Abstract spatial, but not body-related, visual information guides bimanual coordination

www.nature.com/scientificreports OPEN Received: 18 April 2017 Accepted: 19 November 2017 Published: xx xx xxxx Abstract spatial, but not bodyrelated, visual information guides bimanual coordination Janina Brandes1, Farhad Rezvani1 & Tobias Heed1,2 Visual spatial information is paramount in guiding bimanual coordination, but anatomical factors, too, modulate performance in bimanual tasks. Vision conveys not only abstract spatial information, but also informs about body-related aspects such as posture. Here, we asked whether, accordingly, visual information induces body-related, or merely abstract, perceptual-spatial constraints in bimanual movement guidance. Human participants made rhythmic, symmetrical and parallel, bimanual index finger movements with the hands held in the same or different orientations. Performance was more accurate for symmetrical than parallel movements in all postures, but additionally when homologous muscles were concurrently active, such as when parallel movements were performed with differently rather than identically oriented hands. Thus, both perceptual and anatomical constraints were evident. We manipulated visual feedback with a mirror between the hands, replacing the image of the right with that of the left hand and creating the visual impression of bimanual symmetry independent of the right hand’s true movement. Symmetrical mirror feedback impaired parallel, but improved symmetrical bimanual performance compared with regular hand view. Critically, these modulations were independent of hand posture and muscle homology. Thus, visual feedback appears to contribute exclusively to spatial, but not to body-related, anatomical movement coding in the guidance of bimanual coordination. Whether we type on a keyboard, applaud, or ride a bike – bimanual coordination is crucial in many of our everyday activities. Therefore, the principles that guide bimanual coordination have received much interest, not least to inform treatment to restore regular bimanual function in clinical settings. Beyond therapeutic considerations, coordinative action can be viewed as an ecologically valid model to understand the principles of movement planning1. Accordingly, experiments have studied the factors that constrain bimanual movement execution. A prominent and consistent finding has been that humans can perform symmetrical movements – with symmetry usually defined relative to the sagittal body midline – with higher precision and at higher speeds than parallel movements2–4. During symmetrical movements, the two effectors move towards opposite sides of space; for instance, one hand moves to the right while the other concurrently moves to the left. Conversely, parallel movements implicate movements towards the same direction of space; for instance, both hands synchronously move to the left or to the right. The symmetry bias has been demonstrated across a variety of effectors and movement types, such as finger flexion and extension5,6, finger tapping7, wrist movements2, line drawing8, elbow flexion and extension9, and circling arm movements10. Given its stability across many qualitatively different movements, symmetry is thought to constitute a general organizing principle of bimanual coordination11. One popular experimental paradigm has been finger abduction and adduction, that is, sideways movements of the two index fingers with the hands held palm down. Participants perform these movements rhythmically, and we therefore refer to this task as “finger oscillations”. With the palms down, movement accuracy is high when both fingers are abducted at the same time, that is, when fingers are moved in symmetry. Accuracy is lower when one finger is abducted while the other one is concurrently adducted, that is, when fingers are moved in parallel3. The mechanisms underlying the symmetry bias have been under debate. Early reports suggested that it originates from anatomical constraints within the motor system, that is, from interactions rooted in muscle synergies caused by hemispheric crosstalk2,3,12. Muscle synergies may arise through reciprocal connections between the 1 Faculty of Psychology and Human Movement Science, University of Hamburg, Hamburg, Germany. 2Faculty of Psychology and Sports Science and Center of Excellence in Cognitive Interaction Technology, Bielefeld University, Bielefeld, Germany. Correspondence and requests for materials should be addressed to T.H. (email: tobias.heed@ uni-bielefeld.de) SCIEnTIFIC RepOrTS | 7: 16732 | DOI:10.1038/s41598-017-16860-x 1 www.nature.com/scientificreports/ cortical regions that control homologous muscles of the two body sides and result in preferred activation of homologous limb movements. In this view, symmetrical movements are stable because they involve the same muscles in both limbs, allowing efficient integration of contra- and ipsilateral motor signals. In contrast, parallel finger movements involve different muscles in the two limbs, resulting in reduced stability due to ongoing interference from conflicting ipsi- and contralateral muscle commands13. However, others have suggested that, instead, the symmetry bias originates from interactions rooted in perception7,14. The key finding supporting this proposal was that the symmetry bias prevailed when participants performed oscillatory finger movements with the two hands held in opposite orientations, that is, one palm facing up and the other down. In this situation, symmetrical movements involve non-homologous muscles, whereas parallel movements are achieved through homologous muscles. The persistent advantage of symmetrical over parallel movements despite a reversal of the muscles involved in the bimanual movement is at odds with the idea that muscle synergies alone are responsible for the symmetry bias7,13,14. Several studies have suggested that the previous findings of external vs. anatomical symmetry constraints are not a contradiction, but that both factors jointly influence coordination behavior1,9,15,16. According to this view, anatomical and external contributions flexibly determine bimanual coordination with their relative weighting depending on context and task demands13. In line with this proposal, we recently observed that the perceptual symmetry bias in the finger oscillation task coexisted with an advantage for using homologous muscles17, rather than relying on perceptual coding alone, as had been previously suggested7. Whereas the role of perceptual and anatomical codes has, thus, been firmly established, it is less clear what kind of perceptual information these biases are based on. The prevalent experimental approach has been to contrast vision with posture, and to interpret performance biases induced by vision as evidence for perceptually induced, spatial guidance, and biases induced by posture as evidence for anatomical constraints of movement coordination7,12. Yet, visual information transports not just abstract spatial information, but also info (...truncated)