Modeling a vertebrate motor system: pattern generation, steering and control of body orientation
Introduction
In order to gain insight into the cellular bases of vertebrate motor behavior, different experimental models are required depending on the type of process explored. For fine control of hand movements, primate models may be a first choice, but for the neural control of goal-directed locomotion or control of body orientation simpler vertebrate models may instead be a better alternative. In this chapter, we will review the extensive knowledge gained on the lamprey nervous system through an interactive process between experiments and modeling (see Grillner, 2003, Grillner, 2006). The organization of the locomotor system is to a large extent conserved through vertebrate phylogeny, and it is therefore also pertinent to explore to what an extent this knowledge can be applied to the more complex mammalian nervous system.
We will focus on the modeling of the different components of the neural systems underlying goal-directed locomotion, while referring to the detailed experimental evidence. The overall aim is to account for this complex set of behaviors, based on an understanding of the intrinsic cellular mechanisms determining the operation of the different neuronal networks.
The different subsystems involved in the control of locomotion can be represented as follows (see Fig. 1):
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A neural system responsible for selection of the appropriate behavior, in this case locomotion. The striatum, the input layer of the basal ganglia, has an important role in this context. The striatum receives phasic input from pallium (cortex) and thalamus, and a modulatory input from the dopamine system. The GABAergic striatal neurons have a high threshold for activation. When activated they can indirectly release specific motor programs by inhibiting the GABAergic output neurons of the basal ganglia (pallidum) that at rest provide tonic inhibition of the different motor programs (see Grillner, 2006).
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A command system that, when released from basal ganglia inhibition, can elicit locomotion by activating the pattern-generating circuits in the spinal cord. Two command systems for locomotion, the mesencephalic (MLR) and the diencephalic (DLR) have been defined. They act via a symmetric activation of reticulospinal neurons that turn on the spinal circuits.
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Segmental and intersegmental networks [central pattern generators (CPGs)] located at the spinal level. The CPGs contain the necessary timing information to activate the different motoneurons (MNs) in the appropriate sequence to produce the propulsive movements.
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The segmental burst-generating network in the lamprey contains excitatory interneurons (EINs) that provide excitation within the pool of interneurons. The alternating pattern between the left and the right sides is provided by reciprocal inhibitory connections between pools of EINs.
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A sensory control system, sensing the locomotor movements, helps to compensate for external perturbations by a feedback action on the spinal CPGs.
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A control system for steering the body toward different goals. The steering commands are superimposed on the basic locomotor activity and will bias the control signals, so as to steer the movements to the left or right side or in other orientations.
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During locomotion the body moves with the dorsal side up, regardless of perturbations. This “postural” control system, for orientation of the body in the gravity field, depends on bilateral vestibular input that detects any deviation from the appropriate orientation of the head, whether tilt to the left or right or changes in pitch angle during locomotion. These vestibular effects are mediated via brainstem interneurons to reticulospinal neurons on the left or right side, respectively, that can elicit compensatory movements that restore the body orientation.
Section snippets
Basic mechanisms of burst generation
One major problem when studying vertebrate pattern generation has been the intrinsic function of the networks controlling behaviors such as respiration and locomotion. In the case of lower vertebrates like the lamprey and the frog embryo, they are comparatively well understood. At the segmental level recurring locomotor bursts can be generated even in a hemisegment, provided that the excitability is high enough (Cangiano and Grillner, 2003, Cangiano and Grillner, 2005). The burst generation is
Intersegmental network
The lamprey normally swims by using an undulatory wave propagated from head to tail (Fig. 4A), the faster the wave is propagated backward along the body, the faster the animal will move forward through the water (Grillner, 1974; Wallen and Williams, 1984; Williams et al., 1989). The delay between the activation of each segment is around 1% of the cycle duration regardless of whether the cycle duration is 2 s or one tenth of a second. Since the lamprey has around 100 segments, this means that the
Steering
What we have modeled so far is the neural bases of symmetric locomotor movements. To make them behaviorally meaningful, we need in addition to steer them. Steering movements to the left or right side are achieved through an asymmetric activation of reticulospinal neurons on the left and the right sides particularly involving the middle and posterior rhombencephalic reticular nuclei (Ohta and Grillner, 1989; Wannier et al., 1998; Deliagina et al., 2000, Deliagina et al., 2002; Fig. 8A). This
Control of body orientation
During locomotion the lamprey corrects its body position instantaneously so that the dorsal side is always directed upward. The vestibular organs on the left and the right sides sense any deviation in terms of lateral tilt of the head. The vestibular input is mediated via interneurons to the reticulospinal neurons in the rhombencephalon (Fig. 9), so that a tilt to the left leads to an enhanced activity of reticulospinal neurons on the right side of the brainstem, which elicits a correction of
Sensory feedback helps compensate for perturbations
The spinal CPG can generate the motor pattern underlying locomotion without sensory feedback as shown with the neuromechanical lamprey model in Fig. 10A (Grillner et al., 1976; Ekeberg and Grillner, 1999; Grillner, 2003). Although the CPG operates without sensory feedback, stretch receptors on the lateral margin of the spinal cord (Grillner et al., 1984) sense the locomotor movements, and have a direct synaptic link to the CPG interneurons (Viana Di Prisco et al., 1990;Fig. 10C). They provide
Concluding remarks
In this brief review we have aimed at summarizing the experimentally based modeling of the neural control system for goal-directed locomotion and control of body orientation in the lamprey. Due to the relative simplicity of the lamprey nervous system, it has been possible to address the general principles of the neuronal mechanisms underlying goal-directed motor control. From these, it is possible to infer the control mechanisms underlying goal-directed behavior in more complex vertebrates.
Acknowledgments
We hereby acknowledge the support of the European commission (Neurobotics, PD, SG), The Swedish Research Council (SG, JHK, AL) and The Wallenberg Foundations.
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