The adaptability of self-action perception and movement control when the limb is passively versus actively moved

Abstract

Research suggests that perceptual experience of our movements adapts together with movement control when we are the agents of our actions. Is this agency critical for perceptual and motor adaptation? We had participants view cursor feedback during elbow extension–flexion movements when they (1) actively moved their arm, or (2) had their arm passively moved. We probed adaptation of movement perception by having participants report the reversal point of their unseen movement. We probed adaptation of movement control by having them aim to a target. Perception and control of active movement were influenced by both types of exposure, although adaptation was stronger following active exposure. Furthermore, both types of exposure led to a change in the perception of passive movements. Our findings support the notion that perception and control adapt together, and they suggest that some adaptation is due to recalibrated proprioception that arises independently of active engagement with the environment.

Introduction

For most of our daily actions we spend little time consciously thinking about the locations of our various body parts or how to make these body parts do the things we want them to do. Our sensorimotor system seems to effortlessly draw upon visual, proprioceptive, and vestibular feedback, and probably even upon knowledge of its foregoing commands, to update its estimates of limb and body position and then to fluidly guide our actions. The system is also highly flexible, for it can adapt motor output when we encounter novel environments. If the dynamics of a limb are altered or if visual feedback is distorted, accurate performance can be reacquired after repeated exposure to the distortion (e.g., Krakauer et al., 2000, Shadmehr and Mussa-Ivaldi, 1994, Welch, 1986). What processes drive this motor adaptation and what is the relationship between motor adaptation and our perceptual sense of limb position?

One influential model for motor adaptation suggests that the sensorimotor system uses a copy of an outgoing motor command (an efference copy) to make a prediction about forthcoming sensory feedback, a process called forward modeling (Tseng et al., 2007, Wolpert and Ghahramani, 2000). To the extent that the prediction fails to match the actual sensory outcome, motor updating and forward model updating are required. A similar mechanism is thought to underlie our attribution of agency to our actions (Cullen, 2004): If a comparison of predicted sensory feedback to actual sensory feedback produces a match, we attribute the action to ourselves, while a mismatch suggests that an external force has generated, or at least influenced, the sensory feedback.¹

However, forward modeling for adaptation and forward modeling for agency attribution appear to be operating at cross-purposes. For motor adaptation, the greater the discordance between predicted and actual feedback, the greater the error signal should be and the larger the adaptive response. For agency attribution, on the other hand, the greater the sensory mismatch, the less agency should be attributed, and the less relevant the error signal should be for action modification. (Why modify motor commands when the error is not self-generated?) Research on credit assignment during error correction may resolve this apparent conflict by suggesting that agency attribution comes before motor adaptation. Wei and Kording (2009), for instance, have shown that the larger the error between the target and the reach endpoint, the smaller the weighting of the subsequent adaptive response. It has also been shown that gradual introduction of prismatic displacements produces more robust aftereffects than the sudden onset of a large displacement (Michel, Pisella, Prablanc, Rode, & Rossetti, 2007) and, further, that people who are informed about a prismatic shift adapt less than those who are not (Jakobson & Goodale, 1989). These prism studies suggest that the less aware people are of an external perturbation, and, accordingly, the more confident they are in their agency over the action, the stronger the adaptive response.

If the mechanisms for motor adaptation and sense of agency described in the foregoing paragraphs are correct, and if one further allows that a sense of agency over an action is required for motor adaptation to occur, then at least two claims should follow: (1) motor adaptation should only occur for actively generated movements, for only in these cases will an efference copy-based sensory prediction be produced, and (2) one’s sensory expectations about self-generated movement should adapt in tandem with one’s motor output. This second claim follows from the idea that sense of agency (i.e., one’s sense of having caused a movement) relies on congruency between sensory expectation and sensory outcome; if sensory expectation did not adapt, we would not claim agency for the perturbed feedback, and motor adaptation would stall. Thus, if visual feedback is altered during active movement, we should see a modification in both our motor output and our perceptual expectations about the visual feedback.

With respect to the first claim, the necessity of active movement for motor adaptation has not been definitively shown, although the position has been strongly argued and empirically supported by Held and colleagues (Held, 1965, Held and Hein, 1958, Held and Schlank, 1959). It certainly appears that active exposure to a prismatically-induced perturbation increases the amount of adaptation relative to passive exposure (Pick & Hay, 1965), although whether this is due to the presence of efference copy-based predictions or simply to enhanced proprioceptive feedback during active movement is not entirely clear (Welch, 1986). The ability of a patient with proprioceptive loss to adapt to a cursor rotation (Bernier, Chua, Bard, & Franks, 2006), however, does weigh in favor of the notion that efference copy plays a significant role in adaptation during active movement. Still, prism exposure experiments do appear to show that at least some adaptive response can be generated when participants are passively moved during exposure (Pick and Hay, 1965, Singer and Day, 1966; and see Welch (1986), for a review), suggesting that some form of motor adaptation can occur without efference copy. Such adaptation would presumably be the result of proprioceptive recalibration (i.e., a shift in proprioceptively-perceived limb position), which in turn results in modified active movement control.

As for the relationship between one’s perceptual expectations and motor adaptation, only one study, to our knowledge, has directly investigated it. Synofzik, Thier, and Lindner (2006) showed that people’s perception of their own actions and their motor output were modified as a result of exposure to rotated visual feedback of their hand during active movement. The researchers probed changes in perceptual expectations by having people report the outcome of an active movement in the absence of visual feedback. They probed motor adaptation by examining changes in goal-directed action in the absence of visual feedback. They argued that the changed perceptual expectations were a pre-requisite for the changed motor output, for, although they sometimes observed perceptual adaptation without accompanying motor adaptation, the researchers never observed motor adaptation without perceptual adaptation.

In short, Synofzik et al. (2006) have suggested that motor adaptation develops as a result of modification of an adaptable sensory prediction, a sensory prediction that is generated as a result of active movement. In other words, the sensory consequences of movements for which we claim agency are updated, and this updating leads to motor updating. With the present study we wanted to test whether similar sensory updating and motor adaptation might occur for movements over which we do not claim agency. Can sensory updating of active movements occur when visual exposure is constrained to passive movements? And if it can, does this also lead to motor adaptation? To address these questions, we occluded vision of the hand and forearm and projected a cursor over the location of the index finger. We gradually changed the gain between the finger’s motion and the motion of the cursor and then examined how this perturbed visual feedback influenced subsequent perception and control of the limb. In the passive case, we exposed participants to the cursor perturbation while their limb was moved by a motor and then we probed active movement perception and control on trials in which there was no vision of the cursor or the limb. The absence of the cursor on probe trials was important for assessing adaptive influences that were independent of the effects of visual capture. Visual capture, a phenomenon whereby one perceives the limb to be at the same location as a perturbed representation of it, would be expected to occur when the cursor is visible (Hay, Pick, & Ikeda, 1965).

We also investigated a secondary question, one that pertains to actively-guided movements: Might some of the perceptual updating observed by Synofzik et al. (2006) reflect recalibration of proprioception rather than an updated sensory prediction? There is some evidence that exposure to altered visual feedback during active movement recalibrates proprioception (Cressman and Henriques, 2009, Malfait et al., 2008, cf. Smeets et al., 2006, Wong and Henriques, 2009). To address this question we exposed participants to a cursor perturbation during active movements and then probed not only perception and control of active movements but also perception of passive movements. For the sake of completeness and clarity, we lay out below each of the questions that our experiment was designed to address:

Does exposure to visual feedback during passive movement of the limb influence perception of the passively moved limb? Does it influence perception of an actively moved limb? Does it influence goal-directed action?

Does exposure to visual feedback during active movement of the limb influence perception of the passively moved limb? Does it influence perception of an actively moved limb? Does it influence goal-directed action?