Towards Effective Non-Invasive Brain-Computer Interfaces Dedicated to Gait Rehabilitation Systems
In the last few years, significant progress has been made in the field of walk rehabilitation. Motor cortex signals in bipedal monkeys have been interpreted to predict walk kinematics. Epidural electrical stimulation in rats and in one young paraplegic has been realized to partially restore motor control after spinal cord injury. However, these experimental trials are far from being applicable to all patients suffering from motor impairments. Therefore, it is thought that more simple
... ion systems are desirable in the meanwhile. The goal of this review is to describe and summarize the progress made in the development of non-invasive brain-computer interfaces dedicated to motor rehabilitation systems. In the first part, the main principles of human locomotion control are presented. The paper then focuses on the mechanisms of supra-spinal centers active during gait, including results from electroencephalography, functional brain imaging technologies [near-infrared spectroscopy (NIRS), functional magnetic resonance imaging (fMRI), positron-emission tomography (PET), single-photon emission-computed tomography (SPECT)] and invasive studies. The first brain-computer interface (BCI) applications to gait rehabilitation are then presented, with a discussion about the different strategies developed in the field. The challenges to raise for future systems are identified and discussed. Finally, we present some proposals to address these challenges, in order to contribute to the improvement of BCI for gait rehabilitation. Brain Sci. 2014, 4 2 Keywords: brain-computer interface; brain dynamics; brain imaging; electroencephalography; rehabilitation; supra-spinal control of locomotion; walk Production of the Basic Locomotor Patterns: Arguments in Favor of a Human CPG Network The rhythmic movements of the legs during stepping require a complex sequence of muscle contractions to be executed by the lower limbs. The timing and level of activity of the numerous muscles involved differ widely, as illustrated in Figure 3 . The complex sequence of muscle contractions is called the motor pattern for stepping. These patterns vary as a function of walking speed, the largest differences occurring between 2.0 and 2.5 km/h for most muscles. A growing body of evidence suggests that the patterns for stepping in mammals are produced at the spinal level by the central pattern generators network  . The spinal central pattern generator network consists of coupled antagonist oscillators specifically dedicated to extensor or flexor muscles acting at the different joints. This network generates the rhythm and shapes the pattern of the motor bursts of motoneurons [19, 20] . Their mechanism allows one to produce simple and coordinated rhythmic movements, such as those involved in steady walking. Numerous experiments with spinal cats (i.e., with complete transection of the spinal cord) have demonstrated the presence of such CPG in lower mammals  , and a similar conclusion has been reached for primates  . Regarding humans, the evidence is only indirect [21, 22] . The first argument is the fact that human infants exhibit a stepping behavior from birth  and even before birth, as seen from ultrasound  or imaging recordings  , although the brain has a weak influence on the lower limbs movements at this early stage of development. Similar patterns are seen in a variety of other immature mammals    . Furthermore, studies with young infants stepping on a split-belt treadmill have shown that the stepping patterns in the two legs could be independent, but always remained coordinated (only one leg entering the swing phase at a time), resulting in an integer relationship between the steps on each side. This finding is in favor of the CPG hypothesis, because a stepping movement that would be due to a reflex mechanism (e.g., such as the stretch reflex, a muscle contraction in response to stretching in the muscle) would not exhibit such precise coordination. Other studies with babies have also shown that their stepping mechanism responds to different perturbations the same way as the one of lower mammals, for which the existence of CPG is almost certain  . Recently, this analogy has been verified on the basis of experimental results consistent with the hypothesis that, despite substantial phylogenetic distances and morphological differences, locomotion in several animal species is built starting from common primitives, perhaps related to a common ancestral neural network  . Another argument supporting the theory of a human CPG comes from patients exhibiting involuntary rhythmic spontaneous leg movements after both clinically complete [31, 32] and incomplete  spinal cord injury (SCI), thus with minimal influence of cortical signals. Similarly, sleep-related periodic leg movements have been reported. These stereotyped, periodic, repetitive movements involve one or both lower limbs. They consist of dorsiflexion of the ankle and toes and flexion of the hip and knee while the subject is lying down or asleep [34, 35] . The spinal origin of such movements is supported by their presence in patients with complete spinal lesion.