05529.x · Cited by 11 · see citing works
Cui, E., & Strowbridge, B. W. (2019) · eLife · doi:10.7554/elife.44954 · Cited by 9 · see citing works
“…channels (BK) channels like contribute to the fastest AHP (Gu et al., 2005) while multiple currents appear contribute to the medium AHP, including SK channels (Schwindt et al., 1988a), I-H (Spain et al., 1987, Schwindt et al., 1988, Gu et al., 2005) and the M current (Storm, 1989, Gu et al., 2005).”
BackgroundResultLarkman, P. M., & Kelly, J. S. (1995) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(94)00191-i · Cited by 9 · see citing works
Opioid-Induced Reductions in Amygdala Lateral Paracapsular GABA Neuron Circuit Activity
Ronström, J. W., Johnson, N. L., Jones, S. T., Werner, S. J., Wadsworth, H. A., Brundage, J., Stolp, V., Graziane, N., Silberman, Y., Steffensen, S. C., et al. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24031929 · Cited by 6 · see citing works
“These channels are shown to regulate neuronal firing frequency in various parts of the central nervous system by contributing to the AHP of an action potential [68,69].”
BackgroundElectrophysiological aspects of 5-HT receptor-mediated adenylyl cyclase activation
Larkman, P. M. (1995) · Seminars in Neuroscience · doi:10.1016/1044-5765(95)90002-0 · Cited by 3 · see citing works
Membrane Properties of Cat Betz Cells Studied In Vitro
Crill, W. E., Schwindt, P. C., & Spain, W. J. (1990) · Birkhäuser Boston eBooks · doi:10.1007/978-1-4684-6767-3_5 · Cited by 2 · see citing works
Self-citationEffect of Background Synaptic Activity on Excitatory-Postsynaptic Potential-Spike Coupling
Zsiros, V. (2003) · doi:10.21007/etd.cghs.2003.0387
“Although we know more about the ionic mechanisms underlying the refractory period (Hodgkin and Huxley, 1952, Schwindt et al., 1988b, Schwindt et al., 1988a, Schwindt et al., 1989, Spain et al., 1991, Schwindt et al., 1992, Sah and Faber, 2002), its role in neuronal integration is not well…”
BackgroundSeigneur, J. (2013) · Corpus Université Laval (Université Laval)
- Authors
- Schwindt, P. C., Spain, W. J., & Crill, W. E.
- Affiliations
- University of Washington (US)
- ORCID
- Spain, W. J.
- Venue
- Journal of Neurophysiology
- Publisher
- American Physiological Society
- Published
- 1988-02-01
- Volume
- 59
- Issue
- 2
- Pages
- 468-481
- ISSN
- 0022-3077 (ISSN-L)
- 1522-1598
- OpenAlex
- W2404561157
- Cited by
- 55
- References
- 0
- Citations by year
- 2023: 1 · 2020: 2 · 2019: 1 · 2015: 1 · 2013: 1 · 2012: 1
- FWCI
- 1.45
- 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, NS01166)
- 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
- afterhyperpolarization, Betz cells, sensorimotor cortex, layer V neurons, potassium currents, repetitive firing, membrane time constant, extracellular potassium, hyperpolarization, neuronal excitability
- MeSH terms
- Animals, Cats, Electrophysiology, Models, Neurological, Motor Cortex, Neurons, Somatosensory Cortex, In Vitro Techniques
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