ReviewNeural bases of goal-directed locomotion in vertebrates—An overview
Introduction
In this brief report, we will provide an overview of the different components of the control systems involved in generating goal-directed locomotion in vertebrates. It is written from a general vertebrate perspective, but will provide more detailed examples from the lamprey system. Fig. 1 summarizes the different subsystems that need to be considered and that will be discussed below. The motor pattern itself is generated at the spinal level by central pattern generator networks (CPGs). The CPGs are modulated by movement-related sensory feedback that can adapt the movements to unexpected perturbations (Grillner et al., 1981, Grillner, 1981, Grillner, 1985, Grillner, 2003, Rossignol et al., 2006). The level of activity is determined from the brainstem locomotor command systems (see Orlovsky et al., 1999). The basal ganglia plays a critical role for determining which motor program should be active at a given instant. At rest the different motor programs in the brainstem are subject to a powerful tonic inhibition (Grillner et al., 2005a, Hikosaka, 2007). It is only when for instance the MLR is disinhibited that locomotion will be initiated (see Grillner, 2006, Ménard et al., 2007).
In addition to regulating the level of locomotor activity, a number of other control systems must operate to achieve behaviourally meaningful locomotor movements (see Fig. 1). The movements must be steered towards different targets of interest for the individual, whether fish or primate. Steering commands need to be issued. The optic tectum/superior colliculus plays an important role in this context and the commands are mediated via reticulospinal pathways to the spinal cord (Fagerstedt et al., 2001, Saitoh et al., 2007). The individual must also be able to maintain the body orientation whether swimming, walking or flying. The postural control systems therefore play a critical role. Vestibular receptors provide information about the orientation and movements of the head and sensory input from the limbs and trunk provide important complementary information (Deliagina et al., 2006, Deliagina and Orlovsky, 2002).
We will start from the CPG level in Fig. 1 and work our way upwards to the more complex processes underlying the selection of different motor programs, to finally return to the lamprey CPG and whether an understanding of this circuitry can provide an insight into the mammalian CPGs for limb motor control.
Section snippets
The brainstem–spinal cord locomotor synergy
In all vertebrates, networks coordinating the basic propulsive movement synergy are located at the spinal level, whether in fish swimming, bird flight or mammalian locomotion. These networks, usually referred to as CPGs, are responsible for the sequential activation of the different motoneuron/muscle groups taking part in the movement (Grillner et al., 1981, Grillner, 1981, Grillner, 1985, Grillner, 2003, Rossignol et al., 2006). Below follows a brief account of the intrinsic function of these
Integration of posture and locomotion—a requirement for all vertebrates
All vertebrates control their body orientation during locomotion mostly with the dorsal side up except for bipeds like humans. For swimming animals, like the lamprey, the main bases for the control is input from the gravistatic receptors in the vestibular system. These receptors sense any deviation from the normal dorsal side up position (Deliagina and Orlovsky, 2002). In this “desired” position, the vestibular afferents on the two sides have approximately equal and relatively low discharge
The basic machinery underlying steering of locomotor movements
Whereas the propulsive machinery provides the basis for forward movements, a steering control needs to be added to enable the animal to reach different points in the environment. Again the situation in water-living animals, like the lamprey, is relatively simple. The steering commands can be studied in both intact and reduced preparations (Fagerstedt et al., 2001, Kozlov et al., 2002). Swimming movements can be elicited in the lamprey–brainstem spinal cord semi-intact preparations. Under the
Goal-directed aspects of locomotion—mammalian perspective
So far we have described the neural mechanism underlying propulsion, control of body orientation and steering with regard purely to the neural control mechanisms used. In order for these different motor programs to be useful in a behavioural context, they need to be adapted to the environment, which requires a more complex form of sensory–motor integration. The forebrain is required for adaptive movements to occur, in particular the basal ganglia and related structures. It is noteworthy that
Forebrain control of movement—the lamprey model
Recent studies have aimed at elucidating the neural structures rostral to the lower brainstem–spinal cord in the lamprey, which has been reviewed extensively before (Grillner, 2003), in the context of motor control. These studies have involved the control of eye, orientation and locomotor movements and also the postural adjustments adapted to different patterns of behaviour like the dorsal light response (Saitoh et al., 2007, Robertson et al., 2006, Robertson et al., 2007).
One important aspect
From the lamprey CPG to the mammalian CPG
Now let us return to where we started, the CPG level, and ask ourselves if the knowledge from the well-studied lamprey CPG can provide insights into the operation of the mammalian more complex CPG. The main players in the lamprey segmental burst-generating network are the excitatory glutamatergic premotor interneurons (EINs) that activate motoneurons via both NMDA and AMPA receptors. EINs form a pool within each segment and excite each other, and provide the burst generating kernel (Buchanan
In conclusion
We have provided a brief survey of the neural control of goal-directed locomotion in vertebrates, and the different control systems required to generate this complex aspect of the mammalian motor repertoire. Detailed accounts of the many different aspects of these control systems will be presented in the different chapters of this volume.
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