XB-ART-42860
J Neurophysiol
2011 May 01;1055:2487-500. doi: 10.1152/jn.00779.2010.
Show Gene links
Show Anatomy links
Pharmacology of currents underlying the different firing patterns of spinal sensory neurons and interneurons identified in vivo using multivariate analysis.
Winlove CI
,
Roberts A
.
???displayArticle.abstract???
The operation of neuronal networks depends on the firing patterns of the network's neurons. When sustained current is injected, some neurons in the central nervous system fire a single action potential and others fire repetitively. For example, in Xenopus laevis tadpoles, primary-sensory Rohon-Beard (RB) neurons fired a single action potential in response to 300-ms rheobase current injections, whereas dorsolateral (DL) interneurons fired repetitively at 10-20 Hz. To investigate the basis for these differences in vivo, we examined drug-induced changes in the firing patterns of Xenopus spinal neurons using whole cell current-clamp recordings. Neuron types were initially separated through cluster analysis, and we compared results produced using different clustering algorithms. We used these results to develop a predictive function to classify subsequently recorded neurons. The potassium channel blocker tetraethylammonium (TEA) converted single-firing RB neurons to low-frequency repetitive firing but reduced the firing frequency of repetitive-firing DL interneurons. Firing frequency in DL interneurons was also reduced by the potassium channel blockers 4-aminopyridine (4-AP), catechol, and margatoxin; 4-AP had the greatest effect. The calcium channel blockers amiloride and nimodipine had few effects on firing in either neuron type but reduced action potential duration in DL interneurons. Muscarine, which blocks M-currents, did not affect RB neurons but reduced firing frequency in DL interneurons. These results suggest that potassium currents may control neuron firing patterns: a TEA-sensitive current prevents repetitive firing in RB neurons, whereas a 4-AP-sensitive current underlies repetitive firing in DL interneurons. The cluster and discriminant analysis described could help to classify neurons in other systems.
???displayArticle.pubmedLink??? 21346204
???displayArticle.pmcLink??? PMC3094184
???displayArticle.link??? J Neurophysiol
???displayArticle.grants??? [+]
Biotechnology and Biological Sciences Research Council , BB/G006652/1 Biotechnology and Biological Sciences Research Council , BB_BB/G006652/1 Biotechnology and Biological Sciences Research Council
Species referenced: Xenopus laevis
References [+] :
Abdulla,
Axotomy- and autotomy-induced changes in the excitability of rat dorsal root ganglion neurons.
2001, Pubmed
Abdulla, Axotomy- and autotomy-induced changes in the excitability of rat dorsal root ganglion neurons. 2001, Pubmed
Adams, M-currents and other potassium currents in bullfrog sympathetic neurones. 1982, Pubmed
Aiken, Xenopus embryonic spinal neurons recorded in situ with patch-clamp electrodes--conditional oscillators after all? 2003, Pubmed , Xenbase
Aiken, Reduction of spike frequency adaptation and blockade of M-current in rat CA1 pyramidal neurones by linopirdine (DuP 996), a neurotransmitter release enhancer. 1995, Pubmed
Alexander, Guide to Receptors and Channels (GRAC), 3rd edition. 2008, Pubmed
Allen, M1 and M2 muscarinic receptors mediate excitation and inhibition of guinea-pig intracardiac neurones in culture. 1990, Pubmed
Baccaglini, Developmental changes in the inward current of the action potential of Rohon-Beard neurones. 1977, Pubmed , Xenbase
Baccei, Intrinsic firing properties of developing rat superficial dorsal horn neurons. 2005, Pubmed
Baranauskas, Kv3.4 subunits enhance the repolarizing efficiency of Kv3.1 channels in fast-spiking neurons. 2003, Pubmed
Barish, Differentiation of voltage-gated potassium current and modulation of excitability in cultured amphibian spinal neurones. 1986, Pubmed
Barry, JPCalc, a software package for calculating liquid junction potential corrections in patch-clamp, intracellular, epithelial and bilayer measurements and for correcting junction potential measurements. 1994, Pubmed
Beurrier, Subthalamic nucleus neurons switch from single-spike activity to burst-firing mode. 1999, Pubmed
Bi, Synaptic modifications in cultured hippocampal neurons: dependence on spike timing, synaptic strength, and postsynaptic cell type. 1998, Pubmed
Brodin, Effects of magnesium on fictive locomotion induced by activation of N-methyl-D-aspartate (NMDA) receptors in the lamprey spinal cord in vitro. 1986, Pubmed
Brown, Muscarinic suppression of a novel voltage-sensitive K+ current in a vertebrate neurone. 1980, Pubmed
Brumberg, Ionic mechanisms underlying repetitive high-frequency burst firing in supragranular cortical neurons. 2000, Pubmed
Buchanan, Electrophysiological properties of identified classes of lamprey spinal neurons. 1993, Pubmed
Buss, Membrane properties related to the firing behavior of zebrafish motoneurons. 2003, Pubmed
Catacuzzeno, The differential expression of low-threshold K+ currents generates distinct firing patterns in different subtypes of adult mouse trigeminal ganglion neurones. 2008, Pubmed
Cauli, Classification of fusiform neocortical interneurons based on unsupervised clustering. 2000, Pubmed
Chandler, Electrophysiological properties of guinea pig trigeminal motoneurons recorded in vitro. 1994, Pubmed
Clarke, Sensory physiology, anatomy and immunohistochemistry of Rohon-Beard neurones in embryos of Xenopus laevis. 1984, Pubmed , Xenbase
Connor, Inward and delayed outward membrane currents in isolated neural somata under voltage clamp. 1971, Pubmed
Connor, Voltage clamp studies of a transient outward membrane current in gastropod neural somata. 1971, Pubmed
Connors, Electrophysiological properties of neocortical neurons in vitro. 1982, Pubmed
Dale, Ion channels and the control of swimming in the Xenopus embryo. 1997, Pubmed , Xenbase
Deuchars, Properties of interneurones in the intermediolateral cell column of the rat spinal cord: role of the potassium channel subunit Kv3.1. 2001, Pubmed
Eckert, Interference of biocytin with opioid-evoked hyperpolarization and membrane properties of rat spinal substantia gelatinosa neurons. 2001, Pubmed
Erisir, Function of specific K(+) channels in sustained high-frequency firing of fast-spiking neocortical interneurons. 1999, Pubmed
Feldman, Synaptic plasticity at thalamocortical synapses in developing rat somatosensory cortex: LTP, LTD, and silent synapses. 1999, Pubmed
Fenwick, Sodium and calcium channels in bovine chromaffin cells. 1982, Pubmed
Fox, Kinetic and pharmacological properties distinguishing three types of calcium currents in chick sensory neurones. 1987, Pubmed
Fuhrmann, Coding of temporal information by activity-dependent synapses. 2002, Pubmed
Gamkrelidze, The differential expression of low-threshold sustained potassium current contributes to the distinct firing patterns in embryonic central vestibular neurons. 1998, Pubmed
Garcia-Calvo, Purification, characterization, and biosynthesis of margatoxin, a component of Centruroides margaritatus venom that selectively inhibits voltage-dependent potassium channels. 1993, Pubmed
Garrido-Sanabria, Electrophysiological and morphological heterogeneity of slow firing neurons in medial septal/diagonal band complex as revealed by cluster analysis. 2007, Pubmed
Gerstner, Neural codes: firing rates and beyond. 1997, Pubmed
Getchell, Responses of olfactory receptor cells to step pulses of odour at different concentrations in the salamander. 1978, Pubmed
González-Burgos, Functional properties of fast spiking interneurons and their synaptic connections with pyramidal cells in primate dorsolateral prefrontal cortex. 2005, Pubmed
Grolleau, Dorsal unpaired median neurones in the insect central nervous system: towards a better understanding of the ionic mechanisms underlying spontaneous electrical activity. 2000, Pubmed
Gurantz, Temporal regulation of Shaker- and Shab-like potassium channel gene expression in single embryonic spinal neurons during K+ current development. 1996, Pubmed , Xenbase
Halabisky, Electrophysiological classification of somatostatin-positive interneurons in mouse sensorimotor cortex. 2006, Pubmed
Halliwell, Voltage-clamp analysis of muscarinic excitation in hippocampal neurons. 1982, Pubmed
Helmstaedter, L2/3 interneuron groups defined by multiparameter analysis of axonal projection, dendritic geometry, and electrical excitability. 2009, Pubmed
Hess, Characterization of a high-voltage-activated IA current with a role in spike timing and locomotor pattern generation. 2001, Pubmed
Hochman, Membrane properties of deep dorsal horn neurons from neonatal rat spinal cord in vitro. 1997, Pubmed
Hochner, Action-potential duration and the modulation of transmitter release from the sensory neurons of Aplysia in presynaptic facilitation and behavioral sensitization. 1986, Pubmed
Hodgkin, The local electric changes associated with repetitive action in a non-medullated axon. 1948, Pubmed
HODGKIN, The effect of temperature on the electrical activity of the giant axon of the squid. 1949, Pubmed
Hopkins, Toxin and subunit specificity of blocking affinity of three peptide toxins for heteromultimeric, voltage-gated potassium channels expressed in Xenopus oocytes. 1998, Pubmed , Xenbase
Hounsgaard, Intrinsic determinants of firing pattern in Purkinje cells of the turtle cerebellum in vitro. 1988, Pubmed
Hsiao, Intrinsic membrane properties and morphological characteristics of interneurons in the rat supratrigeminal region. 2007, Pubmed
Inokuchi, The effects of catechol on various membrane conductances in lumbar sympathetic postganglionic neurones of the guinea-pig. 1997, Pubmed
Ito, Catechol: a potent and specific inhibitor of the fast potassium channel in frog primary afferent neurones. 1986, Pubmed
Iwasaki, Low-voltage-activated potassium channels underlie the regulation of intrinsic firing properties of rat vestibular ganglion cells. 2008, Pubmed
Jentsch, Neuronal KCNQ potassium channels: physiology and role in disease. 2000, Pubmed
Johnston, Active properties of neuronal dendrites. 1996, Pubmed
Karagiannis, Classification of NPY-expressing neocortical interneurons. 2009, Pubmed
Karube, Axon branching and synaptic bouton phenotypes in GABAergic nonpyramidal cell subtypes. 2004, Pubmed
Knaus, [125I]margatoxin, an extraordinarily high affinity ligand for voltage-gated potassium channels in mammalian brain. 1995, Pubmed
Krahe, Burst firing in sensory systems. 2004, Pubmed
Kuenzi, The pharmacology and roles of two K+ channels in motor pattern generation in the Xenopus embryo. 1998, Pubmed , Xenbase
Kupper, Recombinant Kv1.3 potassium channels stabilize tonic firing of cultured rat hippocampal neurons. 2002, Pubmed
Lamborghini, Rohon-beard cells and other large neurons in Xenopus embryos originate during gastrulation. 1980, Pubmed , Xenbase
Lazaroff, In vivo analysis of Kvbeta2 function in Xenopus embryonic myocytes. 2002, Pubmed , Xenbase
Lazaroff, Xenopus embryonic spinal neurons express potassium channel Kvbeta subunits. 1999, Pubmed , Xenbase
Li, The spinal interneurons and properties of glutamatergic synapses in a primitive vertebrate cutaneous flexion reflex. 2003, Pubmed , Xenbase
Li, Reconfiguration of a vertebrate motor network: specific neuron recruitment and context-dependent synaptic plasticity. 2007, Pubmed , Xenbase
Li, Dorsal spinal interneurons forming a primitive, cutaneous sensory pathway. 2004, Pubmed , Xenbase
Li, Defining classes of spinal interneuron and their axonal projections in hatchling Xenopus laevis tadpoles. 2001, Pubmed , Xenbase
Li, Spinal inhibitory neurons that modulate cutaneous sensory pathways during locomotion in a simple vertebrate. 2002, Pubmed , Xenbase
Li, A direct comparison of whole cell patch and sharp electrodes by simultaneous recording from single spinal neurons in frog tadpoles. 2004, Pubmed , Xenbase
Lin, Action potentials and underlying voltage-dependent currents studied in cultured spiral ganglion neurons of the postnatal gerbil. 1997, Pubmed
Luhmann, Cellular physiology of the neonatal rat cerebral cortex: intrinsic membrane properties, sodium and calcium currents. 2000, Pubmed
Madison, Control of the repetitive discharge of rat CA 1 pyramidal neurones in vitro. 1984, Pubmed
Markram, Interneurons of the neocortical inhibitory system. 2004, Pubmed
Marrion, Control of M-current. 1997, Pubmed
Mathieson, Morphological and electrophysiological properties of a novel in vitro preparation: the electrosensory lateral line lobe brain slice. 1988, Pubmed
McCormick, Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex. 1985, Pubmed
McKay, Kv3 K+ channels enable burst output in rat cerebellar Purkinje cells. 2004, Pubmed
McQuiston, Electrophysiology of interneurons in the glomerular layer of the rat olfactory bulb. 2001, Pubmed
Melnick, Mechanism of spike frequency adaptation in substantia gelatinosa neurones of rat. 2004, Pubmed
Melnick, Ionic basis of tonic firing in spinal substantia gelatinosa neurons of rat. 2004, Pubmed
Mo, Dendrotoxin-sensitive K(+) currents contribute to accommodation in murine spiral ganglion neurons. 2002, Pubmed
Mogul, Evidence for multiple types of Ca2+ channels in acutely isolated hippocampal CA3 neurones of the guinea-pig. 1991, Pubmed
O'Dowd, Development of voltage-dependent calcium, sodium, and potassium currents in Xenopus spinal neurons. 1988, Pubmed , Xenbase
Ohki, Divalent cation-induced phosphatidic acid membrane fusion. Effect of ion binding and membrane surface tension. 1985, Pubmed
Orlowski, Na+/H+ exchangers of mammalian cells. 1997, Pubmed
Pape, Electrophysiological and pharmacological properties of interneurons in the cat dorsal lateral geniculate nucleus. 1995, Pubmed
Paton, Characteristic firing behavior of cell types in the cardiorespiratory region of the nucleus tractus solitarii of the rat. 1993, Pubmed
Pérez, The muscarinic inhibition of the potassium M-current modulates the action-potential discharge in the vestibular primary-afferent neurons of the rat. 2009, Pubmed
Prescott, Four cell types with distinctive membrane properties and morphologies in lamina I of the spinal dorsal horn of the adult rat. 2002, Pubmed
Reyes, Membrane properties underlying the firing of neurons in the avian cochlear nucleus. 1994, Pubmed
Ribera, Differentiation of IKA in amphibian spinal neurons. 1990, Pubmed , Xenbase
Ribera, Primary sensory neurons express a Shaker-like potassium channel gene. 1993, Pubmed , Xenbase
Risner, Heterogeneous potassium conductances contribute to the diverse firing properties of postnatal mouse vestibular ganglion neurons. 2006, Pubmed
Roberts, Simple mechanisms organise orientation of escape swimming in embryos and hatchling tadpoles of Xenopus laevis. 2000, Pubmed , Xenbase
Roberts, How neurons generate behavior in a hatchling amphibian tadpole: an outline. 2010, Pubmed , Xenbase
Ruscheweyh, Distinctive membrane and discharge properties of rat spinal lamina I projection neurones in vitro. 2004, Pubmed
Russo, Dynamics of intrinsic electrophysiological properties in spinal cord neurones. 1999, Pubmed
Sabourin, Behaviorally relevant burst coding in primary sensory neurons. 2009, Pubmed
Sah, Potassium currents contributing to action potential repolarization and the afterhyperpolarization in rat vagal motoneurons. 1992, Pubmed
Sautois, Role of type-specific neuron properties in a spinal cord motor network. 2007, Pubmed
Schlösser, The intracellular tracer Neurobiotin alters electrophysiological properties of rat neostriatal neurons. 1998, Pubmed
Schwarz, Firing properties of spherical bushy cells in the anteroventral cochlear nucleus of the gerbil. 1997, Pubmed
Scroggs, Muscarine reduces calcium-dependent electrical activity in substantia nigra dopaminergic neurons. 2001, Pubmed
Segal, A transient potassium conductance regulates the excitability of cultured hippocampal and spinal neurons. 1984, Pubmed
Sivaramakrishnan, Distinct K currents result in physiologically distinct cell types in the inferior colliculus of the rat. 2001, Pubmed
Smith, Intrinsic properties shape the firing pattern of ventral horn interneurons from the spinal cord of the adult turtle. 2006, Pubmed
Soffe, The pattern of sensory discharge can determine the motor response in young Xenopus tadpoles. 1997, Pubmed , Xenbase
Spitzer, The development of the action potential mechanism of amphibian neurons isolated in culture. 1976, Pubmed , Xenbase
Sun, Developmental changes in expression of ion currents accompany maturation of locomotor pattern in frog tadpoles. 1998, Pubmed , Xenbase
Sun, Serotonergic inhibition of the T-type and high voltage-activated Ca2+ currents in the primary sensory neurons of Xenopus larvae. 1997, Pubmed , Xenbase
Svirskis, Transmitter regulation of plateau properties in turtle motoneurons. 1998, Pubmed
Szabó, Ionic currents determining the membrane characteristics of type I spiral ganglion neurons of the guinea pig. 2002, Pubmed
Tang, Amiloride selectively blocks the low threshold (T) calcium channel. 1988, Pubmed
Tell, Whole-cell analysis of ionic currents underlying the firing pattern of neurons in the gustatory zone of the nucleus tractus solitarii. 1994, Pubmed
Turrigiano, Activity-dependent changes in the intrinsic properties of cultured neurons. 1994, Pubmed
Vydyanathan, A-type voltage-gated K+ currents influence firing properties of isolectin B4-positive but not isolectin B4-negative primary sensory neurons. 2005, Pubmed
Waddell, Electrophysiological properties of subpopulations of rat dorsal root ganglion neurons in vitro. 1990, Pubmed
Wall, A role for potassium currents in the generation of the swimming motor pattern of Xenopus embryos. 1994, Pubmed , Xenbase
Wang, KCNQ2 and KCNQ3 potassium channel subunits: molecular correlates of the M-channel. 1998, Pubmed , Xenbase
Yarom, Ionic currents and firing patterns of mammalian vagal motoneurons in vitro. 1985, Pubmed
Yuste, The cortex as a central pattern generator. 2005, Pubmed
Zhou, Layer I neurons of rat neocortex. I. Action potential and repetitive firing properties. 1996, Pubmed
Zucker, Short-term synaptic plasticity. 2002, Pubmed