Neural mechanisms of intersegmental coordination in lamprey: local excitability changes modify the phase coupling along the spinal cord

1992 ◽  
Vol 67 (2) ◽  
pp. 373-388 ◽  
Author(s):  
T. Matsushima ◽  
S. Grillner

1. To elucidate the neural mechanisms responsible for coordinating undulatory locomotor movements, the intersegmental phase lag was analyzed from ventral roots along the spinal cord during fictive swimming. It was induced by bath application of N-methyl-D-aspartate (NMDA) in in vitro preparations of lamprey spinal cord, while the excitability of different segments were modified. The phase lag between consecutive segments during normal forward swimming is 1% of the cycle duration in a broad range of values. Rostral segments are activated before more caudal ones. 2. Under control conditions, whole preparations (12-24 segment long; n = 22) were perfused with NMDA solutions of the same concentration (100-150 microM). The intersegmental phase lag values varied in a continuous range with a single peak around a median value of forward +0.74% per segment (range: forward +2.23% to backward -0.97%). 3. To examine whether excitability differences along the spinal cord could modify the intersegmental phase lag, different levels of excitatory amino acids (NMDA) were applied to spinal cord preparations positioned in a partitioned chamber. Different portions of the cord could be perfused separately by NMDA solutions of different concentrations (50-150 microM). If rostral segments were perfused with the higher NMDA solution, the lag was inevitably in the forward direction. Conversely, if the caudal portion was perfused with the higher NMDA solution, caudally located ventral roots became activated before the rostral ventral roots in a caudorostral succession, thus reversing the direction of the fictive swimming wave to propagate as during backward swimming. If the middle portion was perfused by the highest NMDA solution, this portion instead became leading, and the activity propagated from this point in both the rostral and the caudal directions. The portion located in the pool with highest NMDA concentration always gave rise to a "leading" segment. 4. When a portion of the preparation was perfused with an NMDA solution of a high concentration (75-150 microM), the cycle duration was close to that recorded when the whole preparation was perfused with the same high NMDA solution. The ensemble cycle duration is, therefore, largely determined by the leading segment. 5. The phase lag changes were not restricted to the region around the barrier separating pools with different NMDA solutions.(ABSTRACT TRUNCATED AT 400 WORDS)

1992 ◽  
Vol 67 (6) ◽  
pp. 1683-1690 ◽  
Author(s):  
T. Matsushima ◽  
S. Grillner

1. The intersegmental coordination during undulatory locomotion in lamprey is characterized by a constant phase lag between consecutive segments, that is, the ratio between the intersegmental time lag and the cycle duration remains constant. It is shown that the spinal 5-HT (serotonin) system can, in a graded fashion, control the phase lag value from a rostrocaudal to a caudorostral lag corresponding to a reversed direction of swimming. These effects can be explained by a 5-HT-induced depression of Ca(2+)-dependent K+ channels (KCa channels) in network neurons. 2. The actions of the spinal 5-HT system were analyzed in the lamprey spinal cord preparation in vitro. Fictive swimming was induced by bath application of N-methyl-D-aspartate (NMDA). The intersegmental phase lag between ventral root burst activities was measured along the ipsilateral side of the spinal cord. The chamber with the preparation was partitioned into two pools so that the rostral and caudal halves of the preparation could be perfused independently with solutions containing the same level of NMDA (100-150 microM) with or without additional 5-HT or a 5-HT uptake blocker (citalopram). 3. Addition of 5-HT to one of these partitioned pools changed the intersegmental phase lag in this pool, whereas the cycle duration remained unchanged. It was determined by the activity in the "non-5-HT" pool. Addition of 5-HT to the caudal pool resulted in an increased rostrocaudal phase lag. When 5-HT was added to the rostral pool, on the other hand, the phase lag shifted direction to a backward coordination.(ABSTRACT TRUNCATED AT 250 WORDS)


1999 ◽  
Vol 82 (2) ◽  
pp. 1074-1077 ◽  
Author(s):  
Isabelle Delvolvé ◽  
Pascal Branchereau ◽  
Réjean Dubuc ◽  
Jean-Marie Cabelguen

An in vitro brain stem–spinal cord preparation from an adult urodele ( Pleurodeles waltl) was developed in which two fictive rhythmic motor patterns were evoked by bath application of N-methyl-d-aspartate (NMDA; 2.5–10 μM) with d-serine (10 μM). Both motor patterns displayed left-right alternation. The first pattern was characterized by cycle periods ranging between 2.4 and 9.0 s (4.9 ± 1.2 s, mean ± SD) and a rostrocaudal propagation of the activity in consecutive ventral roots. The second pattern displayed longer cycle periods (8.1–28.3 s; 14.2 ± 3.6 s) with a caudorostral propagation. The two patterns were inducible after a spinal transection at the first segment. Preliminary experiments on small pieces of spinal cord further suggested that the ability for rhythm generation is distributed along the spinal cord of this preparation. This study shows that the in vitro brain stem–spinal cord preparation from Pleurodeles waltl may be a useful model to study the mechanisms underlying the different axial motor patterns and the flexibility of the neural networks involved.


1999 ◽  
Vol 87 (3) ◽  
pp. 1066-1074 ◽  
Author(s):  
Chun-Kuei Su

To understand the origination of sympathetic nerve discharge (SND), I developed an in vitro brain stem-spinal cord preparation from neonatal rats. Ascorbic acid (3 mM) was added into the bath solution to increase the viability of preparations. At 24°C, rhythmic SND (recorded from the splanchnic nerve) was consistently observed, but it became quiescent at <16°C. Respiratory-related SND (rSND) was discernible and was well correlated with C4 root activity. Power spectral analysis of SND revealed a dominant 2-Hz oscillation. In most preparations (86%), such oscillation was persistent, whereas it only slightly reduced its magnitude after isolation from the brain stem. The removal of neural structures rostral to the superior cerebellar artery (equivalent to the level of facial nuclei) reduced rSND, increased tonic SND, but did not affect the temporal coupling between SND and C4 root activity. Our data suggest a prominent contribution of SND from the neural mechanisms confined within the neonatal rat spinal cord. This ascorbic acid-enhanced in vitro preparation is a very useful model to study neural mechanisms underlying sympathorespiratory integration.


1991 ◽  
Vol 65 (3) ◽  
pp. 454-467 ◽  
Author(s):  
J. Keifer ◽  
J. C. Houk

1. Bursts of discharge have been recorded in the red nucleus in several species and are thought to represent the expression of motor commands. A cerebellorubral circuit comprised of recurrent connections among the cerebellum, red nucleus, and reticular formation was postulated to function as a positive feedback loop that generates these motor commands and transmits them to the spinal cord via the rubrospinal pathway. We have used an in vitro preparation from the turtle that leaves the circuitry connecting the cerebellum, brain stem, and spinal cord intact to study the role of excitatory amino acid neurotransmitters and recurrent excitation in mediating the generation of burst discharges in the red nucleus. 2. Burst discharges were recorded extracellularly from single cells in the red nucleus in response to single pulse or brief train stimulation of the contralateral spinal cord or brief train stimuli applied to the ipsilateral cerebellar cortex. The firing characteristics and pharmacologic sensitivities of the bursts were independent of the type of stimulus used. The bursts had long durations ranging from 2 to 17 s and showed spike frequency adaptation. 3. Transection of the cerebellar peduncle, which eliminates inhibition impinging onto the cerebellorubral circuit, greatly enhanced the spontaneous activity and burst discharges recorded in the contralateral red nucleus. Furthermore, bath application of a solution containing elevated levels of calcium and magnesium blocked the expression of burst discharges even though synaptic activation of the neurons was not blocked. 4. The possibility that excitatory amino acid receptors mediate burst responses in the red nucleus was investigated in light of the antagonistic effects of elevated magnesium ions on bursting. Bath application of 100 microns DL-2-amino-5-phosphonovaleric acid (APV), a specific N-methyl-D-aspartate (NMDA) receptor antagonist; [10 microM 6-cyano-7-nitroquinoxaline-2,3-dione (CNQX)], a specific non-NMDA receptor antagonist; or 100 microM, DL-2-amino-4-phosphonobutyric acid (AP4), an agonist of a fourth class of excitatory amino acid receptor, blocked burst activity in the red nucleus. With a multibarreled pipette for simultaneous ejection of drug and recording, iontophoresis of APV or CNQX into the red nucleus blocked bursting whereas AP4 failed to show a significant effect. These data suggest that red nucleus neurons have both NMDA and non-NMDA receptors. The site of action of the AP4-sensitive receptor appears to be elsewhere in the cerebellorubral circuit. 5. Iontophoretic application of excitatory amino acid receptor agonists NMDA and quisqualate (Q) induced excitation of red nucleus neurons.(ABSTRACT TRUNCATED AT 400 WORDS)


1985 ◽  
Vol 54 (4) ◽  
pp. 959-977 ◽  
Author(s):  
C. M. Rovainen

Fictive swimming activity was induced in isolated spinal cords of adult lampreys Ichthyomyzon unicuspis and Petromyzon marinus by addition of D-glutamate or N-methyl-D,L-aspartate (NMA) to the bathing fluid. Propriospinal interneurons are defined as nerve cells within the spinal cord with projections longer than 1 segment. The hypothesis that propriospinal interneurons contribute to intersegmental coordination during fictive swimming was tested using electrical stimulation, extracellular recording, and separated compartments. Stimulation of the split caudal end of the spinal cord indirectly excited ascending propriospinal interneurons, which enhanced and entrained bursts in rostral contralateral ventral roots. Indirect electrical stimulation of descending propriospinal interneurons could delay and diminish bursts in caudal contralateral ventral roots. Extracellular recordings from the rostral and caudal split ends of the spinal cord sometimes showed spike activities in phase with contralateral or ipsilateral ventral roots. Inhibition of 1-3 segments by spot applications of glycine or gamma-aminobutyric acid (GABA) did not interrupt normal coordination or rostrocaudal phase lag. When a middle region of spinal cord was inhibited in a compartment with GABA or glycine, the caudal spinal cord could entrain the bursts in rostral ventral roots. In a few preparations the caudal region induced antiphasic bursts in previously silent rostral roots through the inhibited region. The maximum separation for caudal-upon-rostral antiphasic entrainment was approximately 20 segments in Ichthyomyzon and 36 segments in Petromyzon. Increased concentrations of an excitatory amino acid in a rostral compartment could produce descending entrainment of bursts in an adjacent caudal compartment at a higher frequency with rostrocaudal phase lag. The rostral-upon-caudal entrainment could still occur through spot applications of GABA or glycine but not through long inhibited regions. Two hypothetical groups of propriospinal interneurons are proposed for the coordination of swimming activities in the isolated spinal cords of adult lampreys. 1) Crossed, ascending interneurons may be excited in phase with nearby motoneurons and may excite and entrain rostral pattern generators on the opposite side. 2) Short, commissural interneurons may be excited in phase with nearby motoneurons and may inhibit contralateral generators.


2012 ◽  
Vol 107 (8) ◽  
pp. 2250-2259 ◽  
Author(s):  
S. Clemens ◽  
A. Belin-Rauscent ◽  
J. Simmers ◽  
D. Combes

The role of dopamine in regulating spinal cord function is receiving increasing attention, but its actions on spinal motor networks responsible for rhythmic behaviors remain poorly understood. Here, we have explored the modulatory influence of dopamine on locomotory central pattern generator (CPG) circuitry in the spinal cord of premetamorphic Xenopus laevis tadpoles. Bath application of exogenous dopamine to isolated brain stem-spinal cords exerted divergent dose-dependent effects on spontaneous episodic patterns of locomotory-related activity recorded extracellularly from spinal ventral roots. At low concentration (2 μM), dopamine reduced the occurrence of bursts and fictive swim episodes and increased episode cycle periods. In contrast, at high concentration (50 μM) dopamine reversed its actions on fictive swimming, now increasing both burst and swim episode occurrences while reducing episode periods. The low-dopamine effects were mimicked by the D2-like receptor agonists bromocriptine and quinpirole, whereas the D1-like receptor agonist SKF 38393 reproduced the effects of high dopamine. Furthermore, the motor response to the D1-like antagonist SCH 23390 resembled that to the D2 agonists, whereas the D2-like antagonist raclopride mimicked the effects of the D1 agonist. Together, these findings indicate that dopamine plays an important role in modulating spinal locomotor activity. Moreover, the transmitter's opposing influences on the same target CPG are likely to be accomplished by a specific, concentration-dependent recruitment of independent D2- and D1-like receptor signaling pathways that differentially mediate inhibitory and excitatory actions.


2008 ◽  
Vol 99 (5) ◽  
pp. 2408-2419 ◽  
Author(s):  
Eric D. Tytell ◽  
Avis H. Cohen

In fishes, undulatory swimming is produced by sets of spinal interneurons constituting a central pattern generator (CPG). The CPG generates waves of muscle activity that travel from head to tail, which then bend the body into wave shapes that also travel from head to tail. In many fishes, the wavelengths of the neural and mechanical waves are different, resulting in a rostral-to-caudal gradient in phase lag between muscle activity and bending. The neural basis of this phase gradient was investigated in the lamprey spinal cord using an isolated in vitro preparation. Fictive swimming was induced using d-glutamate and the output of the CPG was measured using suction electrodes placed on the ventral roots. The spinal cord was bent sinusoidally at various points along its length. First, the ranges of entrainment were estimated. Middle segments were able to entrain to frequencies approximately twice as high as those at end segments. Next, phase lags between centers of ventral root bursts and the stimulus were determined. Two halves of the cycle were identified: stretching and shortening of the edge of spinal cord on the same side as the electrode. Stimuli at rostral segments tended to entrain segmental bursting at the beginning of the stretch phase, almost 50% out of phase with previously measured in vivo electromyography data. Stimuli at caudal segments, in contrast, entrained segments at the end of stretch and the beginning of shortening, approximately the same phase as in vivo data.


1988 ◽  
Vol 2 (7) ◽  
pp. 2283-2288 ◽  
Author(s):  
Jeffrey C. Smith ◽  
Jack L. Feldman ◽  
Brian J. Schmidt

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