Mammalian BarH1Confers Commissural Neuron Identity on Dorsal Cells in the Spinal Cord

Platelet-derived growth factor alpha-receptors (PDGFR alpha) are expressed by a subset of neuroepithelial cells in the ventral half of the embryonic day 14 (E14) rat spinal cord. The progeny of these cells subsequently proliferate and migrate into the dorsal parts of the cord after E16. Here, we show that E14 ventral cells are able to generate oligodendrocytes in culture but that dorsal cells acquire this ability only after E16, coinciding with the appearance of PDGFR alpha-immunoreactive cells in the starting population. PDGFR alpha-positive cells in optic nerve and spinal cord cultures co-labelled with antibody markers of oligodendrocyte progenitors. When PDGFR alpha-positive cells were purified from embryonic rat spinal cords by immunoselection and cultured in defined medium, they all differentiated into oligodendrocytes. Very few oligodendrocytes developed in cultures of embryonic spinal cord cells that had been depleted of PDGFR alpha-expressing cells by antibody-mediated complement lysis. These data demonstrate that all PDGFR alpha-positive cells in the embryonic rat spinal cord are oligodendrocyte progenitors and that most or all early-developing oligodendrocytes are derived from these ventrally-derived precursors.

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Tachykinin-mediated modulation of sensory neurons, interneurons, and synaptic transmission in the lamprey spinal cord

Journal of Neurophysiology ◽

10.1152/jn.1996.76.6.4031 ◽

1996 ◽

Vol 76 (6) ◽

pp. 4031-4039 ◽

Cited By ~ 28

Author(s):

D. Parker ◽

S. Grillner

Keyword(s):

Spinal Cord ◽

Substance P ◽

Synaptic Transmission ◽

Dorsal Root ◽

Input Resistance ◽

Dorsal Column ◽

Giant Interneurons ◽

Potassium Conductances ◽

Dorsal Cells ◽

Measurable Change

1. Tachykinin-like immunoreactivity is found in the dorsal roots, dorsal horn, and dorsal column of the lamprey. The effect of tachykinins on sensory processing was examined by recording intracellularly from primary sensory dorsal cells and second-order spinobulbar giant interneurons. Modulation of synaptic transmission was examined by making paired recordings from dorsal cells and giant interneurons, or by eliciting compound depolarizations in the giant interneurons by stimulating the dorsal root or dorsal column. 2. Bath application of tachykinins depolarized the dorsal cells. This effect was mimicked by stimulation of the dorsal root, suggesting that dorsal root afferents may be a source of endogenous tachykinin input to the spinal cord. The depolarization was reduced by removal of sodium or calcium from the Ringer, or when potassium conductances were blocked, and was not associated with a measurable change in input resistance. Dorsal root stimulation also caused a depolarization in the dorsal cells, and this effect and that of bath-applied substance P, was blocked by the tachykinin antagonist spantide. 3. The tachykinin substance P could reduce inward and outward rectification in the dorsal cells, the effect on outward rectification only being seen when potassium conductances were blocked by tetraethylammonium (TEA). 4. Substance P increased the excitability of the dorsal cells and giant interneurons, shown by the increased spiking in response to depolarizing current pulses. The increased excitability was blocked by the tachykinin antagonist spantide. 5. Substance P modulated the dorsal cell action potential, by increasing the spike duration and reducing the amplitude of the afterhyperpolarization. The spike amplitude was not consistently affected. 6. Stimulation of the dorsal column resulted in either depolarizing or hyperpolarizing potentials in the giant interneurons. The amplitude of the depolarization was increased by substance P, whereas the amplitude of the hyperpolarization was reduced. These effects occurred independently of a measurable change in postsynaptic input resistance, suggesting that the modulation occurred presynaptically. Paired recordings from dorsal cells and giant interneurons failed to reveal an effect of substance P on dorsal cell-evoked excitatory postsynaptic potentials (EPSPs), suggesting that the potentiation of the dorsal column-evoked depolarization was due to an effect on other axons in the dorsal column. Dorsal root-evoked potentials could also be increased in the presence of substance P, although this effect was less consistent than the effect on dorsal column stimulation. 7. These results suggest that tachykinins modulate sensory input to the lamprey spinal cord by increasing the excitability of primary afferents and second-order giant interneurons, and also by modulating synaptic transmission. Tachykinins may result in potentiation of local spinal reflexes and also modulation of descending reticulospinal inputs to the spinal locomotor network as a result of potentiation of spinobulbar inputs.

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Spinobulbar Neurons in Lamprey: Cellular Properties and Synaptic Interactions

Journal of Neurophysiology ◽

10.1152/jn.01331.2005 ◽

2006 ◽

Vol 96 (4) ◽

pp. 2042-2055 ◽

Cited By ~ 12

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.

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Neurophysiology of Lampreys

Canadian Journal of Fisheries and Aquatic Sciences ◽

10.1139/f80-218 ◽

1980 ◽

Vol 37 (11) ◽

pp. 1723-1738 ◽

Cited By ~ 3

Author(s):

Carl M. Rovainen

Keyword(s):

Spinal Cord ◽

Nervous System ◽

Neural Control ◽

Sensory Stimulation ◽

Future Research ◽

Spinal Motoneurons ◽

Dorsal Cells ◽

Considerable Detail ◽

Brain And Spinal Cord ◽

The Brain

The nervous system of the lamprey has been appreciated by comparative neuroanatomists for nearly a century as a "prototype" for the brain and spinal cord of higher vertebrates. Only recently have neurophysiologists discovered the practical advantages of the lamprey brain and spinal cord, such as relative simplicity, survival in isolation, and the occurrence of large, visible, nerve cells and axons. During the past 15 yr rapid progress has been made in understanding the basic physiological, pharmacological, and ultrastructural properties of lamprey neurons and the organization of sensory and motor systems. Several types of neurons are now known in considerable detail and include the prominent Müller and Mauthner cells, respiratory and spinal motoneurons, giant interneurons, and sensory dorsal cells. Some of the important subjects for future research include the behavioral responses of adult lampreys to different modes of sensory stimulation, the neural control of feeding, and the changes which occur in the nervous system during metamorphosis.Key words: brain, lamprey, neurophysiology, respiration, spinal cord, swimming

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

Journal of Neurophysiology ◽

10.1152/jn.1997.77.1.289 ◽

1997 ◽

Vol 77 (1) ◽

pp. 289-298 ◽

Cited By ~ 26

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.

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Identification of interneurons with contralateral, caudal axons in the lamprey spinal cord: synaptic interactions and morphology

Journal of Neurophysiology ◽

10.1152/jn.1982.47.5.961 ◽

1982 ◽

Vol 47 (5) ◽

pp. 961-975 ◽

Cited By ~ 167

Author(s):

J. T. Buchanan

Keyword(s):

Spinal Cord ◽

Motor Coordination ◽

Contralateral Side ◽

Müller Cell ◽

The Body ◽

Intracellular Stimulation ◽

Muller Cell ◽

Axon Branch ◽

Dorsal Cells ◽

Stimulation Of

1. As part of a continuing investigation of the organization of the spinal cord of the lamprey, propriospinal interneurons with axons projecting contralaterally and caudally (CC interneurons) were surveyed with intracellular recordings. 2. CC interneurons were identified by recording their axon spikes extracellularly in the spinal cord during intracellular stimulation of the cell body. The axon projections of Cc interneurons were confirmed after intracellular injection and development of horseradish peroxidase. 3. Intracellular stimulation of CC interneurons produced synaptic potentials in myotomal motoneurons, lateral interneurons and other CC interneurons that lay caudally on the opposite side of the spinal cord. Most CC interneurons were inhibitory, but some were excitatory. 4. CC interneurons were divided into three classes on the basis of reticulospinal Muller cell inputs. CC1 interneurons were excited by the ipsilateral Muller cell B1 and the contralateral Mauthner cell. CC1 interneurons were inhibitory. They were excited polysynaptically by ipsilateral sensory dorsal cells and were inhibited by contralateral dorsal cells. They were distinguished morphologically by having no rostral axon branch and no contralateral dendrites. CC1 interneurons were phasically active during fictive swimming with their peak depolarizations preceding those of myotomal motoneurons by about 0.15 cycle. 5. CC2 interneurons were also inhibitory, but they were distinguished from CC1 interneurons by their excitation from the ipsilateral Muller cells B2-4 nd by their thin rostral and thicker caudal axonal branches on the contralateral side of the spinal cord. 6. CC3 interneurons were excitatory, and they were inhibited by the ipsilateral Muller cell I1. CC3 interneurons could have contralateral dendrites and bifurcating axons, and they had lower average axonal conduction velocities than CC1 and CC2 interneurons. 7. Inhibitory CC interneurons may be important for motor coordination in the lamprey. Movements of the lamprey body during reflexes and swimming consist of contraction and relaxation of myotomal muscles on opposite sides of the body. By being coactive with ipsilateral myotomal motoneurons, inhibitory CC interneurons could contribute to the inhibition of contralateral motoneurons during these movements.

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Calcium Channel Subtypes in Lamprey Sensory and Motor Neurons

Journal of Neurophysiology ◽

10.1152/jn.1997.78.3.1334 ◽

1997 ◽

Vol 78 (3) ◽

pp. 1334-1340 ◽

Cited By ~ 52

Author(s):

A. El Manira ◽

N. Bussières

Keyword(s):

Spinal Cord ◽

Calcium Channels ◽

Calcium Channel ◽

Sensory Neurons ◽

Motor Neurons ◽

Calcium Channel Antagonist ◽

Calcium Currents ◽

Spinal Cord Neurons ◽

Channel Current ◽

Dorsal Cells

El Manira, A. and N. Bussières. Calcium channel subtypes in lamprey sensory and motor neurons. J. Neurophysiol. 78: 1334–1340, 1997. Pharmacologically distinct calcium channels have been characterized in dissociated cutaneous sensory neurons and motoneurons of the larval lamprey spinal cord. To enable cell identification, sensory dorsal cells and motoneurons were selectively labeled with fluorescein-coupled dextran amine in the intact spinal cord in vitro before dissociation. Calcium channels present in sensory dorsal cells, motoneurons, and other spinal cord neurons were characterized with the use of whole cell voltage-clamp recordings and specific calcium channel agonist and antagonists. The results show that a transient low-voltage-activated (LVA) calcium current was present in a proportion of sensory dorsal cells but not in motoneurons, whereas high-voltage-activated (HVA) calcium currents were seen in all neurons recorded. The different components of HVA current were dissected pharmacologically and similar results were obtained for both dorsal cells and motoneurons. The N-type calcium channel antagonist ω-conotoxin-GVIA(ω-CgTx) blocked >70% of the HVA current. A large part of the ω-CgTx block was reversed after washout of the toxin. The L-type calcium channel antagonist nimodipine blocked ∼15% of the total HVA current. The dihydropyridine agonist (±)-BayK 8644 markedly increased the amplitude of the calcium channel current. The BayK-potentiated current was not affected by ω-CgTx, indicating that the reversibility of the ω-CgTx effect is not due to a blockade of L-type channels. Simultaneous application of ω-CgTx and nimodipine left ∼15% of the HVA calcium channel current, a small part of which was blocked by the P/Q-type channel antagonist ω-agatoxin-IVA. In the presence of the three antagonists, the persistent residual current (∼10%) was completely blocked by cadmium. Our results provide evidence for the existence of HVA calcium channels of the N, L, and P/Q types and other HVA calcium channels in lamprey sensory neurons and motoneurons. In addition, certain types of neurons express LVA calcium channels.

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Effects of 5-hydroxytryptamine on the afterhyperpolarization, spike frequency regulation, and oscillatory membrane properties in lamprey spinal cord neurons

Journal of Neurophysiology ◽

10.1152/jn.1989.61.4.759 ◽

1989 ◽

Vol 61 (4) ◽

pp. 759-768 ◽

Cited By ~ 149

Author(s):

P. Wallen ◽

J. T. Buchanan ◽

S. Grillner ◽

R. H. Hill ◽

J. Christenson ◽

...

Keyword(s):

Spinal Cord ◽

Action Potential ◽

Late Phase ◽

Calcium Entry ◽

Spike Frequency ◽

Frequency Regulation ◽

Spinal Cord Neurons ◽

Cyclic Monophosphate ◽

Calcium Dependent ◽

Dorsal Cells

1. Local application of 5-hydroxytryptamine (5-HT) in the area in which a dense 5-HT plexus is located in the lamprey spinal cord leads to a marked depression of the late phase of the afterhyperpolarization (AHP) following the action potential. This effect was observed in motoneurons, premotor interneurons, and giant interneurons, whereas no effect was observed in the sensory dorsal cells and edge cells. 2. The late 5-HT sensitive phase of the AHP was increased in amplitude when calcium entry was enhanced during the prolongation of action potentials caused by tetraethylammonium (TEA). Conversely, a blockade of Ca2+ entry by manganese reduced the AHP amplitude, suggesting that a calcium-dependent current, most likely carried by potassium, underlies the late phase of the AHP in these cells, as is the case in many other types of neurons. 3. The late phase of the AHP could be depressed by 5-HT although no effects were exerted on either the resting input resistance or on the shape of the action potential in 54% of the cells. The membrane conductance increase associated with the late phase of the AHP was markedly attenuated by 5-HT application. 4. In voltage-clamp experiments, Na+ currents and most K+ currents were blocked by tetrodotoxin (TTX) and TEA, respectively. Under these conditions, voltage steps elicited a slow outward current, most likely representing a Ca2+-activated K+ current, which was depressed by 5-HT application. 5. 5-HT does not appear to reduce AHP amplitude by blocking the calcium entry occurring during the action potential. No evidence was obtained for an involvement of second messengers such as adenosine-3':5'-cyclic monophosphate (cAMP), guanosine-3':5'-cyclic monophosphate (cGMP), diacyglycerol, or arachidonic acid. The effect of 5-HT on the late AHP may be due to a direct action on the calcium-dependent potassium channels or on the intracellular handling of Ca2+ ions. 6. The amplitude reduction of the AHP has a profound influence on the spike frequency regulation of any given cell; the frequency of spikes evoked by a given excitatory stimulus is therefore markedly increased by application of 5-HT. 5-HT thus increases the "gain" of the input-output relation of interneurons and motoneurons responsible for generating the locomotor rhythm. In addition, 5-HT causes a prolongation of the depolarized plateau of the N-methyl-D-aspartate (NMDA) receptor-induced membrane potential oscillations, as expected from the 5-HT-induced effects on the Ca2+-activated K+ channels that contribute to the repolarization.

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

Journal of Neurophysiology ◽

10.1152/jn.1995.73.1.80 ◽

1995 ◽

Vol 73 (1) ◽

pp. 80-87 ◽

Cited By ~ 26

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)

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Activities of identified interneurons, motoneurons, and muscle fibers during fictive swimming in the lamprey and effects of reticulospinal and dorsal cell stimulation

Journal of Neurophysiology ◽

10.1152/jn.1982.47.5.948 ◽

1982 ◽

Vol 47 (5) ◽

pp. 948-960 ◽

Cited By ~ 134

Author(s):

J. T. Buchanan ◽

A. H. Cohen

Keyword(s):

Spinal Cord ◽

Muscle Fibers ◽

Membrane Potentials ◽

Pattern Generation ◽

The Body ◽

Swimming Activity ◽

Burst Intensity ◽

Intracellular Stimulation ◽

Dorsal Cells ◽

Stimulation Of

1. Application of D-glutamate to the isolated spinal cord of the lamprey produces phasic activity in ventral roots, which is similar to that of the muscles of the intact swimming animal (5,18). Therefore, the isolated spinal cord may be used as a convenient model for the investigation of the generation of locomotor rhythms in a vertebrate. 2. Almost all slow muscle fibers exhibited excitatory junctional potentials (EJPs) during swimming activity. The number of EJPs per cycle increased with the intensity of ventral root (VR) bursting. Few twitch fibers were active, and these fired action potentials only during high intensities of VR bursts. 3. As was found by Russell and Wallen (25), myotomal motoneurons had oscillating membrane potentials during fictive swimming which, on the average, reached a peak depolarization in the middle of the VR burst (phi = 0.21 +/- 0.05; phi = 0 is defined as the onset of the VR burst, and the duration of the cycle is set equal to 1). Membrane potential oscillations in fin motoneurons were antiphasic to those of nearby myotomal motoneurons (peak depolarization phi = 0.68 +/- 0.05). 4. Lateral interneurons had oscillating membrane potentials in synchrony with those of myotomal motoneurons (peak depolarization phi = 0.21 +/- 0.10). Interneurons with axons projecting contralaterally and caudally (CC interneurons) had oscillating membrane potentials that peaked significantly earlier in the cycle (peak depolarization phi = 0.06 +/- 0.12). 5. Edge cells were only weakly modulated during fictive swimming. Their peak depolarizations occurred near the end of the VR burst (phi = 0.33 +/- 0.10). Most giant interneurons were not phasically modulated during fictive swimming. 6. Repetitive intracellular stimulation of Muller cells during fictive swimming generally evoked an increased burst intensity in ipsilateral VRs and a decreased burst intensity in contralateral VRs. The cells M3, B1, and B2 also produced increases or decreases in the frequency of VR bursts. Repetitive intracellular stimulation of sensory dorsal cells could also change the intensities and timing of VR bursts. 7. This study is an initial survey of lamprey spinal interneurons that participate in swimming activity. Lateral interneurons and CC interneurons are active during fictive swimming and probably help coordinate the undulations of the body, but their roles in pattern generation are not known. The central pattern generator is subject to modification by descending and sensory inputs.

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