Research Article: When Kinesthesia Becomes Visual: A Theoretical Justification for Executing Motor Tasks in Visual Space

Date Published: July 5, 2013

Publisher: Public Library of Science

Author(s): Michele Tagliabue, Joseph McIntyre, Robert J. van Beers.


Several experimental studies in the literature have shown that even when performing purely kinesthetic tasks, such as reaching for a kinesthetically felt target with a hidden hand, the brain reconstructs a visual representation of the movement. In our previous studies, however, we did not observe any role of a visual representation of the movement in a purely kinesthetic task. This apparent contradiction could be related to a fundamental difference between the studied tasks. In our study subjects used the same hand to both feel the target and to perform the movement, whereas in most other studies, pointing to a kinesthetic target consisted of pointing with one hand to the finger of the other, or to some other body part. We hypothesize, therefore, that it is the necessity of performing inter-limb transformations that induces a visual representation of purely kinesthetic tasks. To test this hypothesis we asked subjects to perform the same purely kinesthetic task in two conditions: INTRA and INTER. In the former they used the right hand to both perceive the target and to reproduce its orientation. In the latter, subjects perceived the target with the left hand and responded with the right. To quantify the use of a visual representation of the movement we measured deviations induced by an imperceptible conflict that was generated between visual and kinesthetic reference frames. Our hypothesis was confirmed by the observed deviations of responses due to the conflict in the INTER, but not in the INTRA, condition. To reconcile these observations with recent theories of sensori-motor integration based on maximum likelihood estimation, we propose here a new model formulation that explicitly considers the effects of covariance between sensory signals that are directly available and internal representations that are ‘reconstructed’ from those inputs through sensori-motor transformations.

Partial Text

A number of previous studies have suggested that the CNS plans and executes targeted movements of the hand using a visual representation of the movement even when the target is presented kinesthetically (e.g. pointing with one hand to the other) and even when no visual feedback about the hand is allowed [1]–[5]. This is in apparent contrast with our own studies on human sensori-motor integration [6], [7] in which we observed that if subjects were asked to align their hidden hand to the orientation of a kinesthetically felt target, they completely ignored the information related to the visual scene, indicating that the brain executes purely kinesthetic tasks (K-K: kinesthetic target and kinesthetic response) without using a visual representation of the movement. This apparent contradiction, however, could be related to a fundamental difference between the motor tasks that the subjects were asked to perform in these different sets of studies. Whilst in our study subjects felt and reproduced the target position/orientation with the same hand, participants in the other aforementioned studies had to sense the target with the left hand or with a foot, hidden under a table, and reproduce its position with the right hand. Based on this observation, we postulated that the use of a visual representation of the movement could be related to the necessity of performing an inter-limb transformation of the kinesthetic information.

Figure 3 shows for the INTRA and INTER-manual conditions the average responses to each target orientation in trials without conflict, which do not differ appreciably between the two experimental conditions: statistical analyses on the aligning errors showed no significant effect of the experimental condition (ANOVA F(1,15) = 2.13, p = 0.17) or interactions between condition and target orientation (ANOVA F(6,90) = 0.92, p = 0.49). On the other hand, clear differences can be observed in Figure 4 for the responses in the trials with conflict: in the INTRA condition the responses were not consistently deviated by the conflict, in the INTER condition conflict caused the responses to all target orientations to be deviated in the same direction. These latter observations were confirmed by the statistical analysis of the global deviation of the responses. Figure 5A shows that in the INTER-manual condition responses were significantly deviated by the inclination of the visual surround (one-tailed t-test with respect to 0: t(15) = 2.27, p = 0.02), whilst no statistical difference from the null deviation could be detected in the INTRA-manual condition (one-tailed t-test with respect to 0: t(15) = −0.37, p0.25). The differing effects between the two experimental conditions was confirmed by a significant difference between the INTRA- and INTER-manual conditions (ANOVA F(1,15) = 8.81, p = 0.009). The comparison of the response variability between the two experimental conditions, reported in Figure 5B, shows that subjects were more precise when they had to reproduce an orientation felt with the same hand than with the other hand (ANOVA F(1,15) = 10.38, p = 0.005).

The results show that, for a purely kinesthetic task of reproducing a kinesthetically sensed orientation with an unseen hand (K-K condition), the brain gives significant weight to visual information when the task requires an inter-limb information transmission (INTER condition), but not when subjects memorized and responded with the same hand (INTRA condition). The lack of a significant effect of visual information in the INTRA condition matches our previous results [6] and is coherent with studies of reaching movements in which subjects also used the same arm to feel the target and to reproduce its remembered position [26]–[29]. The use of visual encoding in otherwise purely kinesthetic pointing tasks has nevertheless been observed in a number of studies that have required comparing one limb to another [1], [4], [5]. Our results suggest that the use of visual encoding in these studies was most likely due to the bilateral nature of the task and that responses would have been different if the subjects had used the same limb to feel the target and to reproduce its position.