Efference copy in kinesthetic perception: a copy of what is it?

Abstract

A number of notions in the fields of motor control and kinesthetic perception have been used without clear definitions. In this review, we consider definitions for efference copy, percept, and sense of effort based on recent studies within the physical approach, which assumes that the neural control of movement is based on principles of parametric control and involves defining time-varying profiles of spatial referent coordinates for the effectors. The apparent redundancy in both motor and perceptual processes is reconsidered based on the principle of abundance. Abundance of efferent and afferent signals is viewed as the means of stabilizing both salient action characteristics and salient percepts formalized as stable manifolds in high-dimensional spaces of relevant elemental variables. This theoretical scheme has led recently to a number of novel predictions and findings. These include, in particular, lower accuracy in perception of variables produced by elements involved in a multielement task compared with the same elements in single-element tasks, dissociation between motor and perceptual effects of muscle coactivation, force illusions induced by muscle vibration, and errors in perception of unintentional drifts in performance. Taken together, these results suggest that participation of efferent signals in perception frequently involves distorted copies of actual neural commands, particularly those to antagonist muscles. Sense of effort is associated with such distorted efferent signals. Distortions in efference copy happen spontaneously and can also be caused by changes in sensory signals, e.g., those produced by muscle vibration.

Keywords: coactivation; force matching; kinesthetic perception; referent coordinate; sense of effort.

Graphical abstract

Figure 1.

The classical scheme of the efference copy (EC) as a copy of the output of the alpha-motoneuronal pool. EC is used to predict changes in sensory signals from proprioceptors expected from the planned action (ReA, reafference); this process involves conversion of EC into “EC” expressed in units commensurate with those encoded by afferent signals. If the prediction is wrong, an error signal (ΔA) is sent to the alpha-motoneurons leading to correction of the action. Reafference affects perception only if it differs from the prediction based on EC. MNs, motoneurons.

Figure 2.

A: the force-length characteristics for a relaxed muscle (dashed curve) and activated muscle (thick, solid curves). Active muscle force (F_A) can be expressed as a function ƒ of the difference between L and λ. A value of λ defines the spatial range where the muscle is active and produces length-dependent active force. A shift of λ (from λ₁ to λ₂) can produce movement, muscle force change, or both depending on the external load (shown with dotted, thin lines). B: the force-coordinate, F(X) characteristics for the agonist muscles (positive force magnitudes) and antagonist muscles (negative force magnitudes). Effector behavior is defined by the algebraic sum of the two muscle characteristics (the thick, slanted line). Its control can be described with referent coordinates to the opposing muscle groups, RC_AG and RC_ANT or, equivalently, by the reciprocal command (R-command, filled circle) and the coactivation command (C-command). The R-command leads to parallel changes in RC_AG and RC_ANT leading to translation of the effector characteristic and in its intercept. The C-command (the distance between RC_AG and RC_ANT) leads to counter-directional changes in RC_AG and RC_ANT leading to rotation of the effector characteristic and in its slope. RC, referent coordinates.

Figure 3.

Body movement in the three-dimensional space can be described by time functions of three-dimensional vectors R and C. Given the actual body anatomy, these task-level control variables have to be transformed into limb-level, joint-level, muscle-level, and motor unit (MU)-level variables. The number of degrees-of-freedom (DOFs) increases as a result of these transformations. Back-coupling loops within the CNS and from peripheral receptors ensure stability of performance. CNS, central nervous system; RC, referent coordinates.

Figure 4.

A cartoon example of two elements, agonist and antagonist muscles acting at a joint, controlled with one neural variable each (λ₁ and λ₂) and equipped with one source of sensory information, e.g. a spindle ending, each (A₁ and A₂). Joint control can be reduced to a single variable, RC_J = (λ₁ + λ₂)/2. A: the solution space for a given magnitude of RC_J—its UCM (slanted line) and a theoretical intertrial data distribution (ellipse elongated along the UCM). B: a linear image of the IPM in the three-dimensional space of RC_J, A₁, and A₂. Stable perception of a joint angle is compatible with both unchanged RC_J and varying RC_J (compare points 1 and 2). IPM, iso-perceptual manifold; RC, referent coordinates; UCM, uncontrolled manifold.

Figure 5.

The efferent process (EFF) defines a magnitude of λ—threshold of stretch reflex. Deviations from λ are associated with an increase in muscle length, force, and activation level. Signals from muscle spindles, Golgi tendon organs, alpha-motoneurons, and even from gamma-motoneurons can be used to identify a point on the muscle force-length characteristic and contribute to perception of both muscle force and length. AFF, afferent contribution; Ia, Ib, and II stand for the corresponding groups of afferent fibers.

Figure 6.

A: the task-hand produces a force magnitude in isometric conditions with a combination of RC to the agonist (RC_AG) and antagonist (RC_ANT) muscles. The effector characteristic is shown with the thick, solid line. B: the match-hand shows higher force, smaller apparent stiffness (slope of the effector characteristic), and large absolute magnitude of its RC (n = 11; ANOVA). All three effects can be expected from a shift of RC_ANT toward the actual fingertip coordinate (ΔRC_ANT). Assuming differences in RC_AG between the two hands or between the R- or C-commands is unable to account for the findings (see text). RC, referent coordinates.

Figure 7.

Effects of vibration of force matching. Left: during vibration of the task-hand, assuming RC_ANT magnitude closer to the actual effector coordinate accounts for the pattern of findings: an increase in the force difference between the hands ΔF, an increase in the absolute magnitude of ΔRC, and a drop in Δk (n = 11; ANOVA). Right: opposite effects are observed during the vibration of the match-hand: a drop in ΔF, a drop in the absolute magnitude of ΔRC, and an increase in Δk. RC, referent coordinates; RC_AG, RC to the agonist muscles; RC_ANT, RC to the antagonist muscle.

Figure 8.

For simplicity, this figure uses only one variable, RC, directed to the instructed effector (task-hand), which has a corollary stream participating in perception (RC_P), equivalent to efference copy (EC). RC_P defines action by the match-hand. It can change due to effects from peripheral sensory signals (e.g., caused by vibration) as well as spontaneously. RC, referent coordinates.

Figure 9.

A: coactivating muscles (C₂ > C₁) lead to an increase in the effector’s apparent stiffness, k (k₂ > k₁). This produces an increase in force from the initial level (white circle) to F_ΔC (black circle) (n = 10; ANOVA). B: the force increase can be partly compensated by a shift in RC toward the actual effector coordinate (gray circle, RC₂ < RC₁). Verbal reports reflect sense of effort, i.e., RC magnitude. Modified by permission from Cuadra et al. (182). RC, referent coordinates. F_∆C, force after additional coactivation; F_TASK, force defined by the task; F_X, force along the X coordinate.