Neural bases of goal-directed locomotion in vertebrates—An overview

Abstract

The different neural control systems involved in goal-directed vertebrate locomotion are reviewed. They include not only the central pattern generator networks in the spinal cord that generate the basic locomotor synergy and the brainstem command systems for locomotion but also the control systems for steering and control of body orientation (posture) and finally the neural structures responsible for determining which motor programs should be turned on in a given instant. The role of the basal ganglia is considered in this context. The review summarizes the available information from a general vertebrate perspective, but specific examples are often derived from the lamprey, which provides the most detailed information when considering cellular and network perspectives.

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.