Olivier White

Altered gravity highlights Central Pattern Generator mechanisms

In many nonprimate species, rhythmic patterns of activity such as locomotion or respiration are generated by neural networks at the spinal level. These neural networks are called central pattern generators (CPGs). Under normal gravitational conditions, the energy efficiency and the robustness of human rhythmic movements are due to the ability of CPGs to drive the system at a pace close to its resonant frequency. This property can be compared with oscillators running at resonant frequency, for which the energy is optimally exchanged with the environment. However, the ability of the CPG to adapt the frequency of rhythmic movements to new gravitational conditions has never been studied. We show here that the frequency of a rhythmic movement of the upper limb is systematically influenced by the different gravitational conditions created in parabolic flight. The period of the arm movement is shortened with increasing gravity levels. In weightlessness, however, the period is more dependent on instructions given to the participants, suggesting a decreased influence of resonant frequency. Our results are in agreement with a computational model of a CPG coupled to a simple pendulum under the control of gravity. We demonstrate that the innate modulation of rhythmic movements by CPGs is highly flexible across gravitational contexts. This further supports the involvement of CPG mechanisms in the achievement of efficient rhythmic arm movements. Our contribution is of major interest for the study of human rhythmic activities, both in a normal Earth environment and during microgravity conditions in space.

Computation of gaze orientation under unrestrained head movements

Given the high relevance of visual input to human behavior, it is often important to precisely monitor the spatial orientation of the visual axis. One popular and accurate technique for measuring gaze orientation is based on the dual search coil. This technique does not allow for very large displacements of the subject, however, and is not robust with respect to translations of the head. More recently, less invasive procedures have been developed that record eye movements with camera-based systems attached to a helmet worn by the subject. Computational algorithms have also been developed that can calibrate eye orientation when the heads position is fixed. Given that camera-based systems measure the eyes position in its orbit, however, the reconstruction of gaze orientation is not as straightforward when the head is allowed to move. In this paper, we propose a new algorithm and calibration method to compute gaze orientation under unrestrained head conditions. Our method requires only the accurate measurement of orbital eye position (for instance, with a camera-based system), and the position of three points on the head. The calculations are expressed in terms of linear algebra, so can easily be interpreted and related to the geometry of the human body. Our calibration method has been tested experimentally and validated against independent data, proving that is it robust even under large translations, rotations, and torsions of the head.

The relation between geometry and time in mental actions.

Mental imagery is a cognitive tool that helps humans take decisions by simulating past and future events. The hypothesis has been advanced that there is a functional equivalence between actual and mental movements. Yet, we do not know whether there are any limitations to its validity even in terms of some fundamental features of actual movements, such as the relationship between space and time. Although it is impossible to directly measure the spatiotemporal features of mental actions, an indirect investigation can be conducted by taking advantage of the constraints existing in planar drawing movements and described by the two-thirds power law (2/3PL). This kinematic law describes one of the most impressive regularities observed in biological movements: movement speed decreases when curvature increases. Here, we compared the duration of identical actual and mental arm movements by changing the constraints imposed by the 2/3PL. In the first two experiments, the length of the trajectory remained constant, while its curvature (Experiment 1) or its number of inflexions (Experiment 2) was manipulated. The results showed that curvature, but not the number of inflexions, proportionally and similarly affected actual and mental movement duration, as expected from the 2/3PL. Two other control experiments confirmed that the results of Experiment 1 were not attributable to eye movements (Experiment 3) or to the perceived length of the displayed trajectory (Experiment 4). Altogether, our findings suggest that mental movement simulation is tuned to the kinematic laws characterizing actions and that kinematics of actual and mental movements is completely specified by the representation of their geometry.

The Role of Left Supplementary Motor Area in Grip Force Scaling

Skilled tool use and object manipulation critically relies on the ability to scale anticipatorily the grip force (GF) in relation to object dynamics. This predictive behaviour entails that the nervous system is able to store, and then select, the appropriate internal representation of common object dynamics, allowing GF to be applied in parallel with the arm motor commands. Although psychophysical studies have provided strong evidence supporting the existence of internal representations of object dynamics, known as “internal models”, their neural correlates are still debated. Because functional neuroimaging studies have repeatedly designated the supplementary motor area (SMA) as a possible candidate involved in internal model implementation, we used repetitive transcranial magnetic stimulation (rTMS) to interfere with the normal functioning of left or right SMA in healthy participants performing a grip-lift task with either hand. TMS applied over the left, but not right, SMA yielded an increase in both GF and GF rate, irrespective of the hand used to perform the task, and only when TMS was delivered 130–180 ms before the fingers contacted the object. We also found that both left and right SMA rTMS led to a decrease in preload phase durations for contralateral hand movements. The present study suggests that left SMA is a crucial node in the network processing the internal representation of object dynamics although further experiments are required to rule out that TMS does not affect the GF gain. The present finding also further substantiates the left hemisphere dominance in scaling GF.

Active collisions in altered gravity reveal eye-hand coordination strategies

Most object manipulation tasks involve a series of actions demarcated by mechanical contact events, and gaze is usually directed to the locations of these events as the task unfolds. Typically, gaze foveates the target 200 ms in advance of the contact. This strategy improves manual accuracy through visual feedback and the use of gaze-related signals to guide the hand/object. Many studies have investigated eye-hand coordination in experimental and natural tasks; most of them highlighted a strong link between eye movements and hand or object kinematics. In this experiment, we analyzed gaze strategies in a collision task but in a very challenging dynamical context. Participants performed collisions while they were exposed to alternating episodes of microgravity, hypergravity and normal gravity. First, by isolating the effects of inertia in microgravity, we found that peak hand acceleration marked the transition between two modes of grip force control. Participants exerted grip forces that paralleled load force profiles, and then increased grip up to a maximum shifted after the collision. Second, we found that the oculomotor strategy adapted visual feedback of the controlled object around the collision, as demonstrated by longer durations of fixation after collision in new gravitational environments. Finally, despite large variability of arm dynamics in altered gravity, we found that saccades were remarkably time-locked to the peak hand acceleration in all conditions. In conclusion, altered gravity allowed light to be shed on predictive mechanisms used by the central nervous system to coordinate gaze, hand and grip motor actions during a mixed task that involved transport of an object and high impact loads.

Grip Force Regulates Hand Impedance to Optimize Object Stability in High Impact Loads

Anticipatory grip force adjustments are a prime example of the predictive nature of motor control. An object held in precision grip is stabilized by fine adjustments of the grip force against changes in tangential load force arising from inertia during acceleration and deceleration. When an object is subject to sudden impact loads, prediction becomes critical as the time available for sensory feedback is very short. Here, we investigated the control of grip force when participants performed a targeted tapping task with a hand-held object. During the initial transport phase of the movement, load force varied smoothly with acceleration. In contrast, in the collision, load forces sharply increased to very large values. In the transport phase, grip force and load force were coupled in phase, as expected. However, in the collision, grip force did not parallel load force. Rather, it exhibited a stereotyped profile with maximum ∼65 ms after peak load at contact. By using catch trials and a virtual environment, we demonstrate that this peak of grip force is pre-programmed. This observation is validated across experimental manipulations involving different target stiffness and directions of movement. We suggest that the central nervous system optimizes stability in object manipulation-as in catching-by regulating mechanical parameters including stiffness and damping through grip force. This study provides novel insights about how the brain coordinates grip force in manipulation involving an object interacting with the environment.

The brain adjusts grip forces differently according to gravity and inertia: a parabolic flight experiment.

In everyday life, one of the most frequent activities involves accelerating and decelerating an object held in precision grip. In many contexts, humans scale and synchronize their grip force (GF), normal to the finger/object contact, in anticipation of the expected tangential load force (LF), resulting from the combination of the gravitational and the inertial forces. In many contexts, GF and LF are linearly coupled. A few studies have examined how we adjust the parameters-gain and offset-of this linear relationship. However, the question remains open as to how the brain adjusts GF regardless of whether LF is generated by different combinations of weight and inertia. Here, we designed conditions to generate equivalent magnitudes of LF by independently varying mass and movement frequency. In a control experiment, we directly manipulated gravity in parabolic flights, while other factors remained constant. We show with a simple computational approach that, to adjust GF, the brain is sensitive to how LFs are produced at the fingertips. This provides clear evidence that the analysis of the origin of LF is performed centrally, and not only at the periphery.

Coherent Multimodal Sensory Information Allows Switching between Gravitoinertial Contexts

Whether the central nervous system is capable to switch between contexts critically depends on experimental details. Motor control studies regularly adopt robotic devices to perturb the dynamics of a certain task. Other approaches investigate motor control by altering the gravitoinertial context itself as in parabolic flights and human centrifuges. In contrast to conventional robotic experiments, where only the hand is perturbed, these gravitoinertial or immersive settings coherently plunge participants into new environments. However, radically different they are, perfect adaptation of motor responses are commonly reported. In object manipulation tasks, this translates into a good matching of the grasping force or grip force to the destabilizing load force. One possible bias in these protocols is the predictability of the forthcoming dynamics. Here we test whether the successful switching and adaptation processes observed in immersive environments are a consequence of the fact that participants can predict the perturbation schedule. We used a short arm human centrifuge to decouple the effects of space and time on the dynamics of an object manipulation task by adding an unnatural explicit position-dependent force. We created different dynamical contexts by asking 20 participants to move the object at three different paces. These contextual sessions were interleaved such that we could simulate concurrent learning. We assessed adaptation by measuring how grip force was adjusted to this unnatural load force. We found that the motor system can switch between new unusual dynamical contexts, as reported by surprisingly well-adjusted grip forces, and that this capacity is not a mere consequence of the ability to predict the time course of the upcoming dynamics. We posit that a coherent flow of multimodal sensory information born in a homogeneous milieu allows switching between dynamical contexts.

Initial information prior to movement onset influences kinematics of upward arm pointing movements

To elaborate a motor plan and perform online control in the gravity field, the brain relies on priors and multisensory integration of information. In particular, afferent and efferent inputs related to the initial state are thought to convey sensorimotor information to plan the upcoming action. Yet it is still unclear to what extent these cues impact motor planning. Here we examined the role of initial information on the planning and execution of arm movements. Participants performed upward arm movements around the shoulder at three speeds and in two arm conditions. In the first condition, the arm was outstretched horizontally and required a significant muscular command to compensate for the gravitational shoulder torque before movement onset. In contrast, in the second condition the arm was passively maintained in the same position with a cushioned support and did not require any muscle contraction before movement execution. We quantified differences in motor performance by comparing shoulder velocity profiles. Previous studies showed that asymmetric velocity profiles reflect an optimal integration of the effects of gravity on upward movements. Consistent with this, we found decreased acceleration durations in both arm conditions. However, early differences in kinematic asymmetries and EMG patterns between the two conditions signaled a change of the motor plan. This different behavior carried on through trials when the arm was at rest before movement onset and may reveal a distinct motor strategy chosen in the context of uncertainty. Altogether, we suggest that the information available online must be complemented by accurate initial information.

Towards human exploration of space: the THESEUS review series on neurophysiology research priorities

The THESEUS project (Towards Human Exploration of Space: a European Strategy), initiated within the seventh Framework Programme by the European Commission, aimed at providing a cross-cutting, life-science-based roadmap for Europe’s strategy towards human exploration of long space missions, and its relevance to applications on Earth. This topic was investigated by experts in the field, in the framework of the THESEUS project whose aim was to develop an integrated life sciences research roadmap regarding human space exploration. In particular, decades of research have shown that altered gravity impairs neurological responses at large, such as perception, sleep, motor control, and cognitive factors. International experts established a list of key issues that should be addressed in that context and provided several recommendations such as a maximal exploitation of currently available resources on Earth and in space.