5-HT2 Receptors Promote Plateau Potentials in Turtle Spinal Motoneurons by Facilitating an L-Type Calcium Current

2003 ◽  
Vol 89 (2) ◽  
pp. 954-959 ◽  
Author(s):  
Jean-François Perrier ◽  
Jørn Hounsgaard
Keyword(s):  
Calcium Current ◽  
Input Resistance ◽  
Inhibitory Effect ◽  
Intracellular Recordings ◽  
Spinal Motoneurons ◽  
Intrinsic Properties ◽  
Plateau Potentials ◽  
Spike Generation ◽  
Slice Preparation ◽  
Extracellular Medium

The effects of serotonin (5-HT) on intrinsic properties of spinal motoneurons were investigated with intracellular recordings in a slice preparation from adult turtles. In 55% of the cells that were recorded, addition of 5-HT to the extracellular medium promoted plateau potentials as revealed by the response to depolarizing current pulses applied through the intracellular electrode. In the remaining 45% of cells, 5-HT had an inhibitory effect. However, when tested with an applied electric field that preferentially polarizes distal dendrites, 5-HT facilitated plateau potentials in 100% of the cells. Plateau potentials were also promoted by 5-HT focally applied on a dendrite by iontophoresis. Applied near the soma, 5-HT either promoted plateau potentials or inhibited spike generation. The latter effect was accompanied by a decrease in input resistance. Voltage-clamp recordings showed that the facilitation of plateau potentials mediated by L-type Ca2+ channels was due to activation of 5-HT2 receptors. These findings show that 5-HT regulates intrinsic properties of motoneurons in opposite ways: activation of 5-HT receptors in the soma region inhibits spike generation and plateau potentials, while activation of 5-HT2 receptors in the dendrites and the soma region promotes spiking by facilitation of plateau potentials mediated by L-type Ca2+ channels.

scholarly journals Postnatal emergence of serotonin-induced plateau potentials in commissural interneurons of the mouse spinal cord

2012 ◽  
Vol 108 (8) ◽  
pp. 2191-2202 ◽  
Author(s):  
Matthew D. Abbinanti ◽  
Guisheng Zhong ◽  
Ronald M. Harris-Warrick
Keyword(s):  
Calcium Current ◽  
Potassium Current ◽  
Neonatal Period ◽  
Calcium Currents ◽  
Intrinsic Properties ◽  
Developmental Difference ◽  
Plateau Potentials ◽  
Plateau Potential ◽  
Voltage Clamp Analysis ◽  
Serotonergic Modulation

Most studies of the mouse hindlimb locomotor network have used neonatal (P0–5) mice. In this study, we examine the postnatal development of intrinsic properties and serotonergic modulation of intersegmental commissural interneurons (CINs) from the neonatal period (P0–3) to the time the animals bear weight (P8–10) and begin to show adult walking (P14–16). CINs show an increase in excitability with age, associated with a decrease in action potential halfwidth and appearance of a fast component to the afterhyperpolarization at P14–16. Serotonin (5-HT) depolarizes and increases the excitability of most CINs at all ages. The major developmental difference is that serotonin can induce plateau potential capability in P14–16 CINs, but not at younger ages. These plateau potentials are abolished by nifedipine, suggesting that they are mediated by an L-type calcium current, ICa(L). Voltage-clamp analysis demonstrates that 5-HT increases a nifedipine-sensitive voltage-activated calcium current, ICa(V), in P14–16 CINs but does not increase ICa(V) in P8–10 CINs. These results, together with earlier work on 5-HT effects on neonatal CINs, suggest that 5-HT increases the excitability of CINs at all ages studied, but by opposite effects on calcium currents, decreasing N- and P/Q-type calcium currents and, indirectly, calcium-activated potassium current, at P0–3 but increasing ICa(L) at P14–16.

Ca2+-Activated Nonselective Cationic Current (I CAN) in Turtle Motoneurons

1999 ◽  
Vol 82 (2) ◽  
pp. 730-735 ◽  
Author(s):  
Jean-François Perrier ◽  
Jørn Hounsgaard
Keyword(s):  
Action Potentials ◽  
Input Resistance ◽  
Plateau Potentials ◽  
Slice Preparation ◽  
Metabotropic Receptors ◽  
Cationic Current ◽  
Current Pulses ◽  
Extracellular Sodium ◽  
Calcium Action Potentials ◽  
Nonselective Cationic Current

The presence of a calcium-activated nonspecific cationic (CAN) current in turtle motoneurons and its involvement in plateau potentials, bistability, and windup was investigated by intracellular recordings in a spinal cord slice preparation. In the presence of tetraethylammonium (TEA) and tetrodotoxin (TTX), calcium action potentials evoked by depolarizing current pulses were always followed by an afterdepolarization associated with a decrease in input resistance. The presence of the afterdepolarization depended on the calcium spike and not on membrane potential. Replacement of extracellular sodium by choline or N-methyl-d-glucamine (NMDG) reduced the afterdepolarization, confirming that it was mediated by a CAN current. Plateau potentials and windup were evoked in response to intracellular current pulses in the presence of agonist for different metabotropic receptors. Replacement of extracellular sodium by choline or NMDG did not abolish the generation of plateau potentials, bistability, or windup, showing that Na+ was not the principal charge carrier. It is concluded that plateau potentials, bistability and windup in turtle motoneurons do not depend on a CAN current even though its presence can be detected.

Pattern Generation for Walking and Searching Movements of a Stick Insect Leg. II. Control of Motoneuronal Activity

2001 ◽  
Vol 85 (1) ◽  
pp. 354-361 ◽  
Author(s):  
Joachim Schmidt ◽  
Hanno Fischer ◽  
Ansgar Büschges
Keyword(s):  
Sensory Feedback ◽  
Input Resistance ◽  
Stick Insect ◽  
Pattern Generation ◽  
Intracellular Recordings ◽  
Basic Pattern ◽  
Intrinsic Properties ◽  
Negative Current ◽  
Flexion And Extension ◽  
Leg Movements

In the stick insect, Cuniculina impigra, intracellular recordings from mesothoracic motoneurons that control flexion and extension of the tibia and depression and levation of the trochantero-femur were made while the leg performed walking-like movements on a treadband or stereotyped rhythmic searching movements. We were interested in how synaptic input and intrinsic properties contribute to form the activity pattern of motoneurons during rhythmic leg movements without sensory feedback from other legs. During searching and walking, motoneurons expressed a rhythmic bursting pattern that was formed by a depolarizing input followed by a hyperpolarizing input in the inter-burst interval. This basic pattern was similar in all fast, semi-fast, and slow motoneurons that were recorded. Hyperpolarizations were in synchrony with activity in the antagonistic motoneurons. De- and hyperpolarizations were associated with a decrease in input resistance. All motoneurons showed spike frequency adaptation when depolarized by current injection to a membrane potential similar to that observed during walking. In the hyperpolarizing phase of fast flexor motoneurons, the initial maximum hyperpolarization was followed by a sag in potential toward more depolarized values. Consistent with this observation, only fast flexor motoneurons developed a depolarizing sag potential when hyperpolarized by injection of constant negative current.

Compartmental Model of Vertebrate Motoneurons for Ca2+-Dependent Spiking and Plateau Potentials Under Pharmacological Treatment

1997 ◽  
Vol 78 (6) ◽  
pp. 3371-3385 ◽  
Author(s):  
Victoria Booth ◽  
John Rinzel ◽  
Ole Kiehn
Keyword(s):  
Ion Channel ◽  
Compartmental Model ◽  
Ionic Currents ◽  
Channel Blockers ◽  
Spinal Motoneurons ◽  
Plateau Potentials ◽  
Firing Patterns ◽  
Calcium Dependent ◽  
Ion Channel Blockers ◽  
Experimental Effect

Booth, Victoria, John Rinzel, and Ole Kiehn. Compartmental model of vertebrate motoneurons for Ca2+-dependent spiking and plateau potentials under pharmacological treatment. J. Neurophysiol. 78: 3371–3385, 1997. In contrast to the limited response properties observed under normal experimental conditions, spinal motoneurons generate complex firing patterns, such as Ca2+-dependent regenerative spiking and plateaus, in the presence of certain neurotransmitters and ion-channel blockers. We have developed a quantitative motoneuron model, based on turtle motoneuron data, toinvestigate the roles of specific ionic currents and the effects of their soma and dendritic distribution in generating these complex firing patterns. In addition, the model is used to explore the effects of multiple ion channel blockers and neurotransmitters that are known to modulate motoneuron firing patterns. To represent the distribution of ionic currents across the soma and dendrites, the model contains two compartments. The soma compartment, representing the soma and proximal dendrites, contains Hodgkin-Huxley-like sodium ( I Na) and delayed rectifier K+ ( I K−dr) currents, an N-like Ca2+ current ( I Ca−N), and a calcium-dependent K+ current [ I K(Ca)]. The dendritic compartment, representing the lumped distal dendrites, contains, in addition to I Ca−N and I K(Ca) as in the soma, a persistent L-like calcium current ( I Ca−L). We determined kinetic parameters for I Na, I K−dr, I Ca−N, and I K(Ca) in order to reproduce normal action-potential firing observed in turtle spinal motoneurons, including fast and slow afterhyperpolarizations (AHPs) and a linear steady-state frequency-current relation. With this parameter set as default, a sequence of pharmacological manipulations were systematically simulated. A small reduction of I K−dr [mimicking the experimental effect of tetraethylammonium (TEA) in low concentration] enhanced the slow AHP and caused calcium spiking (mediated by I Ca−N) when I Na was blocked. Firing patterns observed experimentally in high TEA [and tetrodotoxin (TTX)], namely calcium spikes riding on a calcium plateau, were reproduced only when both I K−dr and I K(Ca) were reduced. Dendritic plateau potentials, mediated by I Ca−L, were reliably unmasked when I K(Ca) was reduced, mimicking the experimental effect of the bee venom apamin. The effect of 5-HT, which experimentally induces the ability to generate calcium-dependent plateau potentials but not calcium spiking, was reproduced in the model by reducing I K(Ca) alone. The plateau threshold current level, however, was reduced substantially if a simultaneous increase in I Ca−L was simulated, suggesting that serotonin (5-HT) induces plateau potentials by regulating more than one conductance. The onset of the plateau potential showed significant delays in response to near-threshold, depolarizing current steps. In addition, the delay times were sensitive to the current step amplitude. The delay and its sensitivity were explained by examining the model's behavior near the threshold for plateau onset. This modeling study thus accurately accounts for the basic firing behavior of vertebrate motoneurons as well as a range of complex firing patterns invoked by ion-channel blockers and 5-HT. In addition, our computational results support the hypothesis that the electroresponsiveness of motoneurons depends on a nonuniform distribution of ionic conductances, and they predict modulatory effects of 5-HT and properties of plateau activation that have yet to be tested experimentally.

Effects of 5-HT on thalamocortical synaptic transmission in the developing rat

1994 ◽  
Vol 72 (5) ◽  
pp. 2438-2450 ◽  
Author(s):  
R. W. Rhoades ◽  
C. A. Bennett-Clarke ◽  
M. Y. Shi ◽  
R. D. Mooney
Keyword(s):  
Synaptic Transmission ◽  
Somatosensory Cortex ◽  
Cortical Neurons ◽  
Input Resistance ◽  
Inhibitory Effect ◽  
Primary Somatosensory Cortex ◽  
Excitatory Postsynaptic Potential ◽  
Dependent Manner ◽  
Cortical Cells ◽  
Thalamocortical Axons

1. Recent immunocytochemical and receptor binding data have demonstrated a transient somatotopic patterning of serotonin (5-HT)-immunoreactive fibers in the primary somatosensory cortex of developing rats and a transient expression of 5-HT1B receptors on thalamocortical axons from the ventral posteromedial thalamic nucleus (VPM). 2. These results suggest that 5-HT should strongly modulate thalamocortical synaptic transmission for a limited time during postnatal development. This hypothesis was tested in intracellular recording experiments carried out in thalamocortical slice preparations that included VPM, the thalamic radiations, and the primary somatosensory cortex. Effects of 5-HT and analogues were monitored on membrane potentials and input resistances of cortical neurons and on the amplitude of the synaptic potentials evoked in them by stimulation of VPM. 3. Results obtained from cortical neurons in slices taken from rats during the first 2 wk of life indicated that 5-HT strongly inhibited the VPM-evoked excitatory postsynaptic potential (EPSP) recorded from cortical neurons in a dose-dependent manner. In contrast, 5-HT had no significant effects on membrane potential, input resistance, or depolarizations induced by direct application of glutamic acid to cortical cells. 4. The effects of 5-HT were mimicked by the 5-HT1B receptor agonists 1-[3-(trifluoromethyl)phenyl]-piperazine (TFMPP) and 7-trifluoromethyl-4(4-methyl-1-piperazinyl)-pyrrolo[1,2-a]-quinoxaline maleate and antagonized by the 5-HT1B receptor antagonist (-)-pindolol. The 5-HT1A agonist [(+/-)8-hydroxydipropylaminotetralin HBr] (8-OH-DPAT) had less effect on the VPM-elicited EPSP, and the effects of 5-HT upon this response were generally not antagonized by either 1-(2-methoxyphenyl)-4-[4-(2- phthalimmido)butyl]piperazine HBr (a 5-HT1A antagonist) or ketanserine (a 5-HT2 antagonist) or spiperone (a 5-HT1A and 2 antagonist). 5. The ability of 5-HT to inhibit the VPM-evoked EPSP in cortical neurons was significantly reduced in slices from animals > 2 wk of age. The effectiveness of TFMPP in such animals was even more attenuated than that of 5-HT, and the effectiveness of 8-OH-DPAT was unchanged with age. These results are consistent with the disappearance of 5-HT1B receptors from thalamocortical axons after the second postnatal week and the maintenance of 5-HT1A receptors on some neurons. 6. All of the results obtained in this study are consistent with the conclusion that 5-HT has a profound, but developmentally transient, presynaptic inhibitory effect upon thalamocortical transmission in the rat's somatosensory cortex.

scholarly journals Differences in spike generation instead of synaptic inputs determine the feature selectivity of two retinal cell types.

2021 ◽  
Author(s):  
Sophia Wienbar ◽  
Gregory Schwartz
Keyword(s):  
Synaptic Input ◽  
Ganglion Cells ◽  
Intrinsic Property ◽  
Retinal Cell ◽  
Projection Neurons ◽  
Functional Difference ◽  
Intrinsic Properties ◽  
Spike Generation ◽  
Synaptic Inputs ◽  
Feature Selectivity

The output of spiking neurons depends both on their synaptic inputs and on their intrinsic properties. Retinal ganglion cells (RGCs), the spiking projection neurons of the retina, comprise over 40 different types in mice and other mammals, each tuned to different features of visual scenes. The circuits providing synaptic input to different RGC types to drive feature selectivity have been studied extensively, but there has been substantially less research aimed at understanding how the intrinsic properties of RGCs differ and how those differences impact feature selectivity. Here, we introduce an RGC type in the mouse, the Bursty Suppressed-by-Contrast (bSbC) RGC, whose contrast selectivity is shaped by its intrinsic properties. Surprisingly, when we compare the bSbC RGC to the OFF sustained alpha (OFFsA) RGC that receives similar synaptic input, we find that the two RGC types exhibit starkly different responses to an identical stimulus. We identified spike generation as the key intrinsic property behind this functional difference; the bSbC RGC undergoes depolarization block in conditions where the OFFsA RGC maintains a high spike rate. Pharmacological experiments, imaging, and compartment modeling demonstrate that these differences in spike generation are the result of differences in voltage-gated sodium channel conductances. Our results demonstrate that differences in intrinsic properties allow these two RGC types to detect and relay distinct features of an identical visual stimulus to the brain.

Calcium Waves and Closure of Potassium Channels in Response to GABA Stimulation in Hermissenda Type B Photoreceptors

2002 ◽  
Vol 87 (2) ◽  
pp. 776-792 ◽  
Author(s):  
K. T. Blackwell
Keyword(s):  
Calcium Current ◽  
Calcium Concentration ◽  
Calcium Release ◽  
Input Resistance ◽  
Receptor Activation ◽  
Memory Storage ◽  
Type B ◽  
Kinase C ◽  
Hyperpolarization Activated Current ◽  
Receptor Channel

Classical conditioning of Hermissenda crassicornisrequires the paired presentation of a conditioned stimulus (light) and an unconditioned stimulus (turbulence). Light stimulation of photoreceptors leads to production of diacylglycerol, an activator of protein kinase C, and inositol triphosphate (IP3), which releases calcium from intracellular stores. Turbulence causes hair cells to release GABA onto the terminal branches of the type B photoreceptor. One prior study has shown that GABA stimulation produces a wave of calcium that propagates from the terminal branches to the soma and raises the possibility that two sources of calcium are required for memory storage. GABA stimulation also causes an inhibitory postsynaptic potential (IPSP) followed by a late depolarization and increase in input resistance, whose cause has not been identified. A model was developed of the effect of GABA stimulation on the Hermissenda type B photoreceptor to evaluate the currents underlying the late depolarization and to evaluate whether a calcium wave could propagate from the terminal branches to the soma. The model included GABAA, GABAB, and calcium-sensitive potassium leak channels; calcium dynamics including release of calcium from intracellular stores; and the biochemical reactions leading from GABAB receptor activation to IP3 production. Simulations show that it is possible for a wave of calcium to propagate from the terminal branches to the soma. The wave is initiated by IP3-induced calcium release but propagation requires release through the ryanodine receptor channel where IP3 concentration is small. Wave speed is proportional to peak calcium concentration at the crest of the wave, with a minimum speed of 9 μm/s in the absence of IP3. Propagation ceases when peak concentration drops below 1.2 μM; this occurs if the rate of calcium pumping into the endoplasmic reticulum is too large. Simulations also show that both a late depolarization and an increase in input resistance occur after GABA stimulation. The duration of the late depolarization corresponds to the duration of potassium leak channel closure. Neither the late depolarization nor the increase in input resistance are observed when a transient calcium current and a hyperpolarization-activated current are added to the model as replacement for closure of potassium leak channels. Thus the late depolarization and input resistance elevation can be explained by a closure of calcium-sensitive leak potassium currents but cannot be explained by a transient calcium current and a hyperpolarization-activated current.

Cholinergic and electrical motoneuron-to-motoneuron synapses contribute to on-cycle excitation during swimming in Xenopus embryos

1995 ◽  
Vol 73 (3) ◽  
pp. 1005-1012 ◽  
Author(s):  
R. Perrins ◽  
A. Roberts
Keyword(s):  
Nicotinic Receptors ◽  
Local Application ◽  
Intracellular Recordings ◽  
Spinal Motoneurons ◽  
Electrical Synapses ◽  
Ampa Antagonist ◽  
Xenopus Embryos ◽  
Fast Excitation ◽  
Spiking Activity

1. We have previously shown that Xenopus spinal motoneurons make both chemical and electrical synapses with neighboring motoneurons. Because motoneurons are active during swimming, these synapses would be expected to contribute excitation to their neighbors. The significance of central motoneuron to motoneuron synapses was therefore investigated by analyzing the composition of the fast on-cycle excitation underlying spiking activity during fictive swimming in spinal motoneurons. To accomplish this we developed a method for very local application of drugs around a caudal recorded neuron while still being able to evoke and record essentially unaltered fictive swimming rostrally. 2. Intracellular recordings were made from spinal motoneurons during fictive swimming. Bicuculline (40 microM) and strychnine (2 microM) were used continuously to block inhibitory potentials locally around the motoneurons. The amplitude and duration of the fast excitation underlying spiking activity was measured before and during local applications of excitatory antagonists. 3. The nicotinic antagonists d-tubocurarine (10 microM) and dihydro-beta-erythroidine (10 microM) reduced the amplitude of this excitation by approximately 20%. Nicotinic antagonists also reduced the duration of this fast on-cycle excitation. The kainate/alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) antagonist 6-cyano-7-nitroquinoxaline-2,3-dione (CNQX, 10 microM) reduced the amplitude (by approximately 30%) but not the duration of the on-cycle excitation. In the presence of 100 microM Cd2+, which blocks all chemically mediated transmission, a considerable amount (50%) of on-cycle excitation remained. 4. These results suggest that 20% of the on-cycle excitation comes from activation of nicotinic receptors by naturally released acetylcholine (ACh), presumably from other motoneurons.(ABSTRACT TRUNCATED AT 250 WORDS)

scholarly journals Transmitter Regulation of Plateau Properties in Turtle Motoneurons

1998 ◽  
Vol 79 (1) ◽  
pp. 45-50 ◽  
Author(s):  
Gytis Svirskis ◽  
Jørn Hounsgaard
Keyword(s):  
Membrane Potential ◽  
Metabotropic Glutamate Receptors ◽  
Input Resistance ◽  
Pattern Generation ◽  
Synaptic Activity ◽  
Membrane Properties ◽  
Resting Membrane Potential ◽  
Type I ◽  
Plateau Potentials ◽  
Inward Current

Svirskis, Gytis and Jørn Hounsgaard. Transmitter regulation of plateau properties in turtle motoneurons. J. Neurophysiol. 79: 45–50, 1998. In motoneurons, generation of plateau potentials is promoted by modulators that block potassium channels. In voltage-clamp experiments with triangular voltage ramp commands, we show that cis-(±)-1-aminocyclopentane-1,3-dicarboxylic acid ( cis-ACPD) and muscarine promote the generation of plateau potentials by increasing the dihydropyridine sensitive inward current, by increasing the input resistance, and by depolarizing the resting membrane potential. Type I metabotropic glutamate receptors (mGluR I) mediate the effects of cis-ACPD. Baclofen suppresses generation of plateau potentials by decreasing the dihydropyridine sensitive inward current, by decreasing the input resistance, and by hyperpolarizing the resting membrane potential. These results suggest that membrane properties of motoneurons are continuously modulated by synaptic activity in ways that may have profound effects on synaptic integration and pattern generation.

Plateau Potentials in Developing Antennal-Lobe Neurons of the Moth, Manduca sexta

2005 ◽  
Vol 93 (4) ◽  
pp. 1949-1958 ◽  
Author(s):  
A. R. Mercer ◽  
P. Kloppenburg ◽  
J. G. Hildebrand
Keyword(s):  
Electrical Activity ◽  
Manduca Sexta ◽  
Antennal Lobe ◽  
Membrane Properties ◽  
Plateau Potentials ◽  
Extracellular Medium ◽  
Threshold Phenomena ◽  
Plateau State ◽  
Developing Neurons

Using whole cell recordings from antennal-lobe (AL) neurons in vitro and in situ, in semi-intact brain preparations, we examined membrane properties that contribute to electrical activity exhibited by developing neurons in primary olfactory centers of the brain of the sphinx moth, Manduca sexta. This activity is characterized by prolonged periods of membrane depolarization that resemble plateau potentials. The presence of plateau potential–generating mechanisms was confirmed using a series of tests established earlier. Brief depolarizing current pulses could be used to trigger a plateau state. Once triggered, plateau potentials could be terminated by brief pulses of hyperpolarizing current. Both triggering and terminating of firing states were threshold phenomena, and both conditions resulted in all-or-none responses. Rebound excitation from prolonged hyperpolarizing pulses could also be used to generate plateau potentials in some cells. These neurons were found to express a hyperpolarization-activated inward current. Neither the generation nor the maintenance of plateau potentials was affected by removal of Na+ ions from the extracellular medium or by blockade of Na+ currents with TTX. However, blocking of Ca2+ currents with Cd2+ (5 × 10−4 M) inhibited the generation of plateau potentials, indicating that, in Manduca AL neurons, plateau potentials depend on Ca2+. Examining Ca2+ currents in isolation revealed that activation of these currents occurs in the absence of experimentally applied depolarizing stimuli. Our results suggest that this activity underlies the generation of plateau potentials and characteristic bursts of electrical activity in developing AL neurons of M. sexta.

Sign in / Sign up

Export Citation Format

Share Document