Article

Two hands, one perception:How bimanual haptic information is combined by the brain

Department of Robotics, Brain and Cognitive Sciences, Istituto Italiano di Tecnologia, Genova, Italy.
Journal of Neurophysiology (Impact Factor: 2.89). 01/2012; 107(2):544-50. DOI: 10.1152/jn.00756.2010
Source: PubMed

ABSTRACT

Humans routinely use both of their hands to gather information about shape and texture of objects. Yet, the mechanisms of how the brain combines haptic information from the two hands to achieve a unified percept are unclear. This study systematically measured the haptic precision of humans exploring a virtual curved object contour with one or both hands to understand if the brain integrates haptic information from the two hemispheres. Bayesian perception theory predicts that redundant information from both hands should improve haptic estimates. Thus exploring an object with two hands should yield haptic precision that is superior to unimanual exploration. A bimanual robotic manipulandum passively moved the hands of 20 blindfolded, right-handed adult participants along virtual curved contours. Subjects indicated which contour was more "curved" (forced choice) between two stimuli of different curvature. Contours were explored uni- or bimanually at two orientations (toward or away from the body midline). Respective psychophysical discrimination thresholds were computed. First, subjects showed a tendency for one hand to be more sensitive than the other with most of the subjects exhibiting a left-hand bias. Second, bimanual thresholds were mostly within the range of the corresponding unimanual thresholds and were not predicted by a maximum-likelihood estimation (MLE) model. Third, bimanual curvature perception tended to be biased toward the motorically dominant hand, not toward the haptically more sensitive left hand. Two-handed exploration did not necessarily improve haptic sensitivity. We found no evidence that haptic information from both hands is integrated using a MLE mechanism. Rather, results are indicative of a process of "sensory selection", where information from the dominant right hand is used, although the left, nondominant hand may yield more precise haptic estimates.

Download full-text

Full-text

Available from: Lorenzo Masia, Jan 18, 2016
  • Source
    • "Studies of information processing by the nervous system have found Bayesian models to often be consistent with empirical data, for a rather broad set of behaviours that includes infant cognition [3], language [4] [5], face perception [6], rhythm perception [7], haptics [8], and multi-signal integration [2]. It is thus an important current theory for sensory-motor neuroscience and motor control. "
    [Show abstract] [Hide abstract]
    ABSTRACT: Information about the position of an object that is held in both hands, such as a golf club or a tennis racquet, is transmitted to the human central nervous system from peripheral sensors in both left and right arms. How does the brain combine these two sources of information? Using a robot to move participant's passive limbs, we performed psychophysical estimates of proprioceptive function for each limb independently, and again when subjects grasped the robot handle with both arms. We compared empirical estimates of bimanual proprioception to several models from the sensory integration literature: some that propose a combination of signals from the left and right arms (such as a Bayesian maximum-likelihood estimate), and some that propose using unimanual signals alone. Our results are consistent with the hypothesis that the nervous system both has knowledge of, and uses the limb with the best proprioceptive acuity for bimanual proprioception. Surprisingly, a Bayesian model that postulates optimal combination of sensory signals could not predict empirically observed bimanual acuity. These findings suggest that while the central nervous system seems to have information about the relative sensory acuity of each limb, it uses this information in a rather rudimentary fashion, essentially ignoring information from the less reliable limb.
    Preview · Article · Dec 2013 · Journal of Neurophysiology
  • Source
    • "In addition, no significant effect was observed in the Handedness × Hand × Task type three-way interaction, indicating that the non-dominant arm/hemisphere superiority was irrespective as to whether the task was performed unimanually or bimanually. This finding contradicts the prediction that sensory selection or sensory gating would be biased towards the dominant side when individuals are required to perform bimanual pinch movement discrimination tasks concurrently [37], and that the hemisphere advantage observed in unimanual tasks would not extend to different bimanual tasks [20]. Rather, the results here support the Goble et al. hypothesis of functional differences between the preferred and non-preferred limbs during bilateral tasks [15]. "
    [Show abstract] [Hide abstract]
    ABSTRACT: It has been proposed that asymmetry between the upper limbs in the utilization of proprioceptive feedback arises from functional differences in the roles of the preferred and non-preferred hands during bimanual tasks. The present study investigated unimanual and bimanual proprioceptive performance in right- and left-handed young adults with an active finger pinch movement discrimination task. With visual information removed, participants were required to make absolute judgments about the extent of pinch movements made to physical stops, either by one hand, or by both hands concurrently, with the sequence of presented movement extents varied randomly. Discrimination accuracy scores were derived from participants' responses using non-parametric signal detection analysis. Consistent with previous findings, a non-dominant hand/hemisphere superiority effect was observed, where the non-dominant hands of right- and left-handed individuals performed overall significantly better than their dominant hands. For all participants, bimanual movement discrimination scores were significantly lower than scores obtained in the unimanual task. However, the magnitude of the performance reduction, from the unimanual to the bimanual task, was significantly greater for left-handed individuals. The effect whereby bimanual proprioception was disproportionately affected in left-handed individuals could be due to enhanced neural communication between hemispheres in left-handed individuals leading to less distinctive separation of information obtained from the two hands in the cerebral cortex.
    Full-text · Article · Mar 2013 · Neuroscience Letters
  • Source
    • "While there is substantial evidence that many biological systems including humans use efference copy mechanisms to control a wide range of behaviors and functions (Kawato et al. 1987;Jordan and Rumelhart 1992;Miall et al. 1993;Wolpert and Kawato 1998;Kawato 1999), the neural mechanisms that link motor commands and sensory data and how these mechanisms develop in human ontogenesis have not yet been completely delineated. To investigate the development of haptic perception and the underlying use of internal and external feedback, we employed a curvature perception paradigm that has been widely used in adult studies (Davidson 1972;Gordon and Morison 1982;Konczak et al. 2008;Sciutti et al. 2010;Squeri et al. 2012). Using a robotic manipulandum, we created boundary forces resembling a virtual curved contour. "
    [Show abstract] [Hide abstract]
    ABSTRACT: Neural processes of sensory-motor- and motor-sensory integration link perception and action, forming the basis for human interaction with the environment. Haptic perception, the ability to extract object features through action, is based on these processes. To study the development of motor-sensory integration, children judged the curvature of virtual objects after exploring them actively or while guided passively by a robot. Haptic acuity reached adult levels only at early adolescence. Unlike in adults, haptic precision in children was consistently lower during active exploration when compared to passive motion. Thus, the exploratory movements themselves constitute a form of noise for the developing haptic system that younger brains cannot compensate until mid-adolescence. Computationally, this is consistent with a noisy efference copy mechanism producing imprecise predicted sensory feedback, which compromises haptic precision in children, while the mature mechanism aids the adult brain to account for the effect of self-generated motion on perception.
    Full-text · Article · Nov 2012 · Experimental Brain Research
Show more