Excitatory amino acid receptors in Xenopus embryo spinal cord and their role in the activation of swimming.

Dale, Nicholas; Roberts, Alan

doi:10.1113/jphysiol.1984.sp015123

Cited by 136 publications

(82 citation statements)

References 21 publications

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“…In both animals, bath-applied agonists acting at either NMDA or kainate receptors can activate swimming (Brodin et al, 1985;Dale and Roberts, 1984;Grillner et al, 198 1;Poon, 1980). The natural activation of swimming in the embryo appears to depend on a transmitter acting at NMDA and kainate receptors (Dale andRoberts, 1983, 1984), and the same seems to be true for the lamprey (Brodin and Grillner, 1985).…”

Section: Possible Anatomical Substratementioning

confidence: 86%

“…NMDA receptor antagonists When 100 MM APV, a specific NMDA antagonist (Brodin and Grillner, 1985;Dale and Grillner, 1986;Dale and Roberts, 1984;Davies et al, 198 1;Wall& and Grillner, 1985), was applied to the bathing medium surrounding the caudal spinal cord, it reversibly abolished rhythmic ventral root activity in the caudal part but did not affect or weaken ongoing ventral root activity in the rostra1 spinal cord (Fig. 6).…”

Section: Resultsmentioning

confidence: 99%

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Excitatory synaptic drive for swimming mediated by amino acid receptors in the lamprey

Dale¹

1986

J. Neurosci.

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In order to investigate the properties and pharmacology of the excitatory synaptic drive received by motoneurons during swimming in the lamprey, propriospinal excitatory interneurons were activated as a population by the regional application of N-methyl-r+-aspartate (NMA) to either the 6-8 rostral-most or the 6-8 caudal-most segments of lengths of isolated spinal cord. This caused a rhythmic motor output to be generated in these regions. Synaptic potentials that were phase-locked to, and dependent on, the rhythmic motor activity of the segments exposed to the agonist could be recorded in motoneurons lying outside the activated regions.The synaptic drive to motoneurons located rostra1 or caudal to the activated regions was studied. Motoneurons received both descending and ascending synaptic input, which consisted of alternating excitatory and inhibitory phases. The inhibition could be reversed by chloride injection and blocked by strychnine, leaving an oscillating excitatory phase. The descending excitatory drive could extend l-9 segments from the active region, while the ascending excitatory drive was recorded only in motoneurons that were l-3 segments rostra1 to the active region. Both types of drive occurred in phase with the ipsilateral ventral root discharge: The peak depolarization of the descending drive occurred at the same point in the swimming cycle as that of the depolarizing phase seen during fictive swimming, while that of the ascending drive occurred significantly later. Both ascending and descending drives were partially reduced in amplitude by Z-aminw5-phosphonovaleric acid or Mg2+. The blocking action of Mg2+ was, in both cases, voltage dependent. Cis-2,3-piperidine dicarboxylic acid or kynurenic acid caused a much greater reduction in the amplitude of the oscillations.These results suggest that a major part of the excitatory drive for swimming in lamprey motoneurons is generated by populations of propriospinal interneurons with relatively long descending and/or short ascending axons, which fire rhythmically during swimming and release an amino acid transmitter that excites motoneurons through N-methyl-o-aspartate (NMDA) and non-NMDA receptors. This information will allow these important neurons to be identified in future experiments.Rhythmic movements and locomotion in both vertebrates and invertebrates are believed to be controlled by networks of neurons capable of producing a motor output largely appropriate to control that behavior in the absence of sensory feedback (see

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Section: Possible Anatomical Substratementioning

confidence: 86%

Section: Resultsmentioning

confidence: 99%

Excitatory synaptic drive for swimming mediated by amino acid receptors in the lamprey

Dale¹

1986

J. Neurosci.

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“…The role of excitatory amino acids in the initiation of locomotion has been investigated previously in various vertebrate species such as the lamprey (Cohen and Wall&, 1980;Grillner et al, 1981), the tadpole (Dale and Roberts, 1984), and the mudpuppy (Wheatley et al, 1992(Wheatley et al, , 1994. In mammals, it was only quite recently that these substances were found to play a crucial role.…”

Section: Lumbar Spinal Cordmentioning

confidence: 99%

The synaptic drive from the spinal locomotor network to motoneurons in the newborn rat

1996

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The nature of the synaptic drive from the locomotor spinal network onto the motoneurons was studied in the newborn rat.For this purpose, an in vitro isolated spinal cord preparation of newborn rat was used. The recording chamber was partitioned with Vaseline walls to separate the Ll/L2 lumbar segments, in which the spinal locomotor network is located, from the motoneurons in the lower lumbar segments. Locomotor-like activity was induced by bath-applying a mixture of serotonin and NMDA to segments LllL2. In this way, the synaptic activity could be modified at the lower lumbar level without affecting the motor pattern. The drive elicited onto the motoneurons during sequences of locomotor-like activity, which was monitored by performing intracellular recordings, consisting of an inhibitory component followed by an excitatory component. The inhibitory synaptic volley was reversed at a membrane potential of -60 mV with K acetate electrodes, whereas it was shifted toward positive values with KCI electrodes. The glycinergic blocker strychnine, bath-applied to segments L3/L5, blocked the inhibitory drive without affecting the rhythmic activity, whereas it disrupted the locomotor-like activity when bathapplied to segments Ll/L2. The inhibitory part of the drive was more sensitive than the excitatory part to changes in the membrane potential. The excitatory phase was mixed and consisted of an NMDA and a non-NMDA component, which were sensitive to 2-amino-Sphosphonovaleric acid and 6-cyano-7-nitroquinoxaline-2,3-dione, respectively. It was concluded that the locomotor network located in segments Ll/L2 sends a biphasic projection to the various groups of motoneurons located along the lumbar spinal cord.Key words: electrophysiology; spinal cord; locomotion; motoneuron drive; glycine; excitatory amino acids During locomotor activity in mammals, the motoneurons are rhythmically depolarized and produce phasic bursts of action potentials which, in turn, elicit muscle contractions and limb movements. Schematically, two main components located at the lumbar spinal level can be described to take part in these motor rhythm generation processes: (1) the premotoneuronal locomotor spinal network, which is also called the central pattern generator (CPG); and (2) the motoneurons onto which all of the integrated information converges (Grillner, 1981). Although a considerable amount of data has been collected on the synaptic mechanisms responsible for this rhythmic behavior (for review, see Jordan, 1983Jordan, , 1991 Shefshick and Jordan, 1985;Perret, 1986;Roberts et al., 1986;Grillner and Matsushima, 1991), one question still remains regarding the relative contributions of these various elements, i.e., those of the premotoneuronal network on the one hand and the output motoneuronal compartment on the other hand. This gap in our knowledge has been attributable mainly to technical limitations that made it impossible to study these two elements separately. Using an in vitro isolated brainstemispinal cord preparation of newborn rat, we recent...

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“…The minor role of NMDA receptors in the generation of rhy-thmic respiratory drive in the neonatal rat contrasts with its proposed role in. other rhythmic motor systems such as locomotion in the neonatal rat (Smith, Feldman & Schmidt, 1988), lamprey (Grillner, McLellan, Sigvardt, Wallen & Willen, 1981), chick embryo (Barry & O'Donovan, 1987) and Xenopus embryos (Dale & Roberts, 1984). Indeed, due to the voltage-dependent properties of NMDA receptor-mediated currents, these receptors are hypothesized to have an important role in rhythmogenesis (Grillner, Wallen, Dale, Brodin, Buchanan & Hill, 1987).…”

Section: Involvement Of Excitatory Amino Acids In Respiratory Rhythmomentioning

confidence: 99%

Role of excitatory amino acids in the generation and transmission of respiratory drive in neonatal rat.

Greer

Smith

Feldman

1991

The Journal of Physiology

241

189

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SUMMARY1. The involvement of excitatory amino acids in the generation and transmission of rhythmic respiratory drive was studied in an in vitro neonatal rat brain stem-spinal cord preparation. The subclasses of excitatory amino acid receptors studied included: (i) N-methyl-D-aspartate (NMDA) receptors, (ii) (R, S)-o-amino-3-hydroxy-5-methylisoxazole-4-propionic acid hydrobromide (AMPA) and kainate (non-NMDA) receptors and (iii) 2-amino-4-phosphonobutyric acid (AP-4)-sensitive receptors. Respiratory motoneurone population discharge was recorded from glossopharyngeal (IX), vagus (X), and hypoglossal (XII) cranial nerves, as well as cervical (C1-C5) and thoracic (T2-T5) spinal ventral roots. This activity is generated in the motoneurone pools that transmit respiratory drive to upper airway, accessory, diaphragm and intercostal muscles. Perturbations of motor nerve discharge were analysed after excitatory amino acid receptor antagonists or agonists were added to bathing solutions surrounding either the spinal cord or brain stem. The excitatory amino acid receptor antagonists included: (i) NMDA receptor antagonist (+)-5-methyl-10,11-dihydro-5H-dibenzo [a,d] cyclohepten-5, 10-imin-H-maleate (MK-801) and (ii) non-NMDA receptor antagonist 6-cyano-7-nitroquinoxaline-2,3-dione (CNQX). The agonists included: (i) NMDA, (ii) non-NMDA receptor agonists AMPA and kainic acid. The effects of perturbations of AP-4-sensitive receptors with AP-4, and of inhibiting excitatory amino acid uptake with dihydrokainic acid (DHK) were also studied.2. Block of non-NMDA receptors in the medulla by CNQX resulted in an antagonist concentration-dependent decrease in the respiratory motoneuronal burst frequency. Non-NMDA receptor activation with kainic acid or AMPA caused a concentration-dependent increase in burst frequency, with competitive interactions with CNQX.3. Inhibition of excitatory amino acid uptake in the medulla with DHK resulted in a reversible, dose-dependent increase in respiratory frequency. A similar increase in respiratory frequency was induced by DHK when medullary NMDA receptors were blocked with MK-801, confirming that endogenously released excitatory amino acids act at non-NMDA receptors to modulate rhythm.4. Non-NMDA receptor block reduced and ultimately abolished the amplitude of MS 8563 J. J. GREER, J. C. SMITH AND J. L. FELDMAN integrated cranial and spinal respiratory motoneuronal discharge when added to the solution bathing the medulla and spinal cord, respectively. 5. NMDA receptor block in the medulla with MK-801 did not perturb the spontaneous respiratory burst frequency, although bath application of NMDA produced a dose-dependent increase in frequency, with non-competitive interactions with MK-801. MK-801 also did not perturb the amplitude of cranial or bulbospinal premotoneurone discharge. Block of NMDA receptors within the spinal cord caused a relatively small (10-30%) decrease in the amplitude of inspiratory motoneurone discharge.6. AP-4 applied to the medullary bathing solution did not affect respiratory r...

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Excitatory amino acid receptors in Xenopus embryo spinal cord and their role in the activation of swimming.

Cited by 136 publications

References 21 publications

Excitatory synaptic drive for swimming mediated by amino acid receptors in the lamprey

Excitatory synaptic drive for swimming mediated by amino acid receptors in the lamprey

The synaptic drive from the spinal locomotor network to motoneurons in the newborn rat

Role of excitatory amino acids in the generation and transmission of respiratory drive in neonatal rat.

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