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

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.

2004 ◽  
Vol 92 (3) ◽  
pp. 1384-1390 ◽  
Author(s):  
James F. Einum ◽  
James T. Buchanan

Reticulospinal neurons of the lamprey brain stem receive rhythmic input from the spinal cord during locomotor activity. The goal of the present study was to determine whether such spinal input has a direct component to reticulospinal neurons or depends on brain stem interneurons. To answer this question, an in vitro lamprey brain stem-spinal cord preparation was used with a diffusion barrier placed caudal to the obex, separating the experimental chamber into two baths. Locomotor activity was induced in the spinal cord by perfusion of d-glutamate or N-methyl-dl-aspartate into the spinal cord bath. The brain stem bath was first perfused with normal Ringer solution followed by a high-Ca2+, -Mg2+ solution, which reduced polysynaptic transmission. The amplitudes of membrane potential oscillations of reticulospinal neurons in the posterior and middle rhombencephalic reticular nuclei (PRRN and MRRN, respectively) recorded with sharp intracellular microelectrodes did not significantly change from normal to high-divalent solution. This finding suggests a large part of the spinal input creating the oscillations is direct to the reticulospinal neurons. Application of strychnine to the high-Ca2+, -Mg2+ solution decreased membrane potential oscillation amplitude, and injection of Cl− reversed presumed inhibitory postsynaptic potentials, indicating a role for direct spinal inhibitory inputs. Although reduced, the persistence of oscillations in strychnine suggests that spinal excitatory inputs also contribute to the oscillations. Thus it was concluded that both excitatory and inhibitory spinal neurons provide direct rhythmic inputs to reticulospinal cells of the PRRN and MRRN during locomotor activity. These inputs provide reticulospinal cells with information regarding the activity of the spinal locomotor networks.


1999 ◽  
Vol 81 (5) ◽  
pp. 2037-2045 ◽  
Author(s):  
James T. Buchanan

Commissural interneurons in rhythm generation and intersegmental coupling in the lamprey spinal cord. To test the necessity of spinal commissural interneurons in the generation of the swim rhythm in lamprey, longitudinal midline cuts of the isolated spinal cord preparation were made. Fictive swimming was then induced by bath perfusion with an excitatory amino acid while recording ventral root activity. When the spinal cord preparation was cut completely along the midline into two lateral hemicords, the rhythmic activity of fictive swimming was lost, usually replaced with continuous ventral root spiking. The loss of the fictive swim rhythm was not due to nonspecific damage produced by the cut because rhythmic activity was present in split regions of spinal cord when the split region was still attached to intact cord. The quality of this persistent rhythmic activity, quantified with an autocorrelation method, declined with the distance of the split spinal segment from the remaining intact spinal cord. The deterioration of the rhythm was characterized by a lengthening of burst durations and a shortening of the interburst silent phases. This pattern of deterioration suggests a loss of rhythmic inhibitory inputs. The same pattern of rhythm deterioration was seen in preparations with the rostral end of the spinal cord cut compared with those with the caudal end cut. The results of this study indicate that commissural interneurons are necessary for the generation of the swimming rhythm in the lamprey spinal cord, and the characteristic loss of the silent interburst phases of the swimming rhythm is consistent with a loss of inhibitory commissural interneurons. The results also suggest that both descending and ascending commissural interneurons are important in the generation of the swimming rhythm. The swim rhythm that persists in the split cord while still attached to an intact portion of spinal cord is thus imposed by interneurons projecting from the intact region of cord into the split region. These projections are functionally short because rhythmic activity was lost within approximately five spinal segments from the intact region of spinal cord.


1989 ◽  
Vol 62 (1) ◽  
pp. 59-69 ◽  
Author(s):  
J. T. Buchanan ◽  
S. Grillner ◽  
S. Cullheim ◽  
M. Risling

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.


2000 ◽  
Vol 83 (5) ◽  
pp. 2497-2507 ◽  
Author(s):  
David Parker

The modulatory effects of neuropeptides on descending inputs to the spinal cord have been examined by making paired recordings from reticulospinal axons and spinal neurons in the lamprey. Four peptides were examined; peptide YY (PYY) and cholecystokinin (CCK), which are contained in brain stem reticulospinal neurons, and calcitonin-gene–related peptide (CGRP) and neuropeptide Y (NPY), which are contained in primary afferents and sensory interneurons, respectively. Each of the peptides reduced the amplitude of monosynaptic reticulospinal-evoked excitatory postsynaptic potentials (EPSPs). The modulation appeared to be presynaptic, because postsynaptic input resistance and membrane potential, the amplitude of the electrical component of the EPSP, postsynaptic responses to glutamate, and spontaneous miniature EPSP amplitudes were unaffected. In addition, none of the peptides affected the pattern of N-methyl-d-aspartate (NMDA)–evoked locomotor activity in the isolated spinal cord. Potential interactions between the peptides were also examined. The “brain stem peptides” CCK and PYY had additive inhibitory effects on reticulospinal inputs, as did the “sensory peptides” CGRP and NPY. Brain stem peptides also had additive inhibitory effects when applied with sensory peptides. However, sensory peptides increased or failed to affect the amplitude of reticulospinal inputs in the presence of the brain stem peptides. These interactive effects also appear to be mediated presynaptically. The functional consequence of the peptidergic modulation was investigated by examining spinal ventral root responses elicited by brain stem stimulation. CCK and CGRP both reduced ventral root responses, although in interaction both increased the response. These results thus suggest that neuropeptides presynaptically influence the descending activation of spinal locomotor networks, and that they can have additive or novel interactive effects depending on the peptides examined and the order of their application.


1995 ◽  
Vol 73 (1) ◽  
pp. 80-87 ◽  
Author(s):  
J. T. Buchanan ◽  
S. Kasicki

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)


2008 ◽  
Vol 100 (1) ◽  
pp. 117-128 ◽  
Author(s):  
Ian T. Gordon ◽  
Mary J. Dunbar ◽  
Kimberly J. Vanneste ◽  
Patrick J. Whelan

At birth, thoracosacral spinal cord networks in mouse can produce a coordinated locomotor-like pattern. In contrast, less is known about the cervicothoracic networks that generate forelimb locomotion. Here we show that cervical networks can produce coordinated rhythmic patterns in the brain stem-spinal cord preparation of the mouse. Segmentally the C5 and C8 neurograms were each found to be alternating left-right, and the ipsilateral C5 and C8 neurograms also alternated. Collectively these patterns were suggestive of locomotor-like activity. This pattern was not dependent on the presence of thoracosacral segments because they could be evoked following a complete transection of the spinal cord at T5. We next demonstrated that activation of thoracosacral networks either pharmacologically or by stimulation of sacrocaudal afferents could produce rhythmic activity within the C5 and C8 neurograms. On the other hand, pharmacological activation of cervical networks did not evoke alternating cervical rhythmic activity either in isolated cervicothoracic or -sacral preparations. Under these conditions, we found that activation of cervicothoracic networks could alter the timing of thoracosacral locomotor-like patterns. When thoracosacral networks were not activated pharmacologically but received rhythmic drive from cervicothoracic networks, a pattern of slow bursts with superimposed fast synchronous oscillations became the dominant lumbar neurogram pattern. Our data suggest that in neonatal mice the cervical CPG is capable of producing coordinated rhythmic patterns in the absence of input from lumbar segments, but caudorostral drive contributes to cervical patterns and rhythm stability.


2001 ◽  
Vol 91 (6) ◽  
pp. 2703-2712 ◽  
Author(s):  
Stephen M. Johnson ◽  
Julia E. R. Wilkerson ◽  
Daniel R. Henderson ◽  
Michael R. Wenninger ◽  
Gordon S. Mitchell

Brain stem preparations from adult turtles were used to determine how bath-applied serotonin (5-HT) alters respiration-related hypoglossal activity in a mature vertebrate. 5-HT (5–20 μM) reversibly decreased integrated burst amplitude by ∼45% ( P < 0.05); burst frequency decreased in a dose-dependent manner with 20 μM abolishing bursts in 9 of 13 preparations ( P < 0.05). These 5-HT-dependent effects were mimicked by application of a 5-HT1A agonist, but not a 5-HT1B agonist, and were abolished by the broad-spectrum 5-HT antagonist, methiothepin. During 5-HT (20 μM) washout, frequency rebounded to levels above the original baseline for 40 min ( P < 0.05) and remained above baseline for 2 h. A 5-HT3 antagonist (tropesitron) blocked the post-5-HT rebound and persistent frequency increase. A 5-HT3 agonist (phenylbiguanide) increased frequency during and after bath application ( P < 0.05). When phenylbiguanide was applied to the brain stem of brain stem/spinal cord preparations, there was a persistent frequency increase ( P < 0.05), but neither spinal-expiratory nor -inspiratory burst amplitude were altered. The 5-HT3receptor-dependent persistent frequency increase represents a unique model of plasticity in vertebrate rhythm generation.


1989 ◽  
Vol 257 (3) ◽  
pp. H785-H790
Author(s):  
T. Sakamoto ◽  
W. W. Monafo

[14C]butanol tissue uptake was used to measure simultaneously regional blood flow in three regions of the brain (cerebral and cerebellar hemispheres and brain stem) and in five levels of the spinal cord in 10 normothermic rats (group A) and in 10 rats in which rectal temperature had been lowered to 27.7 +/- 0.3 degrees C by applying ice to the torso (group B). Pentobarbital sodium anesthesia was used. Mean arterial blood pressure varied minimally between groups as did arterial pH, PO2, and PCO2. In group A, regional spinal cord blood flow (rSCBF) varied from 49.7 +/- 1.6 to 62.6 +/- 2.1 ml.min-1.100 g-1; in brain, regional blood flow (rBBF) averaged 74.4 +/- 2.3 ml.min-1.100 g-1 in the whole brain and was highest in the brain stem. rSCBF in group B was elevated in all levels of the cord by 21-34% (P less than 0.05). rBBF, however, was lowered by 21% in the cerebral hemispheres (P less than 0.001) and by 14% in the brain as a whole (P less than 0.05). The changes in calculated vascular resistance tended to be inversely related to blood flow in all tissues. We conclude that rBBF is depressed in acutely hypothermic pentobarbital sodium-anesthetized rats, as has been noted before, but that rSCBF rises under these experimental conditions. The elevation of rSCBF in hypothermic rats confirms our previous observations.


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