Stability of Action and Kinesthetic Perception in Parkinson's Disease

Abstract

We present a review of action and perception stability within the theoretical framework based on the idea of control with spatial referent coordinates for the effectors at a number of hierarchical levels. Stability of salient variables is ensured by synergies, neurophysiological structures that act in multi-dimensional spaces of elemental variables and limit variance to the uncontrolled manifold during action and iso-perceptual manifold during perception. Patients with Parkinson's disease show impaired synergic control reflected in poor stability (low synergy indices) and poor agility (low indices of anticipatory synergy adjustments prior to planned quick actions). They also show impaired perception across modalities, including kinesthetic perception. We suggest that poor stability at the level of referent coordinates can be the dominant factor leading to poor stability of percepts.

Keywords: abundance; basal ganglia; iso-perceptual manifold; referent coordinate.

Figure 1

Basics of the control with referent coordinates. A: At the level of the muscle, λ specifies the length threshold of the tonic stretch reflex. Changes in muscle length and force can occur from a shift in or from shifts in external load. A combination of force and length when the muscle is in equilibrium with the external load is addressed as the equilibrium point (EP), e.g., EP_2B, with subscripts representative of λ and load. Afferent signals of various modalities increase in magnitude along the force-length characteristics. Efferent (EFF) command serves as a referent coordinate within which afferent (AFF) signals are interpreted to form perception of muscle length and force, symbolized as EFF + AFF. B: At the level of the joint, force-length characteristics for agonist and antagonist muscles are specified by their respective AG and ANT. The resultant torque-angle characteristic defines possible angle/torque combinations for the joint. C: At the level of the joint, the R-command results in a parallel shift in force-length characteristics, effectively moving the torque-angle characteristic without changing its slope. D: The C-command represents shifts of the two force-length characteristics in opposite directions, effectively changing the slope of the torque-angle characteristic.

Figure 2

Synergies. A: A subject is shown an on-screen target and is asked to produce 10 N of force with two fingers of the right hand. B: Across trials, at each time point, Finger 1 force (F1) is plotted against Finger 2 force (F2). The space along which the performance variable remains unchanged (i.e., F1 + F2 = 10 N) is the uncontrolled manifold (UCM); the space along which performance changes is the orthogonal to the UCM space (ORT). Variance of the data within the UCM and within ORT space are graphically represented.

Figure 3

Effects of agonist-antagonist co-contraction. Elbow flexors are defined as positive torque producers and are labeled as agonists. A: The referent coordinate (RC) at the level of muscle group (equivalent to λ from Fig. 1) specifies its force-length characteristic. The resultant torque-angle characteristic defines the joint angle and torque (equal to 0 assuming no external load). B: During co-contraction, a change in the C-command results in opposite shifts of agonist and antagonist force-length characteristics. Efferent and afferent activity to/from both agonist and antagonist musculature increase. The percept of joint position remains unchanged despite changes in all salient afferent and efferent signals.

Figure 4

Kinesthetic Perception at Different Hierarchical Levels. RC_TASK undergoes a sequence of few-to-many transformations to R- and C-commands at the joint level. Each R- and C-command undergoes further few-to-many transformations to individual muscle λ. Sensory endings within muscles comprise many-to-few transformations to form joint angle/force information. Similar many-to-few transformations occur at the joint angle and force level to comprise information of endpoint position and force sense.

Figure 5

Effects of PD on Kinesthetic Perception. Accuracy of perception of coordinate x, estimated as the SDx over successive trials, is defined by variability of the central component, SD_RC, and of the afferent contribution, SD_AFF. The perceived coordinate is equal to RC + ƒ(AFF) and is estimated about a point with coordinates {x, F}. Parkinson’s Disease is expected to lead to SD_RC >> SD_AFF, thus leading to similar effects under small and large SD_AFF.