Human infants and baboons show the same pattern of handedness for a communicative gesture

To test the role of gestures in the origin of language, we studied hand preferences for grasping or pointing to objects at several spatial positions in human infants and adult baboons. If the roots of language are indeed in gestural communication, we expect that human infants and baboons will present a comparable difference in their pattern of laterality according to task: both should be more right-hand/left-hemisphere specialized when communicating by pointing than when simply grasping objects. Our study is the first to test both human infants and baboons on the same communicative task. Our results show remarkable convergence in the distribution of the two species' hand biases on the two kinds of tasks: In both human infants and baboons, right-hand preference was significantly stronger for the communicative task than for grasping objects. Our findings support the hypothesis that left-lateralized language may be derived from a gestural communication system that was present in the common ancestor of baboons and humans.     

How Precisely Do Bonobos (Pan paniscus) Grasp Small Objects?

The general objective of this study was to compare the precise grasping behavior and intermanual differences in performance between three Pan paniscus and five Homo sapiens in grasping small objects. We compared the temporal pattern of two submovements of consecutive grasping cycles, the (visuomotor) reaching and the (sensorimotor) grasping. Both species were similarly successful in this task, they showed a behavioral right-hand preference and preferred specific types of grips. Bonobos required less time for reaching an object but a much longer time to grasp it than humans did. Thus, the species pursued different strategies. We assumed that this might be due to the different grip techniques. However, grip preferences did not serve a quicker intramanual performance but they pronounced differences between hands. Intermanual differences in timing were restricted to the reaching part and more strongly in bonobos than in humans. However, the right hand need not necessarily perform quicker. As in the case of humans, we assume that attentional cues were focused more on preparing a proper grip with the right hand than on a quick performance. However, strong intermanual differences in bonobos may indicate an overall stronger neuronal asymmetry in the motor organization of the finger musculature that prepare a proper grip than is true of humans.     

The Effects of Visual Control and Distance in Modulating Peripersonal Spatial Representation

In the presence of vision, finalized motor acts can trigger spatial remapping, i.e., reference frames transformations to allow for a better interaction with targets. However, it is yet unclear how the peripersonal space is encoded and remapped depending on the availability of visual feedback and on the target position within the individual’s reachable space, and which cerebral areas subserve such processes. Here, functional magnetic resonance imaging (fMRI) was used to examine neural activity while healthy young participants performed reach-to-grasp movements with and without visual feedback and at different distances of the target from the effector (near to the hand–about 15 cm from the starting position–vs. far from the hand–about 30 cm from the starting position). Brain response in the superior parietal lobule bilaterally, in the right dorsal premotor cortex, and in the anterior part of the right inferior parietal lobule was significantly greater during visually-guided grasping of targets located at the far distance compared to grasping of targets located near to the hand. In the absence of visual feedback, the inferior parietal lobule exhibited a greater activity during grasping of targets at the near compared to the far distance. Results suggest that in the presence of visual feedback, a visuo-motor circuit integrates visuo-motor information when targets are located farther away. Conversely in the absence of visual feedback, encoding of space may demand multisensory remapping processes, even in the case of more proximal targets.     

Grasping behavior in tufted capuchin monkeys (Cebus apella): grip types and manual laterality for picking up a small food item

This study investigates prehension in 20 tufted capuchins (Cebus apella) in a reaching task requiring individuals to grasp a small food item fixed to a tray. The aim was twofold: 1) to describe capuchins' grasping techniques in detail, focusing on digit movements and on different areas of contact between the grasping fingers; and 2) to assess the relationship between grip types and manual laterality in this species. Capuchins picked up small food items using a wide variety of grips. In particular, 16 precision grip variants and 4 power grip variants were identified. The most frequently used precision grip involved the distal lateral areas of the thumb and the index finger, while the most preferred kind of power grip involved the thumb and the palm, with the thumb being enclosed by the other fingers. Immature capuchins picked up small food items using power grips more often than precision grips, while adult individuals exhibited no significant preference for either grip type. The analysis performed on the time capuchins took to grasp the food and withdraw it from the tray hole revealed that 1) precision grips were as efficient as power grips; 2) for precision grips, the left hand was faster than the right hand; and 3) for power grips, both hands were equally quick. Hand preference analysis, based on the frequency for the use of either hand for grasping actions, revealed no significant hand bias at group level. Likewise, there was no significant relationship between grip type and hand preference.     

Effects of Visual Cues of Object Density on Perception and Anticipatory Control of Dexterous Manipulation

Anticipatory force planning during grasping is based on visual cues about the object’s physical properties and sensorimotor memories of previous actions with grasped objects. Vision can be used to estimate object mass based on the object size to identify and recall sensorimotor memories of previously manipulated objects. It is not known whether subjects can use density cues to identify the object’s center of mass (CM) and create compensatory moments in an anticipatory fashion during initial object lifts to prevent tilt. We asked subjects (n = 8) to estimate CM location of visually symmetric objects of uniform densities (plastic or brass, symmetric CM) and non-uniform densities (mixture of plastic and brass, asymmetric CM). We then asked whether subjects can use density cues to scale fingertip forces when lifting the visually symmetric objects of uniform and non-uniform densities. Subjects were able to accurately estimate an object’s center of mass based on visual density cues. When the mass distribution was uniform, subjects could scale their fingertip forces in an anticipatory fashion based on the estimation. However, despite their ability to explicitly estimate CM location when object density was non-uniform, subjects were unable to scale their fingertip forces to create a compensatory moment and prevent tilt on initial lifts. Hefting object parts in the hand before the experiment did not affect this ability. This suggests a dichotomy between the ability to accurately identify the object’s CM location for objects with non-uniform density cues and the ability to utilize this information to correctly scale their fingertip forces. These results are discussed in the context of possible neural mechanisms underlying sensorimotor integration linking visual cues and anticipatory control of grasping.     

Visual coding for action violates fundamental psychophysical principles

According to Weber's law, a basic perceptual principle of psychological science, sensitivity to changes along a given physical dimension decreases when stimulus intensity increases [1]. In other words, the ‘just noticeable difference’ (JND) for weaker stimuli is smaller — hence resolution power is greater — than that for stronger stimuli on the same sensory continuum. Although Weber's law characterizes human perception for virtually all sensory dimensions, including visual length [2] and [3], there have been no attempts to test its validity for visually guided action. For this purpose, we asked participants to either grasp or make perceptual size estimations for real objects varying in length. A striking dissociation was found between grasping and perceptual estimations: in the perceptual conditions, JND increased with physical size in accord with Weber's law; but in the grasping condition, JND was unaffected by the same variation in size of the referent objects. Therefore, Weber's law was violated for visually guided action, but not for perceptual estimations. These findings document a fundamental difference in the way that object size is computed for action and for perception and suggest that the visual coding for action is based on absolute metrics even at a very basic level of processing.     

Effects of the Ebbinghaus illusion on different behaviors: one- and two-handed grasping; one- and two-handed manual estimation; metric and comparative judgment

Many studies have suggested that visually-guided action is largely immune to the effects of several pictorial illusions that strongly influence perceptual judgments. The judgments in these experiments, however, have usually involved comparisons of multiple elements within a display, whereas the visually-guided actions have typically involved a pincer grip directed to only one display element. The three experiments presented here assess the influence of this confound on the perception versus action illusion dissociation. In general, the studies suggest (a) that the confound affects perceptual judgment but not grasping or manual estimation, and (b) that difficult visuomotor tasks are more affected by the Ebbinghaus illusion than easier tasks. In Experiment 1, participants reached for or made judgments about plastic disks placed in the center of the Ebbinghaus illusion display. Some participants reached for or made judgments about only the disk on the right, whereas others reached for or judged both disks simultaneously. A large effect of the illusion was found for grasping and comparative judgment, but not for manual estimation or metric judgment. In Experiment 2, the disks were elevated slightly to make gripping the targets easier, and the effects of the illusion on grasping were greatly reduced. For Experiment 3, participants performed the manual estimation task while the hands were placed in view, on the surface of the table, and the effects of the illusion were significantly increased. Taken together, the experiments indicate that task difficulty and hand visibility affect whether a task will be influenced by pictorial illusions or not. One- and two-handed grasping seem to be affected approximately equally.     

Grasping the past. delay can improve visuomotor performance.

"Optic ataxia" is caused by damage to the human posterior parietal cortex (PPC). It disrupts all components of a visually guided prehension movement, not only the transport of the hand toward an object's location, but also the in-flight finger movements pretailored to the metric properties of the object. Like previous cases, our patient (I.G.) was quite unable to open her handgrip appropriately when directly reaching out to pick up objects of different sizes. When first tested, she failed to do this even when she had previewed the target object 5 s earlier. Yet despite this deficit in "real" grasping, we found, counterintuitively, that I.G. showed good grip scaling when "pantomiming" a grasp for an object seen earlier but no longer present. We then found that, after practice, I.G. became able to scale her handgrip when grasping a real target object that she had previewed earlier. By interposing catch trials in which a different object was covertly substituted for the original object during the delay between preview and grasp, we found that I.G. was now using memorized visual information to calibrate her real grasping movements. These results provide new evidence that "off-line" visuomotor guidance can be provided by networks independent of the PPC.     

Grasping Objects with Environmentally Induced Position Uncertainty

Due to noisy motor commands and imprecise and ambiguous sensory information, there is often substantial uncertainty about the relative location between our body and objects in the environment. Little is known about how well people manage and compensate for this uncertainty in purposive movement tasks like grasping. Grasping objects requires reach trajectories to generate object-fingers contacts that permit stable lifting. For objects with position uncertainty, some trajectories are more efficient than others in terms of the probability of producing stable grasps. We hypothesize that people attempt to generate efficient grasp trajectories that produce stable grasps at first contact without requiring post-contact adjustments. We tested this hypothesis by comparing human uncertainty compensation in grasping objects against optimal predictions. Participants grasped and lifted a cylindrical object with position uncertainty, introduced by moving the cylinder with a robotic arm over a sequence of 5 positions sampled from a strongly oriented 2D Gaussian distribution. Preceding each reach, vision of the object was removed for the remainder of the trial and the cylinder was moved one additional time. In accord with optimal predictions, we found that people compensate by aligning the approach direction with covariance angle to maintain grasp efficiency. This compensation results in higher probability to achieve stable grasps at first contact than non-compensation strategies in grasping objects with directional position uncertainty, and the results provide the first demonstration that humans compensate for uncertainty in a complex purposive task.     

Rubber hands feel touch, but not in blind individuals

Psychology and neuroscience have a long-standing tradition of studying blind individuals to investigate how visual experience shapes perception of the external world. Here, we study how blind people experience their own body by exposing them to a multisensory body illusion: the somatic rubber hand illusion. In this illusion, healthy blindfolded participants experience that they are touching their own right hand with their left index finger, when in fact they are touching a rubber hand with their left index finger while the experimenter touches their right hand in a synchronized manner (Ehrsson et al. 2005). We compared the strength of this illusion in a group of blind individuals (n = 10), all of whom had experienced severe visual impairment or complete blindness from birth, and a group of age-matched blindfolded sighted participants (n = 12). The illusion was quantified subjectively using questionnaires and behaviorally by asking participants to point to the felt location of the right hand. The results showed that the sighted participants experienced a strong illusion, whereas the blind participants experienced no illusion at all, a difference that was evident in both tests employed. A further experiment testing the participants' basic ability to localize the right hand in space without vision (proprioception) revealed no difference between the two groups. Taken together, these results suggest that blind individuals with impaired visual development have a more veridical percept of self-touch and a less flexible and dynamic representation of their own body in space compared to sighted individuals. We speculate that the multisensory brain systems that re-map somatosensory signals onto external reference frames are less developed in blind individuals and therefore do not allow efficient fusion of tactile and proprioceptive signals from the two upper limbs into a single illusory experience of self-touch as in sighted individuals.     

Reconstructing mental object representations: a machine vision approach to human visual recognition

This paper introduces a new approach to assess visual representations underlying the recognition of objects. Human performance is modeled by CLARET, a machine learning and matching system, based on inductive logic programming and graph matching principles. The model is applied to data of a learning experiment addressing the role of prior experience in the ontogenesis of mental object representations. Prior experience was varied in terms of sensory modality, i.e. visual versus haptic versus visuohaptic. The analysis revealed distinct differences between the representational formats used by subjects with haptic versus those with no prior object experience. These differences suggest that prior haptic exploration stimulates the evolution of object representations which are characterized by an increased differentiation between attribute values and a pronounced structural encoding.     

Human Left Ventral Premotor Cortex Mediates Matching of Hand Posture to Object Use

Visuomotor transformations for grasping have been associated with a fronto-parietal network in the monkey brain. The human homologue of the parietal monkey region (AIP) has been identified as the anterior part of the intraparietal sulcus (aIPS), whereas the putative human equivalent of the monkey frontal region (F5) is located in the ventral part of the premotor cortex (vPMC). Results from animal studies suggest that monkey F5 is involved in the selection of appropriate hand postures relative to the constraints of the task. In humans, the functional roles of aIPS and vPMC appear to be more complex and the relative contribution of each region to grasp selection remains uncertain. The present study aimed to identify modulation in brain areas sensitive to the difficulty level of tool object - hand posture matching. Seventeen healthy right handed participants underwent fMRI while observing pictures of familiar tool objects followed by pictures of hand postures. The task was to decide whether the hand posture matched the functional use of the previously shown object. Conditions were manipulated for level of difficulty. Compared to a picture matching control task, the tool object – hand posture matching conditions conjointly showed increased modulation in several left hemispheric regions of the superior and inferior parietal lobules (including aIPS), the middle occipital gyrus, and the inferior temporal gyrus. Comparison of hard versus easy conditions selectively modulated the left inferior frontal gyrus with peak activity located in its opercular part (Brodmann area (BA) 44). We suggest that in the human brain, vPMC/BA44 is involved in the matching of hand posture configurations in accordance with visual and functional demands.     

Manual Function in Cebus apella. Digital Mobility,Preshaping, and Endurance in Repetitive Grasping

Manual dexterity varies across species of primates in accord with hand morphology and degree of fine motor control of the digits. Platyrrhine monkeys achieve less direct opposition between thumb and index finger than that of catarrhine primates, and many of them typically whole-hand grip. However, tufted capuchins (Cebus apella), exhibit a degree of independent control of the digits and effective thumb–forefinger opposition. We report how capuchins prehended small objects, with particular attention to the form of sequential fine movements of the fingers, choice of hand, and differences between the two hands in the temporal properties of reaching and grasping. We compare these actions across tasks with differing demands for fine motor control. For tasks that required all the digits to flex in synchrony, capuchins displayed smooth, fast, and efficient reach-to-grasp movements and a higher endurance than for tasks requiring more complex digital coordination. These latter tasks induced a slightly differentiated preshaping of the hand when approaching the objects, indicating preparation for grasping in advance of contact with the object. A right-hand preponderance for complex digital coordination was evident. The monkeys coordinated their fingers rather poorly at the substrate, and they took longer to achieve control of the objects when complex coordination was required than when simultaneous flexion was sufficient. We conclude that precise finger coordination is more effortful and less well coordinated, and the coordination is less lateralized, in capuchins than in catarrhine primates.     

Hand Preference for a Novel Bimanual Coordinated Task During Termite Feeding in Wild Western Gorillas (<Emphasis Type="Italic">Gorilla gorilla gorilla</Emphasis>)

Although the level of handedness in humans varies cross-culturally, humans are generally described as right-handed, which has been considered a uniquely human trait. Recently, captive chimpanzees (Pan troglodytes) have been shown to exhibit right-hand preference when performing bimanual but not unimanual tasks. Less clear is whether this pattern also occurs in wild chimpanzees and other African apes. Using videos (N = 49) of six wild western gorillas (Gorilla gorilla gorilla) feeding on termites at the Mondika Research Center (Republic of Congo), we tested whether they exhibit hand preference when performing unimanual, i.e., reaching for termite mound pieces; bimanual, i.e., “termite tapping”: rhythmically shaking a piece of termite mound with the dominant hand and collecting the termites in the other hand tasks; or hand transfer prior to bimanual tasks, i.e., transferring a piece of termite mound from one hand to the other. All individuals exhibited exclusive hand preference when performing the bimanual tasks, with five of six gorillas preferring the right hand. Conversely, most individuals did not show any manual preference during the unimanual task. In addition, hand preference during hand transfer revealed clear hand dominance of similar strength and direction of those shown for the bimanual task, suggesting that this measure is as sensitive as the bimanual task itself. Thus, we propose “termite feeding” as a novel task to be considered in future hand-preference studies in wild western gorillas. Our results are in concordance with those for chimpanzees and captive gorillas showing hemispheric specialization for bimanual actions in apes.     

Dissociation between ventral and dorsal fMRI activation during object and action recognition

Neuropsychological case studies suggest the existence of two functionally separate visual streams: the ventral pathway, central for object recognition; and the dorsal pathway, engaged in visually guided actions. However, a clear dissociation between the functions of the two streams has not been decisively shown in intact humans. In this study, we demonstrate dissociation between dorsal and ventral fMRI activation patterns during observation of object manipulation video clips. Parietal areas, such as anterior intraparietal sulcus (aIPS) display grasp viewing-dependent adaptation (i.e., fMR adaptation during repeated viewing of the same object-grasping movement) as well as a contralateral preference for the viewed manipulating hand. Ventral regions, such as the fusiform gyrus, show similar characteristics (i.e., adaptation, contralateral preference), but these depend on object identity. Our results support the hypothesized functional specialization in the visual system and suggest that parietal areas (such as aIPS) are engaged in action recognition, as well as in action planning.     

Simulation modifies prehension: evidence for a conjoined representation of the graspable features of an object and the action of grasping it

Movement formulas, engrams, kinesthetic images and internal models of the body in action are notions derived mostly from clinical observations of brain-damaged subjects. They also suggest that the prehensile geometry of an object is integrated in the neural circuits and includes the object's graspable characteristics as well as its semantic properties. In order to determine whether there is a conjoined representation of the graspable characteristics of an object in relation to the actual grasping, it is necessary to separate the graspable (low-level) from the semantic (high-level) properties of the object. Right-handed subjects were asked to grasp and lift a smooth 300-g cylinder with one hand, before and after judging the level of difficulty of a "grasping for pouring" action, involving a smaller cylinder and using the opposite hand. The results showed that simulated grasps with the right hand exert a direct influence on actual motor acts with the left hand. These observations add to the evidence that there is a conjoined representation of the graspable characteristics of the object and the biomechanical constraints of the arm.     

Order Parameter Dynamics of Body-scaled Hysteresis and Mode Transitions in Grasping Behavior

Several experimental studies have shown that human grasping behavior exhibits a transition from one-handed to two-handed grasping when to-be-grasped objects become larger and larger. The transition point depends on the relative size of objects measured in terms of human body-scales. Most strikingly, the transitions between the two different behavioral ‘modes’ of grasping exhibit hysteresis. That is, one-to-two hand transitions and two-to-one hand transitions occur at different relative object sizes when objects are scaled up or down in size. In our study we approach body-scaled hysteresis and mode transitions in grasping by exploiting the notion that human behavior in general results from self-organization and satisfies appropriately-defined order parameter equations. To this end, grasping transitions and grasping hysteresis are discussed from a theoretical perspective in analogy to cognitive processes defined by Haken’s neural network model for pattern recognition. In doing so, issues such as the exclusivity of grasping modes, biomechanical constraints, mode-mode interactions, single subject behavior and population behavior are explored.     

Preserved functional specialization for spatial processing in the middle occipital gyrus of the early blind

The occipital cortex (OC) of early-blind humans is activated during various nonvisual perceptual and cognitive tasks, but little is known about its modular organization. Using functional MRI we tested whether processing of auditory versus tactile and spatial versus nonspatial information was dissociated in the OC of the early blind. No modality-specific OC activation was observed. However, the right middle occipital gyrus (MOG) showed a preference for spatial over nonspatial processing of both auditory and tactile stimuli. Furthermore, MOG activity was correlated with accuracy of individual sound localization performance. In sighted controls, most of extrastriate OC, including the MOG, was deactivated during auditory and tactile conditions, but the right MOG was more activated during spatial than nonspatial visual tasks. Thus, although the sensory modalities driving the neurons in the reorganized OC of blind individuals are altered, the functional specialization of extrastriate cortex is retained regardless of visual experience.     

Manual lateralization in early primates: a comparison of two mouse lemur species

In humans, 90% of the population is right handed. Although population hand preference has been found in some primate species, the evolution of manual lateralization in primates is not yet clear. To gain insight into manual lateralization of ancestral primates, we studied hand usage in unspecialized quadrupedal, nocturnal lemurs, using a large sample size. We compared two closely related mouse lemur species to explore the variation of hand preference within the same genus. We tested 44 gray mouse lemurs and 19 Goodman's mouse lemurs in a forced food grasping task. The tests were videotaped. Measures of hand preference (i.e. the hand that is spontaneously chosen for a specific task) and successful hand usage (i.e. the hand that is successful in completing a specific task) were taken to explore manual lateralization. Both species showed manual lateralization at an individual, but not at a population level. Goodman's mouse lemurs showed stronger individual hand preferences than gray mouse lemurs. This suggests that strength in hand preference is variable within the same genus. No sex and age effects were found. The hand preference of offspring was negatively correlated to that of their mothers, but not correlated to that of their fathers. Thus, no clear genetic effect can be derived from these results. In the Goodman's mouse lemurs, hand preference increased with increasing task experience. However, successful hand usage was not affected by task experience, suggesting that successful hand usage is a more stable measurement for manual lateralization than hand preference.