Activation of NMDA‐receptors elicits “Fictive locomotion” in lamprey spinal cord in vitro

Grillner, Sten; McClellan, Andrew D.; Sigvardt, Karen A.; Wallén, Peter; Wilén, Maria

doi:10.1111/j.1748-1716.1981.tb06937.x

Cited by 203 publications

(89 citation statements)

References 11 publications

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“…1, 2 A) (Pérez et al, 2007). The swimming pattern frequency varied between 2 and 4 Hz, a typical range for 150 M NMDA (Grillner et al, 1981;. Under these conditions fMNs always showed a clear out-of-phase activity with the activity of the ipsilateral mMNs (Figs.…”

Section: Resultsmentioning

confidence: 99%

Neuronal Substrates for State-Dependent Changes in Coordination between Motoneuron Pools during Fictive Locomotion in the Lamprey Spinal Cord

Mentel

Cangiano²,

Grillner³

et al. 2008

J. Neurosci.

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Locomotion relies on a precisely timed activation of sets of motoneurons. A fundamental question is how this is achieved. In the lamprey, fin and myotomal motoneurons located on the same side of the spinal cord display alternating activity during straight swimming. The neural mechanism underlying this alternation is studied here during fictive locomotion induced by superfusion with NMDA, or locomotor bursting induced by electrical stimulation. If the spinal cord is split longitudinally, each hemicord still displays rhythmic locomotor related burst activity, but now fin and myotomal motoneurons become active in-phase. The out-of-phase activation of fin motoneurons persists only when at least three segments are left intact in the rostral part of the spinal cord. Proper coordination of fin motoneurons thus requires input from contralateral rostral segments. We show that commissural excitatory interneurons with long descending axons, previously reported to be active in phase with their ipsilateral myotomal motoneurons, provide monosynaptic excitation to contralateral fin motoneurons. Together, these results strongly indicate that, although myotomal motoneurons receive their phasic excitation from ipsilateral excitatory interneurons, fin motoneurons are mainly driven from the contralateral segmental network during bilateral locomotor activity. However, during unilateral bursting, fin and myotomal motoneurons instead receive a common input, which is apparently masked during normal fictive swimming. The spinal organization thus also provides circuitry for different patterns of coordination, i.e., alternation or coactivation of the two pools of motoneurons, which may subserve different forms of locomotor behavior.

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Section: Resultsmentioning

confidence: 99%

Neuronal Substrates for State-Dependent Changes in Coordination between Motoneuron Pools during Fictive Locomotion in the Lamprey Spinal Cord

Mentel

Cangiano²,

Grillner³

et al. 2008

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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“…This is particularly evident in the isolated spinal cord preparation where the spinal cord has been dissociated from the body and is kept alive in isolation in a bath. Under such conditions, the neuronal networks in the cord are still able to produce well-coordinated motor neuronal activity with most of the characteristics of intact swimming preserved (Grillner et al 1981a). To achieve such ¢ctive swimming, the cord can be activated by adding, for example, glutamate, to the bath.…”

Section: (B) Isolated Spinal Cord Preparationmentioning

confidence: 99%

Simulations of neuromuscular control in lamprey swimming

Ekeberg

Grillner

1999

Phil. Trans. R. Soc. Lond. B

121

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The neuronal generation of vertebrate locomotion has been extensively studied in the lamprey. Models at di¡erent levels of abstraction are being used to describe this system, from abstract nonlinear oscillators to interconnected model neurons comprising multiple compartments and a Hodgkin^Huxley representation of the most relevant ion channels. To study the role of sensory feedback by simulation, it eventually also becomes necessary to incorporate the mechanical movements in the models. By using simplifying models of muscle activation, body mechanics, counteracting water forces, and sensory feedback through stretch receptors and vestibular organs, we have been able to close the feedback loop to enable studies of the interaction between the neuronal and the mechanical systems. The neuromechanical simulations reveal that the currently known network is su¤cient for generating a whole repertoire of swimming patterns. Swimming at di¡erent speeds and with di¡erent wavelengths, together with the performance of lateral turns can all be achieved by simply varying the brainstem input. The neuronal mechanisms behind pitch and roll manoeuvres are less clear. We have put forward a`crossed-oscillators' hypothesis where partly separate dorsal and ventral circuits are postulated. Neuromechanical simulations of this system show that it is also capable of generating realistic pitch turns and rolls, and that vestibular signals can stabilize the posture during swimming.

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Activation of NMDA‐receptors elicits “Fictive locomotion” in lamprey spinal cord in vitro

Cited by 203 publications

References 11 publications

Neuronal Substrates for State-Dependent Changes in Coordination between Motoneuron Pools during Fictive Locomotion in the Lamprey Spinal Cord

Neuronal Substrates for State-Dependent Changes in Coordination between Motoneuron Pools during Fictive Locomotion in the Lamprey Spinal Cord

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

Simulations of neuromuscular control in lamprey swimming

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