Sensorimotor adaptation of point-to-point arm movements after spaceflight: the role of internal representation of gravity force in trajectory planning

Abstract

After an exposure to weightlessness, the central nervous system operates under new dynamic and sensory contexts. To find optimal solutions for rapid adaptation, cosmonauts have to decide whether parameters from the world or their body have changed and to estimate their properties. Here, we investigated sensorimotor adaptation after a spaceflight of 10 days. Five cosmonauts performed forward point-to-point arm movements in the sagittal plane 40 days before and 24 and 72 h after the spaceflight. We found that, whereas the shape of hand velocity profiles remained unaffected after the spaceflight, hand path curvature significantly increased 1 day after landing and returned to the preflight level on the third day. Control experiments, carried out by 10 subjects under normal gravity conditions, showed that loading the arm with varying loads (from 0.3 to 1.350 kg) did not affect path curvature. Therefore, changes in path curvature after spaceflight cannot be the outcome of a control process based on the subjective feeling that arm inertia was increased. By performing optimal control simulations, we found that arm kinematics after exposure to microgravity corresponded to a planning process that overestimated the gravity level and optimized movements in a hypergravity environment (∼1.4 g). With time and practice, the sensorimotor system was recalibrated to Earth's gravity conditions, and cosmonauts progressively generated accurate estimations of the body state, gravity level, and sensory consequences of the motor commands (72 h). These observations provide novel insights into how the central nervous system evaluates body (inertia) and environmental (gravity) states during sensorimotor adaptation of point-to-point arm movements after an exposure to weightlessness.

When Up Is Down in 0g: How Gravity Sensing Affects the Timing of Interceptive Actions

“…For instance, vestibulo-ocular reflexes act to stabilize gaze in the face of head movements (Green and Angelaki, 2003), integration of gravito-inertial cues contributes to spatial navigation (Israël and Berthoz, 1989;Mittelstaedt, 1999), and maintaining an upright posture is a primary function of the vestibular organs (Cathers et al, 2005) and other graviceptor cues. Gravity may also be taken into account in the optimal control of vertical limb movements (Berret et al, 2008; Creve- coeur et al, 2010) and gravity sensing may contribute to the adaptation of limb kinematics in 0g (Papaxanthis et al, 2005;Gaveau et al, 2011). Here, we have implicated gravity sensing in a different type of function, i.e., that of predicting the motion of a visually perceived external object.…”

Direction-dependent arm kinematics reveal optimal integration of gravity cues

“…In contrast, the Smooth-Effort model minimizes a hybrid cost that, in addition to the Jerk , takes the external dynamics into account to minimize the muscular force needed to move the arm (absolute work of muscular torque). Thus, by design, the Smooth-Effort model implements the effort optimization strategy, whereby the brain uses the gravity internal model to predict and take advantage of gravity torques in accelerating and decelerating downward and upward movements, respectively (Berret et al, 2008a, 2008b; Gaveau et al, 2011, 2014). The effort optimization hypothesis predicts a sigmoidal dependence of SR on movement direction ( Smooth-Effort prediction in Figure 1D).…”

“…Although very influential, such a compensation hypothesis has been challenged by results of studies that quantified velocity profiles and revealed that the temporal organization of arm kinematics shows a small, yet consistent, dependence on movement direction, speed and load (Papaxanthis et al, 1998b; Gaveau et al, 2011, 2014). Furthermore, findings inconsistent with the compensation hypothesis have been largely ignored.…”

“…For example, recent studies, which framed motor adaptation as a process of re-optimization (Izawa et al, 2008; Crevecoeur et al, 2009; Gaveau et al, 2011; Cluff and Scott, 2015), have reported subtly altered trajectories – by contrast to the traditional compensation view that assumes invariant trajectories. Thus, newly constructed/calibrated internal models may serve trajectory optimization rather than external force compensation.…”

“…Participants comfortably sat on the aircraft’s floor with their legs strapped and their trunk in the vertical position (Figure 3A). The general organization of the task was exactly as described in previous studies (Gaveau et al, 2011, 2014). Briefly, 3 targets were centered on the participants’ right shoulder (parasagittal plane) at a distance equal to the length of their fully extended arm.…”