Comparing Natural and Constrained Movements: New Insights into the Visuomotor Control of Grasping

PLOS ONE, Oct 2007

Background Neurophysiological studies showed that in macaques, grasp-related sensorimotor transformations are accomplished in a circuit connecting the anterior intraparietal sulcus (area AIP) with premotor area F5. Single unit recordings of macaque indicate that activity of neurons in this circuit is not simply linked to any particular object. Instead, responses correspond to the final hand configuration used to grasp the object. Although a human homologue of such a circuit has been identified, its role in planning and controlling different grasp configurations has not been decisively shown. We used functional magnetic resonance imaging to explicitly test whether activity within this network varies depending on the congruency between the adopted grasp and the grasp called by the stimulus. Methodology/Principal Findings Subjects were requested to reach towards and grasp a small or a large stimulus naturally (i.e., precision grip, involving the opposition of index finger and thumb, for a small size stimulus and a whole hand grasp for a larger stimulus) or with an constrained grasp (i.e., a precision grip for a large stimulus and a whole hand grasp for a small stimulus). The human anterior intraparietal sulcus (hAIPS) was more active for precise grasping than for whole hand grasp independently of stimulus size. Conversely, both the dorsal premotor cortex (dPMC) and the primary motor cortex (M1) were modulated by the relationship between the type of grasp that was adopted and the size of the stimulus. Conclusions/Significance The demonstration that activity within the hAIPS is modulated according to different types of grasp, together with the evidence in humans that the dorsal premotor cortex is involved in grasp planning and execution offers a substantial contribution to the current debate about the neural substrates of visuomotor grasp in humans.

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Comparing Natural and Constrained Movements: New Insights into the Visuomotor Control of Grasping

Castiello U (2007) Comparing Natural and Constrained Movements: New Insights into the Visuomotor Control of Grasping. PLoS ONE 2(10): e1108. doi:10.1371/journal.pone.0001108 Comparing Natural and Constrained Movements: New Insights into the Visuomotor Control of Grasping Chiara Begliomini 0 1 Andrea Caria 0 1 Wolfgang Grodd 0 1 Umberto Castiello 0 1 0 Academic Editor: Edwin Robertson, Harvard Medical School , United States of America 1 1 Centre for Mind and Brain Sciences, University of Trento , Rovereto , Italy , 2 Institute for Medical Psychology, Eberhard-Karls University of Tuebingen , Tuebingen, Germany , 3 Section Experimental MRI of the CNS, Department of Neuroradiology, Tuebingen University Hospital , Tuebingen, Germany , 4 Department of General Psychology, University of Padua , Padua , Italy , 5 Department of Psychology, Royal Holloway, University of London , Egham , United Kingdom Background. Neurophysiological studies showed that in macaques, grasp-related sensorimotor transformations are accomplished in a circuit connecting the anterior intraparietal sulcus (area AIP) with premotor area F5. Single unit recordings of macaque indicate that activity of neurons in this circuit is not simply linked to any particular object. Instead, responses correspond to the final hand configuration used to grasp the object. Although a human homologue of such a circuit has been identified, its role in planning and controlling different grasp configurations has not been decisively shown. We used functional magnetic resonance imaging to explicitly test whether activity within this network varies depending on the congruency between the adopted grasp and the grasp called by the stimulus. Methodology/Principal Findings. Subjects were requested to reach towards and grasp a small or a large stimulus naturally (i.e., precision grip, involving the opposition of index finger and thumb, for a small size stimulus and a whole hand grasp for a larger stimulus) or with an constrained grasp (i.e., a precision grip for a large stimulus and a whole hand grasp for a small stimulus). The human anterior intraparietal sulcus (hAIPS) was more active for precise grasping than for whole hand grasp independently of stimulus size. Conversely, both the dorsal premotor cortex (dPMC) and the primary motor cortex (M1) were modulated by the relationship between the type of grasp that was adopted and the size of the stimulus. Conclusions/Significance. The demonstration that activity within the hAIPS is modulated according to different types of grasp, together with the evidence in humans that the dorsal premotor cortex is involved in grasp planning and execution offers a substantial contribution to the current debate about the neural substrates of visuomotor grasp in humans. - INTRODUCTION The highly developed ability of the hand to grasp and manipulate objects under precise visual control is one of the key features of the human motor system. The skilled use of the hand is fundamental to the technological, social and cultural progress of the human species [13]. The study of grasping was advanced by Napiers landmark work on precision and power grips [3]. According to Napier [3] there are only two main prehensile patterns, namely precision and power grips. The power grip (termed here as whole hand grasp; WHG) is a palmar opposition grasp in which all digits are flexed around the object to provide high stability. The precision grip (PG) has developed in primates for the manipulation of small objects with the tips of the thumb and fingers. In recent years, there have been significant advances in our understanding of the neural mechanisms underlying the transformation of visual information about an object in the outside world into motor commands that allow the hand to be shaped for efficient grasp of the object. The huge variation in the shape, size and texture of the objects we must daily interact in a skillful and precise manner demands that this transformation provides a highly specific and selective matching of the objects properties to the motor commands for grasp and manipulation. An important step forward in understanding how the brain controls grasp comes from the studies in which single neurons were recorded during naturalistic reach-to-grasp actions [48]. These studies showed that in macaques, grasp-related sensorimotor transformations are accomplished in a circuit connecting the anterior-most region within the lateral bank of the intraparietal sulcus (area AIP) with the ventral premotor area F5. It is postulated that AIP may furnish area F5 with visual signals of objects to aid in the selection of grasp configurations that are appropriate for their intrinsic attributes (e.g., size). The AIP-F5 network can then use the physical object properties to select the suitable motor schema according to the goal of the action [9]. An important feature of this network is that different neuronal populations code for specific types of hand shaping s (...truncated)


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Chiara Begliomini, Andrea Caria, Wolfgang Grodd, Umberto Castiello. Comparing Natural and Constrained Movements: New Insights into the Visuomotor Control of Grasping, PLOS ONE, 2007, 10, DOI: 10.1371/journal.pone.0001108