ReviewCellular bases of a vertebrate locomotor system – steering, intersegmental and segmental co-ordination and sensory control
Introduction
Locomotion in vertebrates depends upon several neural systems that control propulsion, maintenance of body orientation (equilibrium or postural control), steering (goal-direction control) and, for tetrapods, the positioning of feet accurately on the ground in each step. Since the mammalian nervous system is comparatively complex and difficult to analyse, it has been important to develop experimental models in which the cellular bases of motor behaviour can be addressed. This is necessary if we are to understand the intrinsic operation of these networks that is how the collective contribution of ion channels, cells and synapses contribute to the generation of accurate and reproducible movements. Some models like the frog embryo and the lamprey have been very useful in this context [27], [53], [66], and others generating walking (mudpuppy, turtle, neonatal rodents) promise to yield important information [46], [47], [54], [65], [70]. The organisation of these neural control systems in the brainstem–spinal cord is similar in all vertebrates [26]. In this paper we will review some aspects of the control systems underlying propulsion and steering in the lamprey. The lamprey has all the basic features of the vertebrate central nervous system, but much fewer neurons than mammals, and is therefore an attractive model system.
The isolated lamprey brainstem–spinal cord (Fig. 1) can be maintained in vitro for several days. The motor pattern underlying locomotion can be elicited through stimulation of the brainstem locomotor areas in the di- or mesencephalon [18], [52], [63] corresponding to the locomotor areas in mammals (see [29], [31]). In the isolated spinal cord, locomotor activity can be elicited by pharmacological activation of different ionotropic glutamate receptors [1], [13], [35], cf. Ref. [59]. The motor activity can be monitored by ventral root recordings, while intracellular recordings are performed from different neurones (Fig. 1). This latter preparation has been used extensively to investigate the organisation of the locomotor pattern generating network that is responsible for the segmental and intersegmental co-ordination underlying locomotion (for review see Ref. [28]).
In this paper we will briefly describe the intrinsic operation of the spinal network, which has been reviewed repeatedly from different aspects [28], [30], [38], [39], [58], followed by a more detailed account of the intersegmental co-ordination, steering and the role of different types of sensory feedback during locomotion. The experimental results and conclusions will be reviewed, and compared with mathematical modelling of the same processes.
Section snippets
Overview of segmental motor mechanisms — biology and mathematical modelling
Fig. 2 shows the spinal pattern generating network and the supraspinal circuitry involved in initiation and maintenance of locomotor activity, as established through a detailed analysis of the connectivity with paired recordings in a number of studies (e.g. Refs. [6], [18], [56], [75]).
At the segmental level burst activity can be elicited by merely elevating the excitability of the network, as with administration of NMDA or d-glutamate. The network is comprised of excitatory interneurones (Fig.
Intersegmental co-ordination—biology and mathematical modelling
Swimming fish and amphibians display to a varying degree a mechanical wave propagated from head to tail with increasing amplitude as they swim. This propagated wave pushes the animal forward through the water. It is produced by a consecutive activation of segments along the body. The time lag between segments is variable, but remains always a fixed proportion of the cycle duration, whether it is 10 s or 0.1 s [25], [32]. This lag is referred to as a constant phase lag. In the lamprey it is
Simulated ‘intersegmental’ network without segmental boundaries
The spinal cord is segmentally organised with regard to ventral and dorsal roots. Within the spinal cord there are, however, no apparent traces of a segmental borders. The motoneurones are for instance organised as a column of cells, and there is no apparent shift at the transition at which the axons of the motoneurones are sent to a rostrally rather than a caudally located ventral root. The overall projections to the caudal or rostral ventral root may even overlap in the transitional zone [73].
Steering—biology and modelling
Locomotor activity is initiated from the mesopontine (MLR) and diencephalic locomotor regions in ventral thalamus through a symmetrical activation of reticulospinal (RS) neurones on both sides, particularly in the middle (mrrn) and posterior (prrn) rhombencephalic nuclei. They activate in turn the network interneurones and motoneurones along the spinal cord [56], [79].
The same RS neurones are often used in several different functional contexts, like locomotion and the control of body
Movement related feedback has powerful effects on the CPG
The isolated spinal cord–notochord in the lamprey displays rhythmic burst activity at ‘rest’ (Fig. 6A; fictive locomotion induced by pharmacological activation of glutamate receptors). If the caudal part of the notochord–spinal cord is moved rhythmically back and forth as in swimming at the same rate as the burst activity, or at a rate somewhat above or below the rest burst rate (Fig. 6A), the burst activity becomes entrained [24]. Clearly the sensory input produced by the movement is
Role of sensory feedback during locomotion
We have also used the neuro–mechanical model discussed above (Fig. 4C) to explore the role of the sensory feedback during ordinary swimming and perturbations (Fig. 8B). During ordinary swimming there is no apparent difference in the movement pattern with and without sensory feedback organised as described above. When, however, a perturbation is introduced, the situation becomes different. The shaded area in Fig. 8B1 and B2 indicates a region in which the water current is simulated to flow
Synaptic input to SR neurones during locomotion
During mammalian locomotion stretch receptors like the muscle spindles receive an additional drive through γ-motoneurones in parallel with the excitation to α-motoneurones in the same muscle [64]. This α–γ linkage, which is common, serves to compensate for the muscle shortening such that the spindle (stretch receptor) remains sensitive to perturbations during the different parts of the movement cycle.
Since the lamprey stretch receptor neurones also will go through phases of loading and
Central and sensory control of fin motoneurones
The thin dorsal fins increase the lateral resistance to sideways movements of the trunk during locomotion. When the myotomes on one side are contracting, the body moves laterally in the opposite direction (Fig. 10A), while the fins will be deviated towards the other side. To maintain an upright fin position, fin motor units on the side opposite to the myotomal motoneurones must be activated. This provides the explanation for the finding that fin motoneurones are activated in antiphase (180°) to
Concluding remarks
The neural control of locomotion in this lower vertebrate nervous system is understood not only on the network level, but also with regard to the intrinsic function of these brainstem–spinal cord networks. We can thus understand how a modulation of a given ion channel affects the overall behaviour of a given cell in the network and correspondingly how this modification influences the network activity and thereby behaviour. We can thus bridge the gap from the molecular level (or genes) to
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2015, Current Opinion in NeurobiologyCitation Excerpt :In many animals, rhythmic movements depend on coordinated action of muscle groups in many body segments. Classical work on leech swimming [73], leech heartbeat [74], and lamprey swimming [75] was critical in posing questions of how appropriate movement could be generated by coupling of many segmental oscillators. New work seeks to understand peristaltic wave propagation in crawling Drosophila larvae [76•], C. elegans [77] and in the crayfish swimmeret system [78•,79•], and further addresses the impact of parameter variability on segmental coordination [39•].