Prehension, the act of reaching to grasp an object, is our most precious behaviour. It is highly evolved in primates and allows us to manipulate objects, acquire and prepare food for eating, construct and use tools, and communicate through gestures, written words, and creative art. Not surprisingly, it is the behavior that people with sensorimotor disorders most want restored. Its neural basis, however, is highly complex, involves distributed pathways that traverse most brain regions, and is not well understood. My long-term research goal is to determine how the human brain generates skilled hand and mouth movements. I am especially interested in how these movements and their underlying neural substrates arose through evolution, are established during development, and breakdown in various neurological disorders. I use 3D linear kinematics, high-speed frame-by-frame video analyses, and more recently functional neuroimaging to characterize the neural and behavioural architecture of skilled hand and mouth movements in human and non-human species.
The most notable theory concerning the neural control of prehension is the Dual Visuomotor Channel theory (1), which proposes that prehension consists of two movements mediated by separate but interacting pathways that project from visual to motor cortex via the parietal lobe (Figure 1). A Reach transports the hand to the location of the target while a Grasp opens and closes the hand for target purchase. As revealed by its name, this theory places special emphasis on the role of vision in Reach and Grasp control. Such a central role for vision caters to current ideas that humans evolved especially dexterous hands only after the emergence of forward facing eyes and a bipedal stance; however, it fails to account for the range of complex hand movements used by non-primates, often to feed themselves in the absence of visual guidance (2), or our ability to readily reach, grasp, and manipulate objects even when vision is not available.
Behavioural Studies in Adults
Behavioural work that I conducted in my Ph.D. confirmed previous findings that when vision is available, participants integrate the Reach and the Grasp into a single prehensile act such that the hand opens, preshapes, and closes to the size of a target by the time it contacts it (preshaping strategy, Figure 2A). When vision is removed, however, prehension decomposes into its constituent components: an open-handed Reach is first used to locate the target by touching it and then tactile cues guide subsequent shaping and closure of the hand to Grasp (touch-then-grasp strategy, Figure 2B). Hand shaping for grasping is equally accurate whether guided by vision or touch (3). Dissociation of the Reach and the Grasp under non-visual control supports the proposition of the Dual Visuomotor Channel theory that the Reach and the Grasp are derived from different neural origins; however, it refutes the idea that vision is privileged, suggesting instead that vision and touch have equal access to the Reach and Grasp pathways in parietofrontal cortex.
Behavioural Studies in Developing Infants
Interestingly, my work with 4- to 24-month-old infants revealed that when infants first begin to reach, they structure their movements much like blindfolded adults, even though they have vision (Figure 3). Thus, rather than integrating the Reach and the Grasp together under vision, they use a tactile touch-then-grasp strategy. This suggests that separate Reach and Grasp movements originate under tactile control early in development and are only integrated under visual control after a prolonged developmental period lasting into early childhood (4).
Studies on non-primate species suggest that the ability to integrate the Reach and the Grasp under visual control is unique to the primate lineage. For instance, when reaching to grasp distal objects rats (5) and raccoons (6) use a touch-then-grasp strategy similar to blindfolded adults and young infants, suggesting that they rely on tactile cues to guide sequential, rather than integrated, Reach and Grasp movements. They can, however, integrate the Reach and the Grasp under tactile control when reaching to grasp an object in their own mouth in order to prepare it for eating (Figure 4). Thus, non-primate mammals can flexibly integrate or dissociate the Reach and the Grasp under tactile control depending on the demands of the task. They cannot, however, do the same under vision. This suggests that tactile Reach and Grasp movements are phylogenetically (or evolutionarily) older than those guided by vision. Collective evidence suggests that the Reach may be derived from forelimb stepping whereas the Grasp may be derived from food handling (7).
The independence of the Reach and the Grasp under non-visual control supports the proposition of the Dual Visuomotor Channel theory that the neural substrates of the Reach and the Grasp are distinct and derived from different evolutionary origins. Thus, distinct motor circuits for the ‘Reach’ and the ‘Grasp’ may have emerged relatively early in evolution and were likely influenced more by tactile than visual inputs. Expansion of the primate visual system would have given rise to a number of new connections between occipital and parietofrontal cortex, allowing vision to harness these pre-existing ‘Reach’ and ‘Grasp’ circuits resulting in multiple visuomotor pathways from occipital to parietofrontal cortex (Figure 5). No longer constrained by the necessity of tactile control, the Reach and the Grasp could be executed simultaneously, rather than sequentially, giving primates the unique ability to preshape the hand to the size and shape of a visual target before touching it.
Neurobehavioural separation of the Reach and the Grasp seems important as it allows us to flexibly recombine the two movements depending on the sensory and cognitive demands of a given situation. For instance, it allows us to combine a variety of pincer, precision, power, or hook grasps with a variety of reaches, swats, pushes, or pulls. Thus, the selection and refinement of separate Reach and Grasp movements under tactile control early in evolution and development likely led to the emergence of a more diverse behavioural repertoire than if the same processes had favoured the selection and refinement of a single prehensile movement under a single, visual, modality.
(1) Jeannerod M. Intersegmental coordination during reaching at natural visual objects. In: Long J, Badeley A, editors. Attention and Performance IX. Hillsdale: Lawrence Erlbaum Associates (1981). p. 153-169.
(2) Whishaw IQ, Sarna JR, Pellis SM. Evidence for rodent-common and species-typical limb and digit use in eating, derived from a comparative analysis of ten rodent species. Behavioural Brain Research (1998) 96:79-91.
(3) Karl JM, Sacrey L-AR, Doan JB, Whishaw IQ. Hand shaping using hapsis resembles visually guided hand shaping. Experimental Brain Research (2012) 219:59-74.
(4) Karl JM, Whishaw IQ. Haptic grasping configurations in early infancy reveal different developmental profiles for visual guidance of the Reach versus the Grasp. Experimental Brain Research (2014) 232:3301-3316.
(5) Metz GA, Whishaw IQ. Skilled reaching an action pattern: stability in rat (Rattus norvegicus) grasping movements as function of changing pellet size. Behavioural Brain Research (2000) 116:111-122.
(6) Iwaniuk AN, Whishaw IQ. How skilled are the skilled limb movements of the raccoon (Procyon lotor)? Behavioural Brain Research (1999) 99:35-44.
(7) Karl JM, Whishaw IQ. Different evolutionary origins for the Reach and the Grasp: An explanation for dual visuomotor channels in primate parietofrontal cortex. Frontiers in Neurology (2013) 4:208.