Ontogeny of Rhythmic Motor Patterns Generated in the Embryonic Rat Spinal Cord

2003 ◽  
Vol 89 (3) ◽  
pp. 1187-1195 ◽  
Author(s):  
Jun Ren ◽  
John J. Greer
Keyword(s):  
Spinal Cord ◽  
Spontaneous Activity ◽  
Developmental Stages ◽  
Rhythmic Activity ◽  
Late Gestation ◽  
Spatiotemporal Pattern ◽  
Rat Spinal Cord ◽  
Motor Patterns ◽  
Rhythmic Motor

Patterned spontaneous activity is generated in developing neuronal circuits throughout the CNS including the spinal cord. This activity is thought to be important for activity-dependent neuronal growth, synapse formation, and the establishment of neuronal networks. In this study, we examine the spatiotemporal distribution of motor patterns generated by rat spinal cord and medullary circuits from the time of initial axon outgrowth through to the inception of organized respiratory and locomotor rhythmogenesis during late gestation. This includes an analysis of the neuropharmacological control of spontaneous rhythms generated within the spinal cord at different developmental stages. In vitro spinal cord and medullary-spinal cord preparations isolated from rats at embryonic ages (E)13.5–E21.5 were studied. We found age-dependent changes in the spatiotemporal pattern, neurotransmitter control, and propensity for the generation of spontaneous rhythmic motor discharge during the prenatal period. The developmental profile of the neuropharmacological control of rhythmic bursting can be divided into three periods. At E13.5–E15.5, the spinal networks comprising cholinergic and glycinergic synaptic interconnections are capable of generating rhythmic activity, while GABAergic synapses play a role in supporting the spontaneous activity. At late stages (E18.5–E21.5), glutamate drive acting via non- N-methyl-d-aspartate (non-NMDA) receptors is primarily responsible for the rhythmic activity. During the middle stage (E16.5–E17.5), the spontaneous activity results from the combination of synaptic drive acting via non-NMDA glutamatergic, nicotinic acetylcholine, glycine, and GABAA receptors. The modulatory actions of chloride-mediated conductances shifts from predominantly excitatory to inhibitory late in gestation.

Effects of inhibitory amino acid antagonists on reciprocal inhibitory interactions during rhythmic motor activity in the in vitro neonatal rat spinal cord

1995 ◽  
Vol 74 (3) ◽  
pp. 1109-1117 ◽  
Author(s):  
K. C. Cowley ◽  
B. J. Schmidt
Keyword(s):  
Spinal Cord ◽  
Motor Activity ◽  
Receptor Agonist ◽  
Gabab Receptor ◽  
Glycine Receptor ◽  
Rhythmic Activity ◽  
Neonatal Rat ◽  
Rat Spinal Cord ◽  
Rhythmic Motor

1. The role of inhibitory amino acid transmission in the coordination and generation of rhythmic motor activity was examined with the use of an in vitro neonatal rat spinal cord preparation. Before adding gamma-aminobutyric acid (GABA) or glycine receptor agonists and antagonists, rhythmic motor activity was induced by bath application of acetylcholine (ACh), N-methyl-D,L-aspartate (NMA), or serotonin (5-HT) while monitoring bilateral ankle flexor and extensor electroneurograms (ENGs). The timing of rhythmic flexor and extensor discharge was consistent with that seen during overground locomotion in 27% of 84 bath applications of these substances (n = 65 preparations). 2. Subsequent addition of the GABAA receptor agonist muscimol, the GABAB receptor agonist baclofen, or glycine, abolished rhythmic activity in 95% of the tested applications. 3. GABAB receptor blockade did not disrupt alternating patterns of ENG discharge. However, addition of the GABAA receptor antagonist bicuculline, or the glycine receptor antagonist strychnine, transformed alternating flexor-extensor and left-right activity into patterns characterized by bilaterally synchronous rhythmic activation of all hindlimb ENGs. The onset of individual ENG bursts was more abrupt following bicuculline or strychnine. Strychnine also synchronized high-frequency (4-8 Hz) packets of rhythmic discharge within ENG bursts. 4. Some preparations developed synchronous, but unstable, rhythmic activity in the presence of bicuculline or strychnine alone. However, NMA, 5-HT, or ACh was usually required in addition to these antagonists to promote sustained rhythmic activity.(ABSTRACT TRUNCATED AT 250 WORDS)

scholarly journals Fictive Rhythmic Motor Patterns Induced by NMDA in an In Vitro Brain Stem–Spinal Cord Preparation From an Adult Urodele

1999 ◽  
Vol 82 (2) ◽  
pp. 1074-1077 ◽  
Author(s):  
Isabelle Delvolvé ◽  
Pascal Branchereau ◽  
Réjean Dubuc ◽  
Jean-Marie Cabelguen
Keyword(s):  
Spinal Cord ◽  
Brain Stem ◽  
Rhythm Generation ◽  
Motor Patterns ◽  
Rhythmic Motor ◽  
Bath Application ◽  
The Neural Networks ◽  
Ventral Roots ◽  
Pleurodeles Waltl

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.

Extracellular K+ Induces Locomotor-Like Patterns in the Rat Spinal Cord In Vitro: Comparison With NMDA or 5-HT Induced Activity

1998 ◽  
Vol 79 (5) ◽  
pp. 2643-2652 ◽  
Author(s):  
E. Bracci ◽  
M. Beato ◽  
A. Nistri
Keyword(s):  
Spinal Cord ◽  
Threshold Concentration ◽  
Pattern Generation ◽  
Neonatal Rat ◽  
Rat Spinal Cord ◽  
Motor Patterns ◽  
Pattern Frequency ◽  
High K ◽  
In Vitro Comparison

Bracci, E., M. Beato, and A. Nistri. Extracellular K+ induces locomotor-like patterns in the rat spinal cord in vitro: comparison with NMDA or 5-HT induced activity. J. Neurophysiol. 79: 2643–2652, 1998. Bath-application of increasing concentrations of extracellular K+ elicited alternating motor patterns recorded from pairs of various lumbar ventral roots of the neonatal rat (0–2 days old) spinal cord in vitro. The threshold concentration of K+ for this effect was 7.9 ± 0.8 mM (mean ± SD). The suprathreshold concentration range useful to evoke persistent motor patterns (lasting ≥10 min) was very narrow (∼1 mM) as further increments elicited only rhythmic activity lasting from 20 s to a few minutes. On average, the fastest period of rhythmic patterns was 1.1 ± 0.3 s. Intracellular recording from lumbar motoneurons showed that raised extracellular K+ elicited membrane potential oscillations with superimposed repetitive firing. In the presence of N-methyl-d-aspartate (NMDA) or non-NMDA receptor blockers [ R(−)-2-amino-phosphonovaleric acid or 6-cyano-7-nitroquinoxaline-2,3-dione, respectively] extracellular K+ increases could still induce motor patterns although the threshold concentration was raised. Serotonin (5-HT) also induced alternating motor patterns (threshold 15 ± 7 μM) that were consistently slower than those induced by high K+ or NMDA. Ritanserin (1 μM) prevented the locomotor-like activity of 5-HT but not that of high K+ provided the concentration of the latter was further increased. Subthreshold concentrations of K+ became effective in the presence of subthreshold doses of 5-HT or NMDA, indicating mutual facilitation between these substances. The fastest pattern frequency was observed by raising K+ or by adding NMDA. In the presence of 5-HT, the pattern frequency was never as fast even if NMDA (or high K+) was coapplied. Furthermore, application of 5-HT significantly slowed down the K+- or NMDA-induced rhythm, an effect strongly potentiated in the presence of ritanserin. It is suggested that the operation of the spinal locomotor network was activated by rises in extracellular K+, which presumably led to a broad increase in neuronal excitability. Whenever the efficiency of excitatory synaptic transmission was diminished (for example by glutamate receptor antagonism), a larger concentration of K+ was required to evoke locomotor-like patterns. The complex effect (comprising stimulation and inhibition) of 5-HT on alternating pattern generation appeared to result from a dual action of this substance on the spinal locomotor network.

scholarly journals How does the Lamprey Central Nervous System make the Lamprey Swim?

1984 ◽  
Vol 112 (1) ◽  
pp. 337-357 ◽  
Author(s):  
STEN GRILLNER ◽  
PETER WALLÉN
Keyword(s):  
Spinal Cord ◽  
Nmda Receptor ◽  
Morphological Characteristics ◽  
Rhythmic Activity ◽  
The Body ◽  
Fictive Locomotion ◽  
Motor Patterns ◽  
Motor Neurones ◽  
Receptor Blockers

The lamprey spinal cord, in isolation or with the brainstem, can be used in vitro. The motor patterns underlying the swimming movements can be elicited by: (1) a pharmacological activation of a specific type of neuronal receptor (NMDA-receptor), that may in other systems give rise to an unstable membrane potential, (2) by stimulation of the brainstem or (3) by tactile activation of skin regions left innervated. In the latter case the initiation of ‘fictive’ swimming is partially caused by a release of a transmitter activating NMDA-receptors, as judged by the effect of NMDA-receptor blockers. The central pattern generator (CPG) is strongly influenced by feedback from mechanosensitive elements, which at least partially reside within the spinal cord. The edge cell in the lamprey spinal cord serves as an intraspinal mechanoreceptor. The ability to generate a coordinated motor output is distributed, since spinal cord sections down to 1.5–2 segments can be made to generate alternating activity. Motor neurones receive an approximately synchronous alternating excitatory and inhibitory drive in each swim cycle and do not appear to be part of the CPG. Motor neurones supplying different parts of the body wall on the same side of a body segment have different morphology with ramifications around different descending axons. The input drive signal during fictive locomotion to motor neurones located close to each other but with different morphological characteristics may differ substantially with regard to the γ-relationship (±25%) and the shape of the oscillation. This implies that even at a segmental level motor neurones may be further subdivided, and furthermore that the ipsilateral network generating the drive signal to ipsilateral motor neurones generates a more complex and individualized output than previously assumed. Motor neurones are not part of the rhythm-generating circuit. The large identifiable interneurones are not required for rhythmic activity to occur although they may be phasically active in the swim cycle. The small segmental interneurones have not yet been completely characterized. Many are phasically active during ‘fictive locomotion’ and lack an apparent axon. Their phase relationships in relation to the burst patterns vary over the entire swim cycle.

Respiratory and locomotor patterns generated in the fetal rat brain stem-spinal cord in vitro

1992 ◽  
Vol 67 (4) ◽  
pp. 996-999 ◽  
Author(s):  
J. J. Greer ◽  
J. C. Smith ◽  
J. L. Feldman
Keyword(s):  
Spinal Cord ◽  
Brain Stem ◽  
Cellular Mechanisms ◽  
Motor Patterns ◽  
Rhythmic Motor ◽  
Fetal Rat ◽  
Fetal Rats ◽  
Locomotor Patterns ◽  
Fetal Rat Brain

An in vitro brain stem-spinal cord preparation from last trimester (E13-E21) fetal rats, which generates rhythmic respiratory and locomotor patterns, is described. These coordinated motor patterns emerge at stages E17-E18. Synchronous rhythmic motor activity, not clearly characterized as respiratory or locomotor, can occur as early as E13. With this preparation, it is now possible to study the ontogenesis of circuits and cellular mechanisms underlying these critical movements.

Rhythmic Motor Activity in Thin Transverse Slice Preparations of the Fetal Rat Spinal Cord

2004 ◽  
Vol 92 (1) ◽  
pp. 648-652 ◽  
Author(s):  
Kiyomi Nakayama ◽  
Hiroshi Nishimaru ◽  
Norio Kudo
Keyword(s):  
Spinal Cord ◽  
Motor Activity ◽  
Temporal Correlation ◽  
Rhythmic Activity ◽  
Lumbar Spinal Cord ◽  
Rat Spinal Cord ◽  
Commissural Neurons ◽  
Rhythmic Motor ◽  
Lumbar Spinal ◽  
Transverse Slice

Networks generating locomotor-like rhythmic motor activity are formed during the last week of the fetal period in the rat spinal cord. We investigated the coordinated rhythmic motor activity induced in transverse slice preparations of the lumbar spinal cord taken from fetal rats as early as embryonic day (E) 16.5. In slices as thin as 100 μm, bath-application of 5-hydroxytryptamine (5-HT) induced rhythmic [Ca2+]i elevations in motoneurons labeled with Calcium Green-1 dextran. The rhythmic [Ca2+]i elevations were similar in frequency to that in the intact lumbar spinal cord, although there was no temporal correlation between the activity in the left and right sides of 100-μm slices. Such rhythmic [Ca2+]i elevations were observed in the slices taken from all lumbar segments. Moreover, the rhythmic activity was abolished by simultaneous blockade of glutamate, glycine, and GABAA receptors, indicating that synaptic transmission mediated by these receptors is important for the generation of the rhythm in these slices. Synchronous rhythmic activity between the left-right sides was found in slices thicker than 200 μm taken from any segmental level of the lumbar spinal cord. In these preparations, commissural neurons were activated synchronously with ipsilateral motoneurons. These results indicate that the neuronal networks sufficient to generate coordinated rhythmic activity are contained in one-half of a single lumbar segment at E16.5. Such spinal cord slices are a promising experimental model to investigate the neuronal mechanisms and the development of rhythm generation in the spinal cord.

Neuronal Bursting Induced by NK3 Receptor Activation in the Neonatal Rat Spinal Cord In Vitro

2001 ◽  
Vol 86 (6) ◽  
pp. 2939-2950 ◽  
Author(s):  
Cristina Marchetti ◽  
Andrea Nistri
Keyword(s):  
Spinal Cord ◽  
Membrane Potential ◽  
Dorsal Root ◽  
Extracellular Recording ◽  
Rhythmic Activity ◽  
Input Resistance ◽  
Receptor Activation ◽  
Neonatal Rat ◽  
Rat Spinal Cord

Intracellular recording from lumbar motoneurons and extracellular recording from ventral roots of the neonatal rat isolated spinal cord were used to study the mechanisms responsible for the excitation mediated by NK3 tachykinin receptors. The selective NK3 agonists senktide or [MePhe7]neurokinin B induced a slow depolarization with superimposed oscillations (mean period ± SD was 2.8 ± 0.8 s) that, in the majority of cases, showed left-right alternation at segmental level and were synchronous between L2 and L5 of the same side. During agonist wash out (5–20 min) a delayed form of hyperexcitability emerged consisting of bursts lasting 8 ± 2 s (average interburst interval 55 ± 21 s) with superimposed oscillations usually with homosegmental alternation and heterosegmental synchronicity. Such bursting was accompanied by depression of GABAergic dorsal root potentials evoked by dorsal root stimulation and of the recurrent inhibitory postsynaptic potential recorded from motoneurons. Despite bursting, motoneuron membrane potential returned to baseline while input resistance was increased. Bursts were a network-dependent phenomenon triggered by previous NK3 receptor activation because bursting was suppressed by glutamate receptor antagonists and was insensitive to motoneuron membrane potential or subsequent application of an NK3 receptor antagonist. NK3 receptors operated synergistically with N-methyl-d-aspartate (NMDA) and 5-hydroxytryptamine (5-HT) to trigger fully alternating locomotor-like rhythms while NK3 receptor antagonism disrupted the same rhythm. In summary, in the neonatal rat spinal cord NK3 receptors could trigger rhythmic activity predominantly with alternation at segmental level but with synchronous coupling between ipsilateral motor pools. NK3receptor activation could also facilitate fictive locomotor patterns induced by NMDA and 5-HT.

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