Computer simulation of the segmental neural network generating locomotion in lamprey by using populations of network interneurons (original) (raw)
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Simulation of the segmental burst generating network for locomotion in lamprey
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.
Role of A-current in lamprey locomotor network neurons
Neurocomputing, 2003
A compartmental model of lamprey central pattern generator neurons was built in order to examine the e ects of a fast, transient, high-voltage-activated potassium current (A-current) found experimentally. The model consisted of a soma, a compartment corresponding to the axon initial segment, and a dendritic tree. The simulation showed that the A-current was necessary for repetitive spiking in the single neuron following current injection. The functional role of adding an A-current was also examined in a network model. In this model, the A-current stabilizes the swimming rhythm by making the burst cycle duration and the number of spikes per burst less variable. All these e ects are also seen experimentally.
The Activity of Spinal Commissural Interneurons During Fictive Locomotion in the Lamprey
Journal of Neurophysiology, 2008
Commissural interneurons in the lamprey coordinate activity of the hemisegmental oscillators to ensure proper left-right alternation during swimming. The activity of interneuronal axons at the ventral commissure was studied together with potential target motoneurons during fictive locomotion in the isolated lamprey spinal cord. To estimate the unperturbed activity of the interneurons, axonal recordings were chosen because soma recordings inevitably will affect the level of membrane depolarization and thereby spike initiation. Of 227 commissural axons recorded during locomotor activity, 14 produced inhibitory and 3 produced excitatory postsynaptic potentials (PSPs) in target motoneurons. The axons typically fired multiple spikes per locomotor cycle, with approximately 10 Hz sustained frequency. The average shortest spike interval in a burst corresponded to an instantaneous frequency of approximately 50 Hz for both the excitatory and inhibitory axons. The maximum number of spikes per locomotor cycle was inversely related to the locomotor frequency, in accordance with previous observations in the spinal hemicord preparation. In axons that fired multiple spikes per cycle, the mean interspike intervals were in the range in which the amplitude of the slow afterhyperpolarization (sAHP) is large, providing further support for the role of the sAHP in spike timing. One hundred ninety-five axons (86%) fired rhythmically during fictive locomotion, with preferred phase of firing distributed over either the segmental locomotor burst phase (40% of axons) or the transitional phase (between bursts; 60%). Thus in lamprey commissural interneurons, we found a broad distribution of firing rates and phases during fictive locomotion.
Modeling of the Spinal Neuronal Circuitry Underlying Locomotion in a Lower Vertebratea
Annals of the New York Academy of Sciences, 1998
The neural circuitry generating lamprey undulatory swimming is among the most accessible and best known of the vertebrate neuronal locomotor systems. It therefore serves as an experimental model for such systems. Modeling and computer simulation of this system was initiated at a point when a significant part of the network had been identified, although much detail was still lacking. The model has been further developed over 10 years in close interaction with experiments. The local burst generating circuitry is formed by ipsilateral excitatory neurons and crossed reciprocal inhibitory neurons. Early models also incorporated an off-switch lateral interneuron (L), the connectivity of which suggested it could contribute to burst termination at moderate to high bursting frequencies. Later examination of this model suggested, however, that the L interneuron was not of primary importance for burst termination, and this was later verified experimentally. Further, early models explained the effects of 5-HT on bursting frequency, spike frequency, and burst duration as being due to its modulatory action on the spike frequency adaptation of lamprey premotor interneurons. In current network models, accumulated adaptation is in addition the main burst terminating factor. Drive-related modulation of adaptation is explored as a mechanism for control of burst duration. This produces an adequate burst frequency range and a constant burst proportion within each cycle. It further allows for hemisegmental bursting, which has been observed experimentally. The local burst generator forms the basis of a network model of the distributed pattern generator that extends along the spinal cord. Phase constancy and flexibility of intersegmental coordination has been studied in such a simulated network. Current modeling work focuses on neuromodulator circuitry and action, network responses to input transients, how to model the intact versus an isolated piece of spinal cord, as well as on improving an earlier neuromechanical model of lamprey swimming.
Ion channels of importance for the locomotor pattern generation in the lamprey brainstem-spinal cord
The Journal of Physiology, 2001
The intrinsic function of the spinal network that generates locomotion can be studied in the isolated brainstem-spinal cord of the lamprey, a lower vertebrate. The motor pattern underlying locomotion can be elicited in the isolated spinal cord. The network consists of excitatory glutamatergic and inhibitory glycinergic interneurones with known connectivity. The current review addresses the different subtypes of ion channels that are present in the cell types that constitute the network. In particular the roles of the different subtypes of Ca2+ channels and potassium channels that regulate integrated neuronal functions, like frequency regulation, spike frequency adaptation and properties that are important for generating features of the motor pattern (e.g. burst termination), are reviewed. By knowing the role of an ion channel at the cellular level, we also, based on previous knowledge of network connectivity, can understand which effect a given ion channel may exert at the different levels from molecule and cell to network and behaviour.
Roles of Ionic Currents in Lamprey CPG Neurons: A Modeling Study
Journal of Neurophysiology, 2007
The spinal network underlying locomotion in the lamprey consists of a core network of glutamatergic and glycinergic interneurons, previously studied experimentally and through mathematical modeling. We present a new and more detailed computational model of lamprey locomotor network neurons, based primarily on detailed electrophysiological measurements and incorporating new experimental findings. The model uses a Hodgkin–Huxley-like formalism and consists of 86 membrane compartments containing 12 types of ion currents. One of the goals was to introduce a fast, transient potassium current (Kt) and two sodium-dependent potassium currents, one faster (KNaF) and one slower (KNaS), in the model. Not only has the model lent support to the interpretation of experimental results but it has also provided predictions for further experimental analysis of single-network neurons. For example, Kt was shown to be one critical factor for controlling action potential duration. In addition, the model ...
Fast and Slow Locomotor Burst Generation in the Hemispinal Cord of the Lamprey
Journal of Neurophysiology, 2003
A fundamental question in vertebrate locomotion is whether distinct spinal networks exist that are capable of generating rhythmic output for each group of muscle synergists. In many vertebrates including the lamprey, it has been claimed that burst activity depends on reciprocal inhibition between antagonists. This question was addressed in the isolated lamprey spinal cord in which the left and right sides of each myotome display rhythmic alternating activity. We sectioned the spinal cord along the midline and tested whether rhythmic motor activity could be induced in the hemicord with bath-applied d-glutamate or N-methyl-d-aspartate (NMDA) as in the intact spinal cord or by brief trains of electrical stimuli. Fast rhythmic bursting (2–12 Hz), coordinated across ventral roots, was observed with all three methods. Furthermore, to diminish gradually the crossed glycinergic inhibition, a progressive surgical lesioning of axons crossing the midline was implemented. This resulted in a gra...
Biological Cybernetics, 1998
The neuronal network underlying lamprey swimming has stimulated extensive modelling on different levels of abstraction. The lamprey swims with a burst frequency ranging from 0.3 to 8-10 Hz with a rostrocaudal lag between bursts in each segment along the spinal cord. The swimming motor pattern is characterized by a burst proportion that is independent of burst frequency and lasts around 30%-40% of the cycle duration. This also applies in preparations in which the reciprocal inhibition in the spinal cord between the left and right side is blocked. A network of coupled excitatory neurons producing hemisegmental oscillations may form the basis of the lamprey central pattern generator (CPG). Here we explored how such networks, in principle, could produce a large frequency range with a constant burst proportion. The computer simulations of the lamprey CPG use simplified, graded output units that could represent populations of neurons and that exhibit adaptation. We investigated the effect of an active modulation of the degree of adaptation of the CPG units to accomplish a constant burst proportion over the whole frequency range when, in addition, each hemisegment is assumed to be self-oscillatory. The degree of adaptation is increased with the degree of stimulation of the network. This will make the bursts terminate earlier at higher burst rates, allowing for a constant burst proportion. Without modulated adaptation the network operates in a limited range of swimming frequencies due to a progressive increase of burst duration with increasing background stimulation. By introducing a modulation of the adaptation, a broad burst frequency range can be produced. The reciprocal inhibition is thus not the primary burst terminating factor, as in many CPG models, and it is mainly responsible for producing alternation between the left and right sides. The results are compared with the Morris-Lecar oscillator model with parameters set to produce a type A and type B oscillator, in which the burst durations stay constant or increase, respectively, when the background stimulation is increased. Here as well, burst duration can be controlled by modulation of the slow variable in a similar way as above. When oscillatory hemisegmental networks are coupled together in a chain a phase lag is produced. The production of a phase lag in chains of such oscillators is compared with chains of Morris-Lecar relaxation oscillators. Models relating to the intact versus isolated spinal cord preparation are discussed, as well as the role of descending inhibition.
Journal of computational neuroscience, 1998
It is crucial to determine the effects on the network level of a modulation of intrinsic membrane properties. The role calcium-dependent potassium channels, KCa, in the lamprey locomotor system has been investigated extensively. Earlier experimental studies have shown that apamin, which affects one type of KCa, increases the cycle duration of the locomotor network, due to effects on the burst termination. The effects of apamin were here larger when the network had a low level of activity (burst frequency 0.5 to 1 Hz) as compared to a higher rate (> 2 Hz). By using a previously developed simulation model based on the lamprey locomotor network, we show that the model could account for the frequency dependence of the apamin modulation, if only the KCa conductance activated by Ca2+ entering during the action potential was altered and not the KCa conductance activated by Ca2+ entering through NMDA channels. The present simulation model of the spinal network in the lamprey can thus acc...
Low-voltage-activated calcium channels in the lamprey locomotor network: simulation and experiment
Journal of neurophysiology, 1997
To evaluate the role of low-voltage-activated (LVA) calcium channels in the lamprey spinal locomotor network, a previous computer simulation model has been extended to include LVA calcium channels. It is also of interest to explore the consequences of a LVA conductance for the electrical behavior of the single neuron. The LVA calcium channel was modeled with voltage-dependent activation and inactivation using the m3h form, following a Hodgkin-Huxley paradigm. Experimental data from lamprey neurons was used to provide parameter values of the single cell model. The presence of a LVA calcium conductance in the model could account for the occurrence of a rebound depolarization in the simulation model. The influence of holding potential on the occurrence of a rebound as well the latency at which it is elicited was investigated and compared with previous experiments. The probability of a rebound increased at a more depolarized holding potential and the latency was also reduced under these...