Ana Bengoetxea

From Spinal Central Pattern Generators to Cortical Network: Integrated BCI for Walking Rehabilitation

Success in locomotor rehabilitation programs can be improved with the use of brain-computer interfaces (BCIs). Although a wealth of research has demonstrated that locomotion is largely controlled by spinal mechanisms, the brain is of utmost importance in monitoring locomotor patterns and therefore contains information regarding central pattern generation functioning. In addition, there is also a tight coordination between the upper and lower limbs, which can also be useful in controlling locomotion. The current paper critically investigates different approaches that are applicable to this field: the use of electroencephalogram (EEG), upper limb electromyogram (EMG), or a hybrid of the two neurophysiological signals to control assistive exoskeletons used in locomotion based on programmable central pattern generators (PCPGs) or dynamic recurrent neural networks (DRNNs). Plantar surface tactile stimulation devices combined with virtual reality may provide the sensation of walking while in a supine position for use of training brain signals generated during locomotion. These methods may exploit mechanisms of brain plasticity and assist in the neurorehabilitation of gait in a variety of clinical conditions, including stroke, spinal trauma, multiple sclerosis, and cerebral palsy.

Effect of gravity on human spontaneous 10-Hz electroencephalographic oscillations during the arrest reaction.

Electroencephalographic oscillations at 10 Hz (alpha and mu rhythms) are the most prominent rhythms observed in awake, relaxed (eye-closed) subjects. These oscillations may be considered as a marker of cortical inactivity or an index of the active inhibition of the sensory information. Different cortical sources may participate in the 10-Hz oscillation and appear to be modulated by the sensory context and functional demands. In microgravity, the marked reduction in multimodal graviceptive inputs to cortical networks participating in the representation of space could be expected to affect the 10-Hz activity. The effect of microgravity on this basic oscillation has heretofore not been studied quantitatively. Because the alpha rhythm has a functional role in the regulation of network properties of the visual areas, we hypothesised that the absence of gravity would affect its strength. Here, we report the results of an experiment conducted over the course of 3 space flights, in which we quantified the power of the 10-Hz activity in relation to the arrest reaction (i.e., in 2 distinct physiological states: eyes open and eyes closed). We observed that the power of the spontaneous 10-Hz oscillation recorded in the eyes-closed state in the parieto-occipital (alpha rhythm) and sensorimotor areas (mu rhythm) increased in the absence of gravity. The suppression coefficient during the arrest reaction and the related spectral perturbations produced by eye-opening/closure state transition also increased in on orbit. These results are discussed in terms of current theories on the source and the importance of the alpha rhythm for cognitive function.

Evidence of a preprogrammed deactivation of the hamstring muscles for triggering rapid changes of posture in humans

Normal subjects were asked to make rapid flexions of the legs from a stationary initial standing posture in a self-paced mode. Because this movement implicates a rapid change in posture, questions were asked about the type of central command which must include the rupture of the erect posture and the accomplishment of the goal directed movement. Movements of the different segments of the body were recorded and analyzed using the optoelectronic ELITE system. Electromyographic (EMG) activities of 8 muscles of the lower limb on one side were recorded, rectified and integrated. The time relationships of the different EMG signals (activation or deactivation) were analyzed with respect to selected kinetic measures of the related segments of the body. In the majority of the subjects, before the movement onset, EMG events included a specific deactivation of the tonic EMG activity of the semimembranous (SM) and semitendinous (ST) muscles (time onset relative to the onset of the legs flexion: -196.9 +/- 96.4 ms and -180.5 +/- 89.7 ms, respectively). A second event was a phasic activation of the tibialis anterior (TA) muscle (time onset: -60.5 +/- 117.6 ms). Conjugate cross-correlation analysis of these EMG signals demonstrated the existence of a common coordinated strategy between the deactivation of the hamstring and the TA activation. Even though a small horizontal displacement of the head was recorded prior to leg movement, it occurred too late to induce deactivation of the hamstring muscles. These results demonstrate that for rapid legs flexion, where the gravity forces are the main source of joint angle acceleration, the deactivation of the SM and ST muscles acts in conjunction with the phasic activation of the TA. The preprogrammed deactivation of the SM and ST muscles represents the early phase of the central command to switch from the standing to the squatting posture.

Early emergence of temporal co-ordination of lower limb segments elevation angles in human locomotion

We analysed the co-ordination of the elevation angles of the thigh (alpha(t)), shank (alpha(s)) and foot (alpha(f)) during walking in 19 adults and 21 children (aged 11--144 months), including the very first unsupported steps in four. Cross-correlation functions (CCF) maturation of pairs of elevation angles was quantified by a global error parameter (Et((CCF))) reflecting the difference between particular CCF value of toddlers and mean adult value (Ea((CCF))). During the very first step, Et((CCF)) could be five times higher than Ea((CCF)). With walking experience, Et((CCF)) for both alpha(t)-alpha(s) and alpha(s)-alpha(f) pairs evolved following a biexponential profile, with a fast time constant below 6 months. Adult-like CCF parameters were reached earlier for alpha(s)-alpha(f) than alpha(t)-alpha(s), indicating disto-proximal maturation of the temporal co-ordination of the lower limb segments in human locomotion.

A dynamic recurrent neural network for multiple muscles electromyographic mapping to elevation angles of the lower limb in human locomotion.

This paper describes the use of a dynamic recurrent neural network (DRNN) for simulating lower limb coordination in human locomotion. The method is based on mapping between the electromyographic signals (EMG) from six muscles and the elevation angles of the three main lower limb segments (thigh, shank and foot). The DRNN is a fully connected network of 35 hidden units taking into account the temporal relationships history between EMG and lower limb kinematics. Each EMG signal is sent to all 35 units, which converge to three outputs. Each output neurone provides the kinematics of one lower limb segment. The training is supervised, involving learning rule adaptations of synaptic weights and time constant of each unit. Kinematics of the locomotor movements were recorded and analysed using the opto-electronic ELITE system. Comparative analysis of the learning performance with different types of output (position, velocity and acceleration) showed that for common gait mapping velocity data should be used as output, as it is the best compromise between asymptotic error curve, rapid convergence and avoidance of bifurcation. Reproducibility of the identification process and biological plausibility were high, indicating that the DRNN may be used for understanding functional relationships between multiple EMG and locomotion. The DRNN might also be of benefit for prosthetic control.

Optimal walking speed following changes in limb geometry

SUMMARY The principle of dynamic similarity states that the optimal walking speeds of geometrically similar animals are independent of size when speed is normalized to the dimensionless Froude number (Fr). Furthermore, various studies have shown similar dimensionless optimal speed (Fr ∼0.25) for animals with quite different limb geometries. Here, we wondered whether the optimal walking speed of humans depends solely on total limb length or whether limb segment proportions play an essential role. If optimal walking speed solely depends on the limb length then, when subjects walk on stilts, they should consume less metabolic energy at a faster optimal speed than when they walk without stilts. To test this prediction, we compared kinematics, electromyographic activity and oxygen consumption in adults walking on a treadmill at different speeds with and without articulated stilts that artificially elongated the shank segment by 40 cm. Walking on stilts involved a non-linear reorganization of kinematic and electromyography patterns. In particular, we found a significant increase in the alternating activity of proximal flexors–extensors during the swing phase, despite significantly shorter normalized stride lengths. The minimal metabolic cost per unit distance walked with stilts occurred at roughly the same absolute speed, corresponding to a lower Fr number (Fr ∼0.17) than in normal walking (Fr ∼0.25). These findings are consistent with an important role of limb geometry optimization and kinematic coordination strategies in minimizing the energy expenditure of human walking.

Distinct multi-joint control strategies in spastic diplegia associated with prematurity or Angelman syndrome

Spastic diplegia is commonly due to periventricular leucomalacia associated with premature birth. It is also a feature of Angelman syndrome (AS), a neurogenetic disorder with developmental delay, absent speech and mirthful behaviour. We studied the kinematics and kinetics of the squatting movement and associated electromyographic (EMG) activities in 20 children with spastic diplegia associated with periventricular leucomalacia (SDPL) or AS and 18 unimpaired children. While movement of normal subjects consisted of vertical translation of most body segments, the movement of SDPL children was operated around the fixed knee with backward shift of the hip, and AS children performed a forward flexion of the trunk over the thigh. Trunk stability was correlated with movement velocity in both pathological groups. In normal subjects, anticipatory EMG pattern consisted of silencing of hamstring muscle tonic activity prior to movement onset. This deactivation was not present in spastic diplegia. In SDPL, anticipatory overactivation of ankle joint actuators was recorded and tonic co-contraction persisted throughout the movement. In AS, rhythmic EMG bursting was seen during the movement. Shoulder, hip and knee trajectories in the sagittal plane showed marked within-group stereotypies in orientation, shape and length. The patterns in both pathological groups were therefore distinctive. We speculate that they reflect corticospinal impairment in SDPL and combined corticospinal and cerebellar dysfunction in AS.

Movement gating of beta/gamma oscillations involved in the N30 somatosensory evoked potential.

Evoked potential modulation allows the study of dynamic brain processing. The mechanism of movement gating of the frontal N30 component of somatosensory evoked potentials (SEP) produced by the stimulation of the median nerve at wrist remains to be elucidated. At rest, a power enhancement and a significant phase‐locking of the electroencephalographic (EEG) oscillation in the beta/gamma range (25–35 Hz) are related to the emergence of the N30. The latter was also perfectly identified in presence of pure phase‐locking situation. Here, we investigated the contribution of these rhythmic activities to the specific gating of the N30 component during movement. We demonstrated that concomitant execution of finger movement of the stimulated hand impinges such temporal concentration of the ongoing beta/gamma EEG oscillations and abolishes the N30 component throughout their large topographical extent on the scalp. This also proves that the phase‐locking phenomenon is one of the main actors for the N30 generation. These findings could be explained by the involvement of neuronal populations of the sensorimotor cortex and other related areas, which are unable to respond to the phasic sensory activation and to phase‐lock their firing discharges to the external sensory input during the movement. This new insight into the contribution of phase‐locked oscillation in the emergence of the N30 and in its gating behavior calls for a reappraisal of fundamental and clinical interpretation of the frontal N30 component. Hum Brain Mapp 2009.

Gravity Influences Top-Down Signals in Visual Processing

Visual perception is not only based on incoming visual signals but also on information about a multimodal reference frame that incorporates vestibulo-proprioceptive input and motor signals. In addition, top-down modulation of visual processing has previously been demonstrated during cognitive operations including selective attention and working memory tasks. In the absence of a stable gravitational reference, the updating of salient stimuli becomes crucial for successful visuo-spatial behavior by humans in weightlessness. Here we found that visually-evoked potentials triggered by the image of a tunnel just prior to an impending 3D movement in a virtual navigation task were altered in weightlessness aboard the International Space Station, while those evoked by a classical 2D-checkerboard were not. Specifically, the analysis of event-related spectral perturbations and inter-trial phase coherency of these EEG signals recorded in the frontal and occipital areas showed that phase-locking of theta-alpha oscillations was suppressed in weightlessness, but only for the 3D tunnel image. Moreover, analysis of the phase of the coherency demonstrated the existence on Earth of a directional flux in the EEG signals from the frontal to the occipital areas mediating a top-down modulation during the presentation of the image of the 3D tunnel. In weightlessness, this fronto-occipital, top-down control was transformed into a diverging flux from the central areas toward the frontal and occipital areas. These results demonstrate that gravity-related sensory inputs modulate primary visual areas depending on the affordances of the visual scene.

Two reference frames for visual perception in two gravity conditions

The processing and storage of visual information concerning the orientation of objects in space is carried out in anisotropic reference frames in which all orientations are not treated equally. The perceptual anisotropies, and the implicit reference frames that they define, are evidenced by the observation of ‘oblique effects’ in which performance on a given perceptual task is better for horizontally and vertically oriented stimuli. The question remains how the preferred horizontal and vertical reference frames are defined. In these experiments cosmonaut subjects reproduced the remembered orientation of a visual stimulus in 1g (on the ground) and in 0g, both attached to a chair and while free-floating within the International Space Station. Results show that while the remembered orientation of a visual stimulus may be stored in a multimodal reference frame that includes gravity, an egocentric reference is sufficient to elicit the oblique effect when all gravitational and haptic cues are absent.