Functional Synergies Underlying Control of Upright Posture during Changes in Head Orientation

<div><h3>Background</h3><p>Studies of human upright posture typically have stressed the need to control ankle and hip joints to achieve postural stability. Recent studies, however, suggest that postural stability involves multi degree-of-freedom (DOF) coordination, especially when performing supra-postural tasks. This study investigated kinematic synergies related to control of the body’s position in space (two, four and six DOF models) and changes in the head’s orientation (six DOF model).</p> <h3>Methodology/Principal Findings</h3><p>Subjects either tracked a vertically moving target with a head-mounted laser pointer or fixated a stationary point during 4-min trials. Uncontrolled manifold (UCM) analysis was performed across tracking cycles at each point in time to determine the structure of joint configuration variance related to postural stability or tracking consistency. The effect of simulated removal of covariance among joints on that structure was investigated to further determine the role of multijoint coordination. Results indicated that cervical joint motion was poorly coordinated with other joints to stabilize the position of the body center of mass (CM). However, cervical joints were coordinated in a flexible manner with more caudal joints to achieve consistent changes in head orientation.</p> <h3>Conclusions/Significance</h3><p>An understanding of multijoint coordination requires reference to the stability/control of important performance variables. The nature of that coordination differs depending on the reference variable. Stability of upright posture primarily involved multijoint coordination of lower extremity and lower trunk joints. Consistent changes in the orientation of the head, however, required flexible coordination of those joints with motion of the cervical spine. A two-segment model of postural control was unable to account for the observed stability of the CM position during the tracking task, further supporting the need to consider multijoint coordination to understand postural stability.</p> </div

Example of components of joint configuration variance across the tracking cycle.

<p>Components of joint configuration variance per dimension of joint subspace (deg²) across the tracking cycle, related to stability of the 4-DOF CM position of a representative subject. Note the consistency of V_UCM and V_ORT across the cycle, leading to using the average across the cycle for further statistical analyses.</p

Constant and variable error of targeting.

<p>Upper Panels: Average across trials projection of the laser pointer (black dots) onto the screen at every 10 frames of tracking for one representative subject, after each cycle was normalized to 100 frames. Units are in meters (m). Lower Panels: Average across-subjects constant error (±SEM) and variable error (±SEM) of targeting with respect to the moving cursor are shown.</p

Average components of joint configuration variance.

<p>Mean (±SEM) components of joint configuration variance per dimension of joint subspace, related to stability of the center of mass position based on a 6-joint (CM_POS-6DOF) and a 4-joint (CM_POS-4DOF) geometric model and a 2 segment model, and for head orientation with the target (HEAD_ORI), all computed during quiet standing while visually fixating a point between two stationary targets and across cycles of tracking the moving target with the head. Significant differences between V_UCM and V_ORT: <b>^*</b>p<0.05; <b>^#</b>p<0.005; <b>^##</b>p<0.001.</p

Experimental setup.

<p>A. Cartoon of experimental setup showing link-segment model, reflective marker locations, and position of subject relative to the projection screen mounted on a rigid wall. Circles indicate frontal plane view of 10-cm diameter fixed targets and 5-cm diameter moving target; B. Calibration trial had the hat placed on a high stool. H₁, H₂, and H₃ are the reflective markers on the hat brim comprising the rigid body from which a local coordinate system was constructed. P₁ is the reflective marker placed during calibration at the location where the beam was emitted from the laser. P₀ is the point of intersection of the laser with the screen, calibrated with a reflective marker. P₁ and P₀ were used to determine the unit vector û along the laser beam in relation to the local coordinate system of the hat rigid body. Wall markers W₁, W₂, and W₃ were used to calibrate the wall’s position in the global coordinate frame.</p

Range of joint excursion.

<p>Mean across subjects (±SEM) of the maximum joint excursions for all measured joint motions for quiet standing while visually fixating a point between two stationary targets and across cycles of tracking the moving target with the head; L5-S1 =  joint between 5^th lumbar and 1^st sacral vertebrae, C7-T1 =  joint between 7^th cervical and 1^st thoracic vertebrae. Cycles were defined as pseudo-cycles for quiet standing with the same average cycle time as with target tracking.</p

Emergence of bias for inferred reaches in the DNF model.

<p>The figure shows two snapshots of the activation patterns in the model during a single PMG trial. (A) During the memory period, after the presentation of a spatial cue, an activation peak has formed in the association field. Its position along the spatial axis reflects the direction of the spatial cue, while its location along the second dimension is unspecific and spans both context-sensitive regions (shown as outlines in the association field, green for direct, white for inferred context). The region that shows preference for the inferred context is substantially larger than the direct-context region, due to the high proportion of inferred trials during training. This region projects to the location in the motor preparation field which codes for a reach in the direction opposite to the spatial cue. The competitive interactions in the motor preparation field further amplify this stronger input that supports the inferred reach. (B) When a context signal for a direct trial is given at the end of the memory period, the context input induces a shift of the peak in the association field: It is pulled almost completely onto the region specific for the direct context with which it partly overlapped. The input to the motor preparation field changes accordingly, leading to a switch in that field's activation pattern and a stronger activation of the ‘direct’ reach direction.</p

Choice behavior of monkeys and model in PMG-NC trials.

<p>If no context instruction is given in a trial, both model and monkeys show an inherent bias to perform the inferred reach after training (A). A balanced choice behavior (B) can be achieved by application of an appropriate reward schedule (BRMS).</p

Influence of input statistics on model behavior and activation pattern during the memory period.

<p>(A) The behavioral bias for inferred reaches in the free-choice trials depends on the percentage of inferred trials during IR training and rises continuously in a sigmoidal fashion (logistic fit function; black curve). (B) The difference of the mean activation of the motor preparation field at the preferred and opposite-to-preferred position during the memory period shows a softer, but also approximately sigmoid increase when the number of inferred trials is increased.</p

Origin of generalization errors in the model.

<p>Two snapshots of the activation patterns in the model during the memory period are shown, taken from different trials that developed different movement plans due to random noise in the model. In both cases, the spatial cue was located at 225° (an oblique direction not used during training), the blue context input indicates that an inferred reach should be performed. The model is depicted in the same form as in <a href="http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1002774#pcbi-1002774-g001" target="_blank">Figure 1</a>. Arrows show the dominant active projections between fields that arise from the current activation patterns. Regions with pronounced preference for one context are outlined in the association field (green for direct context, white for inferred). (A) When the spatial cue was presented at the beginning of the trial (white arrow), it created an activation peak in the association field at the untrained oblique direction. This active region in the association field projects topologically to the motor preparation field, therefore preparing a reach to the spatial cue direction. This corresponds to a deviation of 180° from the goal direction, since the context cue indicates that an inferred reach should be performed. (B) If the activation peak in the association overlaps partly with a region that is selective for the inferred context, the activation peak may shift over to that region (the figure shows an intermediate step of this shift). This is driven by the input from the context node. The region of the association field that is now active has adapted its projection to the motor preparation field during training, and induces a new activation peak in the motor preparation field around 360°. This yields a deviation of 45° from the goal location, since the model now prepares one of the trained reaches in a cardinal direction.</p