Simulation of the segmental burst generating network for locomotion in lamprey

doi:10.1016/0304-3940(88)90476-4

Neuroscience Letters

Volume 89, Issue 1, 17 June 1988, Pages 31-35

https://doi.org/10.1016/0304-3940(88)90476-4 Get rights and content

Abstract

Recently a segmental network of inhibitory and excitatory interneurones, which are active during locomotion, has been described in the lamprey, a lower vertebrate. The interactions between the different neurones were established by paired intracellular recordings. A computer simulation of the segmental network has been performed, which shows that with the established neuronal connectivity rhythmic alternating burst activity can be generated within the upper part of the normal physiological range of locomotion. Three neurones of each kind were used (altogether 18 neurones). As shown previously the lower frequency range used in locomotion most likely depends on an activation of voltage-dependent $N- methyl- d -aspartate$ (NMDA) receptors, which could, however, not be simulated with the present neuronal models.

References (19)

L. Brodin et al.
The role of putative excitatory amino acid neurotransmitters in the initiation of locomotion in the lamprey spinal cord. I. The effects of excitatory amino acid antagonists
Brain Res.
(1985)
L. Brodin et al.
Effects of magnesium on fictive locomotion induced by activation of $N- methyl- d -aspartate$ (NMDA) receptors in the lamprey spinal cord in vitro
Brain Res.
(1986)
L. Brodin et al.
NMDA, kainate and quisqualate receptors and the generation of fictive locomotion in the lamprey spinal cord
Brain Res.
(1985)
J.T. Buchanan
Identification of interneurons with contralateral, caudal axons in the lamprey spinal cord: synaptic interactions and morphology
J. Neurophysiol.
(1982)
J.T. Buchanan et al.
Activities of identified interneurons, motoneurons, and muscle fibres during fictive swimming in the lamprey and effects of reticulospinal and dorsal cell stimulation
J. Neurophysiol.
(1982)
J.T. Buchanan et al.
Newly identified ‘glutamate interneurons’ and their role in locomotion in the lamprey spinal cord
Science
(1987)
A.H. Cohen et al.
The neuronal correlate of locomotion in fish
‘Fictive swimming’ induced in an in vitro preparation of the lamprey spinal cord
Exp. Brain Res.
(1980)
N. Dale
Excitatory synaptic drive for swimming mediated by amino acid receptors in the lamprey
J. Neurosci.
(1986)
S. Grillner
Neurobiological bases of the rhythmic motor acts in vertebrates
Science
(1985)

There are more references available in the full text version of this article.

Cited by (53)

The mammalian central pattern generator for locomotion
2009, Brain Research Reviews
At the beginning of the 20th century, Thomas Graham Brown conducted experiments that after a long hiatus changed views on the neural control of locomotion. His seminal work supported by subsequent evidence generated largely from the 1960s onwards showed that across species walking, flying, and swimming are controlled largely by a neuronal network that has been referred to as the central pattern generator (CPG) for locomotion. In mammals, this caudally localized spinal cord network was found to generate the basic command signals sent to muscles of the limbs for locomotor rhythm and pattern generation. This article constitutes a comprehensive review summarizing key findings on the organization and properties of this network.
The developmental and functional logic of neuronal circuits: Commentary on the Kavli prize in neuroscience
2009, Neuroscience
The first Kavli Prize in Neuroscience recognizes a confluence of career achievements that together provide a fundamental understanding of how brain and spinal cord circuits are assembled during development and function in the adult. The members of the Kavli Neuroscience Prize Committee have decided to reward three scientists (Sten Grillner, Thomas Jessell, and Pasko Rakic) jointly “for discoveries on the developmental and functional logic of neuronal circuits”.
Pasko Rakic performed groundbreaking studies of the developing cerebral cortex, including the discovery of how radial glia guide the neuronal migration that establishes cortical layers and for the radial unit hypothesis and its implications for cortical connectivity and evolution.
Thomas Jessell discovered molecular principles governing the specification and patterning of different neuron types and the development of their synaptic interconnection into sensorimotor circuits.
Sten Grillner elucidated principles of network organization in the vertebrate locomotor central pattern generator, along with its command systems and sensory and higher order control.
The discoveries of Rakic, Jessell and Grillner provide a framework for how neurons obtain their identities and ultimate locations, establish appropriate connections with each other, and how the resultant neuronal networks operate. Their work has significantly advanced our understanding of brain development and function and created new opportunities for the treatment of neurological disorders. Each has pioneered an important area of neuroscience research and left a legacy of exceptional scientific achievement, insight, communication, mentoring and leadership.
Locomotor network modeling based on identified zebrafish neurons
2006, Neurocomputing
The larval zebrafish generates a discrete set of locomotor maneuvers, each with distinctive bending patterns and tail-beat frequencies (TBFs). It is not known how these locomotor patterns are generated. We had previously shown that aspects of the locomotor repertoire could be modeled with a simple 2-cell segmental oscillator replicated in series to simulate the 30 segment larval spinal cord. This model, however, conflicted with known features of the spinal circuitry and was not able to produce the natural whole-cord activity patterns. We present here three new more realistic CPG models which incorporate anatomical and neurotransmitter features of identified zebrafish spinal interneurons. These whole-cord models were able to produce oscillatory rhythms across the range of natural TBFs in ways that the simpler model could not.
Contributions of identifiable neurons and neuron classes to lamprey vertebrate neurobiology
2001, Progress in Neurobiology
Among the advantages offered by the lamprey brainstem and spinal cord for studies of the structure and function of the nervous system is the unique identifiability of several pairs of reticulospinal neurons in the brainstem. These neurons have been exploited in investigations of the patterns of sensory input to these cells and the patterns of their outputs to spinal neurons, but no doubt these cells could be used much more effectively in exploring their roles in descending control of the spinal cord. The variability of cell positions of neurons in the spinal cord has precluded the recognition of unique spinal neurons. However, classes of nerve cells can be readily defined and characterized within the lamprey spinal cord and this has led to progress in understanding the cellular and synaptic mechanisms of locomotor activity. In addition, both the identifiable reticulospinal cells and the various spinal nerve cell classes and their known synaptic interactions have been used to demonstrate the degree and specificity of regeneration within the lamprey nervous system. The lack of uniquely identifiable cells within the lamprey spinal cord has hampered progress in these areas, especially in gaining a full understanding of the locomotor network and how neuromodulation of the network is accomplished.
The intrinsic function of a motor system - From ion channels to networks and behavior
2000, Brain Research
Citation Excerpt :
Since we have a relatively detailed knowledge of how the network functions, the network effects of a modulator can (to some extent) be predicted from its different cellular actions. Extensive biologically relevant mathematical models of the locomotor network have also been developed, based on knowledge of the properties and synaptic connectivity of nerve cells in the network [34,41,68]. In these simulations, known specific modulator-mediated effects on the cellular level can be induced to investigate how these different effects contribute to the overall change in the network output.
The forebrain, brainstem and spinal cord contribution to the control of locomotion is reviewed in this article. The lamprey is used as an experimental model since it allows a detailed cellular analysis of the neuronal network underlying locomotion. The focus is on cellular mechanisms that are important for the pattern generation, as well as different types of pre- and postsynaptic modulation. This experimental model is bridging the gap between the molecular and cellular level to the network and behavioral level.
GABA<inf>B</inf>-ergic modulation of burst rate and intersegmental coordination in lamprey: Experiments and simulations
2000, Brain Research
Citation Excerpt :
This can be studied using the lamprey spinal locomotor network [7–9,16,33,42]. The basic segmental network consists of reciprocally connected inhibitory glycinergic interneurons (C-neurons), and glutamatergic excitatory interneurons (E-neurons) which provide alternating glutamatergic excitation and glycinergic inhibition of the interneurons [8,15,20]. By adding excitatory amino acids to the isolated spinal cord an alternating rhythmic bursting activity can be evoked [5,11,17].
Neuromodulators which influence the operation of neural networks act as a rule via several cellular and synaptic mechanisms. Activation of GABA_B-receptors in the lamprey spinal cord reduce both calcium currents and the peak amplitude of the post-spike afterhyperpolarization (AHP). Activation of GABA_B-receptors reduce the segmental alternation rate and modifies the intersegmental coordination when the spinal locomotor circuits are activated by NMDA. Using physiological experiments we find that a reduced AHP is not sufficient to account for the observed reduction of the burst rate. Computer simulations revealed that either a reduced AHP or calcium current could alter the phase coordination between the segments similar to earlier experiments.

View all citing articles on Scopus

View full text

Simulation of the segmental burst generating network for locomotion in lamprey

Abstract

The role of putative excitatory amino acid neurotransmitters in the initiation of locomotion in the lamprey spinal cord. I. The effects of excitatory amino acid antagonists

Brain Res.

Effects of magnesium on fictive locomotion induced by activation of N-methyl-d-aspartate (NMDA) receptors in the lamprey spinal cord in vitro

Brain Res.

NMDA, kainate and quisqualate receptors and the generation of fictive locomotion in the lamprey spinal cord

Brain Res.

Identification of interneurons with contralateral, caudal axons in the lamprey spinal cord: synaptic interactions and morphology

J. Neurophysiol.

Activities of identified interneurons, motoneurons, and muscle fibres during fictive swimming in the lamprey and effects of reticulospinal and dorsal cell stimulation

J. Neurophysiol.

Newly identified ‘glutamate interneurons’ and their role in locomotion in the lamprey spinal cord

Science

The neuronal correlate of locomotion in fish

‘Fictive swimming’ induced in an in vitro preparation of the lamprey spinal cord

Exp. Brain Res.

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

J. Neurosci.

Neurobiological bases of the rhythmic motor acts in vertebrates

Science

Effects of magnesium on fictive locomotion induced by activation of $N- methyl- d -aspartate$ (NMDA) receptors in the lamprey spinal cord in vitro