Activities of spinal neurons during brain stem-dependent fictive swimming in lamprey

1995 ◽  
Vol 73 (1) ◽  
pp. 80-87 ◽  
Author(s):  
J. T. Buchanan ◽  
S. Kasicki
Keyword(s):  
Spinal Cord ◽  
Membrane Potential ◽  
Brain Stem ◽  
Cell Types ◽  
Inhibitory Neurons ◽  
Spinal Neurons ◽  
Potential Oscillations ◽  
Electrical Shocks ◽  
Dorsal Cells ◽  
Membrane Potential Oscillations

1. We made intracellular microelectrode recordings of membrane potential from spinal neurons during fictive swimming elicited by brief electrical shocks to the spinal cord in a brain stem-spinal cord preparation of the adult silver lamprey (Ichthyomyzon unicuspis). 2. We characterized membrane potential activities recorded during brain stem-dependent fictive swimming in five spinal cell types: myotomal motoneurons, lateral interneurons (inhibitory neurons with ipsilateral descending axons), CC interneurons (neurons with contralateral and caudal projecting axons), edge cells (intraspinal stretch receptors), and dorsal cells (primary mechanosensory neurons with cell bodies in the spinal cord). The membrane potential activities were compared with data from previous reports recorded during fictive swimming in the isolated spinal cord with fictive swimming induced by superfusion with D-glutamate. 3. Compared with the same cell types recorded during D-glutamate-induced fictive swimming in brain stem-dependent fictive swimming, the motoneurons and CC interneurons had significantly larger trough-to-peak amplitudes of membrane potential oscillations, whereas lateral interneurons were not significantly different in amplitude. The timings of the membrane potential oscillations and of cell spiking were not significantly different in the two preparations, with the exception that motoneurons in brain stem-dependent fictive swimming were significantly earlier by approximately 10% of a cycle. Edge cells had only weak or no oscillatory activities, and dorsal cells had no detectable input during brain stem-dependent fictive swimming. These findings are similar to those in D-glutamate-induced fictive swimming.(ABSTRACT TRUNCATED AT 250 WORDS)

scholarly journals Intracellular QX-314 Causes Depression of Membrane Potential Oscillations in Lamprey Spinal Neurons During Fictive Locomotion

2002 ◽  
Vol 87 (6) ◽  
pp. 2676-2683 ◽  
Author(s):  
Guo-Yuan Hu ◽  
Zoltán Biró ◽  
Russell H. Hill ◽  
Sten Grillner
Keyword(s):  
Spinal Cord ◽  
Membrane Potential ◽  
Dendritic Tree ◽  
Cell Voltage ◽  
Fictive Locomotion ◽  
Spinal Neurons ◽  
Potential Oscillations ◽  
Short Pulses ◽  
Voltage Dependent ◽  
Membrane Potential Oscillations

Spinal neurons undergo large cyclic membrane potential oscillations during fictive locomotion in lamprey. It was investigated whether these oscillations were due only to synaptically driven excitatory and inhibitory potentials or if voltage-dependent inward conductances also contribute to the depolarizing phase by using N-(2,6-dimethylphenyl carbamoylmethyl)triethylammonium bromide (QX-314) administered intracellularly during fictive locomotion. QX-314 intracellularly blocks inactivating and persistent Na+ channels, and in some neurons, effects on certain other types of channels have been reported. To detail the effects of QX-314 on Na+ and Ca2+ channels, we used dissociated lamprey neurons recorded under whole cell voltage clamp. At low intracellular concentrations of QX-314 (0.2 mM), inactivating Na+ channels were blocked and no effects were exerted on Ca2+ channels (also at 0.5 mM). At 10 mM QX-314, there was, however a marked reduction of I Ca. In the isolated spinal cord of the lamprey, fictive locomotion was induced by superfusing the spinal cord with Ringer's solution containing N-methyl-d-aspartate (NMDA), while recording the locomotor activity from the ventral roots. Simultaneously, identified spinal neurons were recorded intracellularly, while infusing QX-314 from the microelectrode. Patch electrodes cannot be used in the intact spinal cord, and therefore “sharp” electrodes were used. The amplitude of the oscillations was consistently reduced by 20–25% in motoneurons ( P < 0.05) and unidentified spinal neurons ( P < 0.005). The onset of the effect started a few minutes after impalement and reached a stable level within 30 min. These effects thus show that QX-314 causes a reduction in the amplitude of membrane potential oscillations during fictive locomotion. We also investigated whether QX-314 could affect glutamate currents by applying short pulses of glutamate from an extracellular pipette. No changes were observed. We also found no evidence for a persistent Na+ current in dissociated neurons, but these cells have a much-reduced dendritic tree. The results indicate that there is an inward conductance, which is sensitive to QX-314, during membrane potential oscillations that “boosts” the synaptic drive during fictive locomotion. Taken together, the results suggest that inactivating Na+ channels contribute to this inward conductance although persistent Na+channels, if present on dendrites, could possibly also contribute to shaping the membrane potential oscillations.

Endogenous release of 5-HT modulates the plateau phase of NMDA-induced membrane potential oscillations in lamprey spinal neurons

2014 ◽  
Vol 112 (1) ◽  
pp. 30-38 ◽  
Author(s):  
Di Wang ◽  
Sten Grillner ◽  
Peter Wallén
Keyword(s):  
Spinal Cord ◽  
Membrane Potential ◽  
Calcium Channels ◽  
Nmda Receptors ◽  
Plateau Phase ◽  
Spinal Neurons ◽  
Potential Oscillations ◽  
Voltage Dependent ◽  
Endogenous Release ◽  
Membrane Potential Oscillations

The lamprey central nervous system has been used extensively as a model system for investigating the networks underlying vertebrate motor behavior. The locomotor networks can be activated by application of glutamate agonists, such as N-methyl-D-aspartic acid (NMDA), to the isolated spinal cord preparation. Many spinal neurons are capable of generating pacemaker-like membrane potential oscillations upon activation of NMDA receptors. These oscillations rely on the voltage-dependent properties of NMDA receptors in interaction with voltage-dependent potassium and calcium-dependent potassium (KCa) channels, as well as low voltage-activated calcium channels. Upon membrane depolarization, influx of calcium will activate KCa channels, which in turn, will contribute to repolarization and termination of the depolarized phase. The appearance of the NMDA-induced oscillations varies markedly between spinal cord preparations; they may either have a pronounced, depolarized plateau phase or be characterized by a short-lasting depolarization lasting approximately 200–300 ms without a plateau. Both types of oscillations increase in frequency with increased concentrations of NMDA. Here, we characterize these two types of membrane potential oscillations and show that they depend on the level of endogenous release of 5-HT in the spinal cord preparations. In the lamprey, 5-HT acts to block voltage-dependent calcium channels and will thereby modulate the activity of KCa channels. When 5-HT antagonists were administered, the plateau-like oscillations were converted to the second type of oscillations lacking a plateau phase. Conversely, plateau-like oscillations can be induced or prolonged by 5-HT agonists. These properties are most likely of significance for the modulatory action of 5-HT on the spinal networks for locomotion.

Identification of excitatory interneurons contributing to generation of locomotion in lamprey: structure, pharmacology, and function

1989 ◽  
Vol 62 (1) ◽  
pp. 59-69 ◽  
Author(s):  
J. T. Buchanan ◽  
S. Grillner ◽  
S. Cullheim ◽  
M. Risling
Keyword(s):  
Spinal Cord ◽  
Membrane Potential ◽  
Excitatory Amino Acid ◽  
Postsynaptic Membrane ◽  
Fictive Locomotion ◽  
Potential Oscillations ◽  
And Function ◽  
Spherical Vesicles ◽  
Membrane Potential Oscillations

1. In the in vitro preparation of the lamprey spinal cord, paired intracellular recordings of membrane potential were used to identify interneurons producing excitatory postsynaptic potentials (EPSPs) on myotomal motoneurons. 2. Seventy-nine interneurons (8.4% of all neuron-motoneuron pairs tested) elicited unitary EPSPs that followed one-for-one at short, constant latencies and were therefore considered monosynaptic according to conventional criteria. Evidence was obtained for selectivity and divergence of excitatory interneuron (EIN) outputs and for convergence of EIN input to motoneurons. 3. The neurotransmitter released by EINs may be an excitatory amino acid such as glutamate, because the EPSPs were depressed by antagonists of excitatory amino acids. 4. Intracellular dye injection revealed that EINs have small cell bodies (average 11 x 27 microns), transversely oriented dendrites, and thin (less than 3 microns) slowly conducting axons (0.7 m/s) that project caudally and ipsilaterally. One EIN exhibited a system of thin multi-branching axon collaterals with periodic swellings. Ultrastructurally, these swellings contained clear spherical vesicles, and they apposed postsynaptic membrane specializations. 5. During fictive locomotion, the membrane-potential oscillations of EINs were greater in amplitude than, but similar in shape and timing to, those of their postsynaptic motoneurons. EINs fired action potentials during fictive locomotion and contributed to the depolarization of motoneurons. 6. These interneurons are proposed to be a source of excitation to motoneurons and interneurons in the lamprey spinal cord, participating in motor activity including locomotion.

Central modulation of stretch receptor neurons during fictive locomotion in lamprey

1996 ◽  
Vol 76 (2) ◽  
pp. 1224-1235 ◽  
Author(s):  
L. Vinay ◽  
J. Y. Barthe ◽  
S. Grillner
Keyword(s):  
Spinal Cord ◽  
Membrane Potential ◽  
Receptor Antagonist ◽  
Chloride Ions ◽  
Stretch Receptor ◽  
Fictive Locomotion ◽  
Gamma Aminobutyric Acid ◽  
Potential Oscillations ◽  
Receptor Neurons ◽  
Membrane Potential Oscillations

1. In lamprey, stretch receptor neurons (SRNs), also referred to as edge cells, are located along the lateral margin of the spinal cord. They sense the lateral movements occurring in each swim cycle during locomotion. The isolated lamprey spinal cord in vitro was used to investigate the activity of SRNs during fictive locomotion induced by bath-applied N-methyl-D-aspartate (NMDA). Intracellular recordings with potassium acetate filled electrodes showed that 63% of SRNs had a clear locomotor-related modulation of their membrane potential. 2. Of the modulated SRNs, two-thirds had periods of alternating excitation and inhibition occurring during the ipsilateral and the contralateral ventral root bursts, respectively. The phasic hyperpolarization could be reversed into a depolarizing phase after the injection of chloride ions into the cells; this revealed a chloride-dependent synaptic drive. The remaining modulated SRNs were inhibited phasically during ipsilateral motor activity. 3. Experiments with barriers partitioning the recording chamber with the spinal cord into three pools, allowed an inactivation of the locomotor networks within one pool by washing out NMDA from the pool in which the SRN was recorded. This resulted in a marked reduction, but not an abolishment, of the amplitude of the membrane potential oscillations. Both the excitatory and the inhibitory phases were reduced, resulting from removal of input from inhibitory and excitatory interneurons projecting from the adjacent pools. If the glycine receptor antagonist strychnine (1 microM) was applied in one pool, the phasic hyperpolarizing phase disappeared without affecting the excitatory phase. 4. Bath application of the gamma-aminobutyric acid (GABA)A receptor antagonist, bicuculline (50-100 microM) blocked the spontaneous large unitary inhibitory postsynaptic potentials, which occurred without a clear phasic pattern. Bicuculline had no significant effect on the peak to peak amplitude of the locomotor-related membrane potential oscillations. The inhibition in SRNs therefore has a dual origin: glycinergic interneurons provide phasic inhibition, while the GABA system can exert a tonic inhibition via GABAA receptors. 5. These data show that, in addition to the stretch-evoked excitation, which SRNs receive during each locomotor cycle, most of them also receive excitation from the central pattern generator network during the ipsilateral contraction, which may ensure a maintained high level of sensitivity to stretch during the shortening phase of the locomotor cycle. This arrangement is analogous to the efferent control of muscle spindles exerted by gamma-motoneurons in mammals, which as a rule are coactivated with alpha-motoneurons to the same muscle (alpha-gamma linkage).

scholarly journals Spinobulbar Neurons in Lamprey: Cellular Properties and Synaptic Interactions

2006 ◽  
Vol 96 (4) ◽  
pp. 2042-2055 ◽  
Author(s):  
James F. Einum ◽  
James T. Buchanan
Keyword(s):  
Spinal Cord ◽  
Brain Stem ◽  
Feedback Inhibition ◽  
Inhibitory Synapses ◽  
Medium Size ◽  
Spinal Neurons ◽  
Lower Vertebrate ◽  
Dorsal Cells ◽  
The Brain

An in vitro preparation of the nervous system of the lamprey, a lower vertebrate, was used to characterize the properties of spinal neurons with axons projecting to the brain stem [i.e., spinobulbar (SB) neurons)]. To identify SB neurons, extracellular electrodes on each side of the spinal cord near the obex recorded the axonal spikes of neurons impaled with sharp intracellular microelectrodes in the rostral spinal cord. The ascending spinal neurons ( n = 144) included those with ipsilateral (iSB) (63/144), contralateral (cSB) (77/144), or bilateral (bSB) (4/144) axonal projections to the brain stem. Intracellular injection of biocytin revealed that the SB neurons had small- to medium-size somata and most had dendrites confined to the ipsilateral side of the cord, although about half of the cSB neurons also had contralateral dendrites. Most SB neurons had multiple axonal branches including descending axons. Electrophysiologically, the SB neurons were similar to other lamprey spinal neurons, firing spikes throughout long depolarizing pulses with some spike-frequency adaptation. Paired intracellular recordings between SB and reticulospinal (RS) neurons revealed that SB neurons made either excitatory or inhibitory synapses on RS neurons and the SB neurons received excitatory input from RS neurons. Mutual excitation and feedback inhibition between pairs of RS and SB neurons were observed. The SB neurons also received excitatory inputs from primary mechanosensory neurons (dorsal cells), and these same SB neurons were rhythmically active during fictive swimming, indicating that SB neurons convey both sensory and locomotor network information to the brain stem.

Dopaminergic Modulation of Spinal Neurons and Synaptic Potentials in the Lamprey Spinal Cord

1997 ◽  
Vol 77 (1) ◽  
pp. 289-298 ◽  
Author(s):  
Christopher P. Kemnitz
Keyword(s):  
Spinal Cord ◽  
Membrane Potential ◽  
Cycle Period ◽  
Spinal Neurons ◽  
Postsynaptic Potentials ◽  
Giant Interneurons ◽  
Bath Application ◽  
Dopaminergic Modulation ◽  
Dorsal Cells ◽  
Stimulation Of

Kemnitz, Christopher P. Dopamineric modulation of spinal neurons and synaptic potentials in the lamprey spinal cord. J. Neurophysiol. 77: 289–298, 1997. It has been shown previously that dopamine-immunoreactive cells and processes are present in the lamprey spinal cord and that dopamine modulates the cycle period of fictive swimming. The present study was undertaken to further characterize the effects of dopamine on the cellular properties of lamprey spinal neurons and on inhibitory and excitatory postsynaptic potentials to determine how dopaminergic modulation may affect the central pattern generator for locomotion. Dopamine reduced the late afterhyperpolarization (late AHP) following the action potential of motoneurons, and in three types of sensory neurons: dorsal cells, edge cells, and giant interneurons. The late AHP was not reduced in lateral interneurons or CC interneurons, both of which are part of the central motor pattern generating neural network. The reduction of the late AHP in motoneurons, edge cells, and giant interneurons resulted in an increase in firing frequency in response to depolarizing current injection. In the six cell classes examined, no changes were observed in the resting membrane potential, input resistance, rheobase, spike amplitude, or spike duration after application of dopamine. The durations of action potentials broadened by application of tetraethylammonium in motoneurons and of calcium action potentials in dorsal cells and giant interneurons were decreased after bath application of 10 μM dopamine. The durations of tetrodotoxin-resistant, N-methyl-d-aspartate-induced membrane potential oscillations in lamprey spinal motoneurons were increased after bath application of 1–100 μM dopamine, due perhaps to reduced calcium entry and thus reduced Ca2+-dependent K+ current responsible for the repolarization of the membrane potential during each oscillation. Polysynaptic inhibitory postsynaptic potentials (IPSPs) elicited in lamprey spinal motoneurons by stimulation of the contralateral half of the spinal cord were reduced by bath application of 10 μM dopamine. Polysynaptic excitatory postsynaptic potentials were not reduced by dopamine. Monosynaptic IPSPs in motoneurons elicited by stimulation of single contralateral inhibitory CC interneurons and single ipsilateral axons were reduced by bath application of dopamine (10 μM). Monosynaptic IPSPs in CC interneurons elicited by stimulation of ipsilateral lateral interneurons, however, showed no change after application of dopamine. The lack of dopaminergic effect on the late AHP of the locomotor network neurons, lateral interneurons and CC interneurons, and the selective reduction of IPSPs from CC interneurons suggest that synaptic modulation may play an important role in dopaminergic modulation of cycle period during fictive swimming in the lamprey.

Synaptically Evoked Membrane Potential Oscillations Induced by Substance P in Lamprey Motor Neurons

2002 ◽  
Vol 87 (1) ◽  
pp. 113-121 ◽  
Author(s):  
Erik Svensson ◽  
Sten Grillner ◽  
David Parker
Keyword(s):  
Spinal Cord ◽  
Membrane Potential ◽  
Protein Kinase ◽  
Substance P ◽  
Receptor Antagonist ◽  
Motor Neurons ◽  
Network Activity ◽  
Membrane Properties ◽  
Potential Oscillations ◽  
Membrane Potential Oscillations

Short-lasting application (10 min) of tachykinin neuropeptides evokes long-lasting (>24 h) modulation of N-methyl-d-aspartate (NMDA)-evoked locomotor network activity in the lamprey spinal cord. In this study, the net effects of the tachykinin substance P on the isolated spinal cord have been examined by recording from motor neurons in the absence of NMDA and ongoing network activity. Brief bath application of substance P (30 s to 2 min) induced irregular membrane potential oscillations in motor neurons. These oscillations consisted of depolarizing and hyperpolarizing phases and were associated with phasic ventral-root activity. The oscillations were blocked by the tachykinin antagonist spantide II. They were also blocked by tetrodotoxin (TTX), suggesting that they were not dependent on intrinsic membrane properties of the motor neurons but were synaptically mediated. Substance P could also have a direct effect, however, because a membrane potential depolarization persisted in the presence of TTX. Protein kinase agonists and antagonists were used to investigate the intracellular pathways through which substance P acted. The oscillations were blocked by the selective protein kinase C (PKC) antagonist chelerythrine. However, the TTX-resistant membrane potential depolarization was not significantly affected by blocking PKC. The protein kinase A and G antagonist H8 did not affect either the oscillations or the direct TTX-resistant membrane potential depolarization. The glutamate receptor antagonist kynurenic acid abolished the substance-P-evoked oscillations, suggesting that they were dependent on glutamate release. The oscillations were abolished or reduced by the AMPA/kainate receptor antagonist 6-cyano-7-nitroquinoxalene-2,3-dione but were only reduced by the NMDA receptor antagonist d-AP5. The oscillations were thus mediated by glutamatergic inputs with a greater dependence on non-NMDA receptors. Blocking glycinergic inputs with strychnine resulted in large depolarizing plateaus and bursts of spikes. The glutamatergic and glycinergic inputs underlying the oscillations are apparently evoked through direct and indirect excitatory effects on inhibitory and excitatory premotor interneurons. Substance P thus has a distributed excitatory effect in the spinal cord. While it can activate premotor networks, this activation alone is not able to evoke a coordinated behaviorally relevant motor output.

scholarly journals Membrane Potential Oscillations in Reticulospinal and Spinobulbar Neurons During Locomotor Activity

2005 ◽  
Vol 94 (1) ◽  
pp. 273-281 ◽  
Author(s):  
James F. Einum ◽  
James T. Buchanan
Keyword(s):  
Spinal Cord ◽  
Membrane Potential ◽  
Locomotor Activity ◽  
Brain Stem ◽  
Excitatory Amino Acid ◽  
Rhythmic Activity ◽  
Ventral Root ◽  
Potential Oscillations ◽  
Bath Application ◽  
The Brain

Feedback from the spinal locomotor networks provides rhythmic modulation of the membrane potential of reticulospinal (RS) neurons during locomotor activity. To further understand the origins of this rhythmic activity, the timings of the oscillations in spinobulbar (SB) neurons of the spinal cord and in RS neurons of the posterior and middle rhombencephalic reticular nuclei were measured using intracellular microelectrode recordings in the isolated brain stem-spinal cord preparation of the lamprey. A diffusion barrier constructed just caudal to the obex allowed induction of locomotor activity in the spinal cord by bath application of an excitatory amino acid to the spinal bath. All of the ipsilaterally projecting SB neurons recorded had oscillatory membrane potentials with peak depolarizations in phase with the ipsilateral ventral root bursts, whereas the contralaterally projecting SB neurons were about evenly divided between those in phase with the ipsilateral ventral root bursts and those in phase with the contralateral bursts. In the brain stem under these conditions, 75% of RS neurons had peak depolarizations in phase with the ipsilateral ventral root bursts while the remainder had peak depolarizations during the contralateral bursts. Addition of a high-Ca2+, Mg2+ solution to the brain stem bath to reduce polysynaptic activity had little or no effect on oscillation timing in RS neurons, suggesting that direct inputs from SB neurons make a major contribution to RS neuron oscillations under these conditions. Under normal conditions when the brain is participating in the generation of locomotor activity, these spinal inputs will be integrated with other inputs to RS neurons.

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