Jason W. Flindall

On the Evolution of Handedness: Evidence for Feeding Biases

Many theories have been put forward to explain the origins of right-handedness in humans. Here we present evidence that this preference may stem in part from a right hand advantage in grasping for feeding. Thirteen participants were asked to reach-to-grasp food items of 3 different sizes: SMALL (Cheerios®), MEDIUM (Froot Loops®), and LARGE (Oatmeal Squares®). Participants used both their right- and left-hands in separate blocks (50 trials each, starting order counterbalanced) to grasp the items. After each grasp, participants either a) ate the food item, or b) placed it inside a bib worn beneath his/her chin (25 trials each, blocked design, counterbalanced). The conditions were designed such that the outward and inward movement trajectories were similar, differing only in the final step of placing it in the mouth or bib. Participants wore Plato liquid crystal goggles that blocked vision between trials. All trials were conducted in closed-loop with 5000 ms of vision. Hand kinematics were recorded by an Optotrak Certus, which tracked the position of three infrared diodes attached separately to the index finger, thumb, and wrist. We found a task (EAT/PLACE) by hand (LEFT/RIGHT) interaction on maximum grip aperture (MGA; the maximum distance between the index finger and thumb achieved during grasp pre-shaping). MGAs were smaller during right-handed movements, but only when grasping with intent to eat. Follow-up tests show that the RIGHT-HAND/EAT MGA was significantly smaller than all other hand/task conditions. Because smaller grip apertures are typically associated with greater precision, our results demonstrate a right-hand advantage for the grasp-to-eat movement. From an evolutionary perspective, early humans may have preferred the hand that could grasp food with more precision, thereby maximizing the likelihood of retrieval, consumption, and consequently, survival.

Manual asymmetries in the kinematics of a reach-to-grasp action

In the present study, we manipulated the perceived demand of an ecologically valid task to investigate the possible presence of manual asymmetries in a reach-to-grasp action. Participants reached, grasped and sipped from a water glass under low (nearly empty) and high (nearly full) demand conditions. Participants reached to grasp in closed-loop, open-loop and delay visual conditions. Manual asymmetries were found in movement time, peak velocity and maximum grip aperture variability. Consistent with reach-to-point literature: (1) right-handed actions were completed in less time than left-handed actions in visually and memory-guided conditions; (2) right-handed movements were more accurate (i.e., produced more consistent maximum grip apertures) than left-handed movements in visually guided conditions. The results support a theory of left-hemisphere specialization for visual control of action.

Evidence for right-hand feeding biases in a left-handed population

We have recently shown that actions with similar kinematic requirements, but different end-state goals may be supported by distinct neural networks. Specifically, we demonstrated that when right-handed individuals reach-to-grasp food items with intent to eat, they produce smaller maximum grip apertures (MGAs) than when they grasp the same item with intent to place it in a location near the mouth. This effect was restricted to right-handed movements; left-handed movements showed no difference between tasks. The current study investigates whether (and to which side) the effect may be lateralized in left-handed individuals. Twenty-one self-identified left-handed participants grasped food items of three different sizes while grasp kinematics were captured via an Optotrak Certus motion capture array. A main effect of task was identified wherein the grasp-to-eat action generated significantly smaller MGAs than did the grasp-to-place action. Further analysis revealed that similar to the findings in right-handed individuals, this effect was significant only during right-handed movements. Upon further inspection however, we found individual differences in the magnitude and direction of the observed lateralization. These results underscore the evolutionary significance of the grasp-to-eat movement in producing population-level right-handedness in humans as well as highlighting the heterogeneity of the left-handed population.

Eating interrupted: the effect of intent on hand-to-mouth actions

Evidence from recent neurophysiological studies on nonhuman primates as well as from human behavioral studies suggests that actions with similar kinematic requirements but different end-state goals are supported by separate neural networks. It is unknown whether these different networks supporting seemingly similar reach-to-grasp actions are lateralized, or if they are equally represented in both hemispheres. Recently published behavioral evidence suggests certain networks are lateralized to the left hemisphere. Specifically, when participants used their right hand, their maximum grip aperture (MGA) was smaller when grasping to eat food items than when grasping to place the same items. Left-handed movements showed no difference between tasks. The present study investigates whether the differences between grasp-to-eat and grasp-to-place actions are driven by an intent to eat, or if placing an item into the mouth (sans ingestion) is sufficient to produce asymmetries. Twelve right-handed adults were asked to reach to grasp food items to 1) eat them, 2) place them in a bib, or 3) place them between their lips and then toss them into a nearby receptacle. Participants performed each task with large and small food items, using both their dominant and nondominant hands. The current study replicated the previous finding of smaller MGAs for the eat condition during right-handed but not left-handed grasps. MGAs in the eat and spit conditions did not significantly differ from each other, suggesting that eating and bringing a food item to the mouth both utilize similar motor plans, likely originating within the same neural network. Results are discussed in relation to neurophysiology and development.

Hand preference across the lifespan: effects of end-goal, task nature, and object location

In the present study we investigate age-related changes in hand preference for grasping and the influence of task demands on such preference. Children (2–11), young-adults (17–28) and older-adults (57–90) were examined in a grasp-to-eat and a grasp-to-construct task. The end-goal of these tasks was different (eat vs. construct) as was the nature of the task (unimanual vs. bimanual). In both tasks, ipsilateral and contralateral grasps were analyzed. Results showed a right-hand preference that did not change with age. Across the three age groups, a more robust right-hand preference was observed for the unimanual, grasp-to-eat task. To disentangle if the nature (unimanual) or the end-goal (grasp-to-eat) was the driver of the robust right-hand preference, a follow up experiment was conducted. Young-adult participants completed a unimanual grasp-to-place task. This was contrasted with the unimanual grasp-to-eat task and the bimanual grasp-to-construct task. Rates of hand preference for the grasp-to-eat task remained the highest when compared to the other two grasping tasks. Together, the results demonstrate that hand preference remains stable from childhood to older adulthood, and they suggest that a left hemisphere specialization exists for grasping, particularly when bringing food to the mouth.

Children's bilateral advantage for grasp-to-eat actions becomes unimanual by age 10 years.

Studies have shown that infants tend to develop a lateralized hand preference for hand-to-mouth actions earlier than they do a preference for many other grasp-to-place or grasp-to-manipulate tasks, years even before direction of hand preference can be reliably determined. This observation has led to a series of studies contrasting the kinematics of grasp-to-eat and grasp-to-place actions in adults. These studies have described a robust kinematic asymmetry between left- and right-handed grasp-to-eat maximum grip apertures (MGAs) that has been interpreted as a right-hand advantage for feeding that may have led to right-handedness as observed on a global scale. The current study examines grasp-to-eat and grasp-to-place kinematics in two groups of typically developing children aged 7 to 12 years. It was found that the previously described task difference is present in both hands among younger children and that the effect does not become lateralized until the end of the first decade of life. Additional kinematics of both the dominant and non-dominant hands are described in detail to augment a growing catalogue of reach-to-grasp action descriptions for typically developing children. The maturation of the right-hand advantage for grasp-to-eat actions is discussed in terms of an inherent right-hand/left-hemisphere bias for such actions that may have influenced the development of population-level right-handedness in humans.

The destination defines the journey: an examination of the kinematics of hand-to-mouth movements

Long-train electrical stimulation of the motor and premotor cortices of nonhuman primates can produce either hand-to-mouth or grasp-to-inspect movements, depending on the precise location of stimulation. Furthermore, single-neuron recording studies identify discrete neuronal populations in the inferior parietal and ventral premotor cortices that respond uniquely to either grasp-to-eat or grasp-to-place movements, despite their identical mechanistic requirements. These studies demonstrate that the macaque motor cortex is organized around producing functional, goal-oriented movements, rather than simply fulfilling muscular prerequisites of action. In humans, right-handed hand-to-mouth movements have a unique kinematic signature; smaller maximum grip apertures are produced when grasping to eat than when grasping to place identical targets. This is evidence that the motor cortex in humans is also organized around producing functional movements. However, in both macaques and humans, grasp-to-eat/hand-to-mouth movements have always been elicited using edible targets and have (necessarily) been paired with mouth movement. It is therefore unknown whether the kinematic distinction is a natural result of grasping food and/or is simply attributable to concurrent opening of the mouth while grasping. In experiment 1, we used goal-differentiated grasping tasks, directed toward edible and inedible targets, to show that the unique kinematic signature is present even with inedible targets. In experiment 2, we used the same goal-differentiated grasping tasks, either coupled with or divorced from an open-mouth movement, to show that the signature is not attributable merely to a planned opening of the mouth during the grasp. These results are discussed in relation to the role of hand-to-mouth movements in human development, independently of grasp-to-eat behavior.

The inimitable mouth: task-dependent kinematic differences are independent of terminal precision

Previous studies in our lab have described kinematic difference between grasp-to-eat and grasp-to-place movements, whereby participants produce smaller maximum grip apertures (MGAs) when grasping to bring the item to the mouth than when grasping to bring the item to a container near the mouth. This task difference is limited to right-handed movements, regardless of handedness; it has, therefore, been interpreted as evidence of left-hemisphere lateralization of the grasp-to-eat and other hand-to-mouth grasping movements. However, the difference in end-goal aperture may have accounted for both the kinematic signature (smaller MGAs) and their lateralized expression. Specifically, if the right hand is more sensitive to the precision requirements of secondary movements, it may have produced more precise MGAs for actions whose ultimate goal is the small-aperture mouth rather than a comparatively large aperture container. The current study addresses this question by replacing the previously-used bib with a small drinking glass whose aperture more closely resembles that of the mouth. 25 adult participants reached-to-grasp small cereal items to either (a) eat them, or (b) place them into a small-aperture glass hanging beneath their chin. Results once more showed a lateralised kinematic signature in the form of smaller MGAs for the eat action, demonstrating that the signature is not a result of lateralized sensitivity to a movement’s secondary precision requirements. We discuss these results in terms of their impact on predominant theories regarding visual guidance of grasping movements.

Kinematics of ventrally mediated grasp-to-eat actions: right-hand advantage is dependent on dorsal stream input

Studies have suggested a left-hemisphere specialization for visually guided grasp-to-eat actions by way of task-dependent kinematic asymmetries (i.e., smaller maximum grip apertures for right-handed grasp-to-eat movements than for right-handed grasp-to-place movements or left-handed movements of either type). It is unknown, however, whether this left-hemisphere/right-hand kinematic advantage is reliant on the dorsal “vision-for-action” visual stream. The present study investigates the kinematic differences between grasp-to-eat and grasp-to place actions performance during closed-loop (i.e., dorsally mediated) and open-loop delay (i.e., ventrally mediated) conditions. Twenty-one right-handed adult participants were asked to reach to grasp small food items to (1) eat them, or (2) place them in a container below the mouth. Grasps were performed in both closed-loop and open-loop delay conditions, in separate sessions. We show that participants displayed the right-hand grasp-to-eat kinematic advantage in the closed-loop condition, but not in the open-loop delay condition. As no task-dependent kinematic differences were found in ventrally mediated grasps, we posit that the left-hemisphere/right-hand advantage is dependent on dorsal stream processing.

Hear speech, change your reach: changes in the left-hand grasp-to-eat action during speech processing

Research has shown that the kinematic characteristics of right-hand movements change when executed during both speech production and processing. Despite the variety of prehension and manual actions used to examine this relationship, the literature has yet to examine potential movement effects using an action with a distinct kinematic signature: the hand-to-mouth (grasp-to-eat) action. In this study, participants performed grasp-to-eat and grasp-to-place actions in (a) a quiet environment and (b) while processing speech. Results during the quiet condition replicated the previous findings; consistently smaller grasp-to-eat (compared to grasp-to-place), maximum grip apertures appeared only when using the right hand. Interestingly, in the listen condition, smaller maximum grip apertures in the grasp-to-eat movement appeared in both the right and left hands, despite the fact that participants were right-handed. This paper addresses these results in relation with similar behaviour observed in children, and discusses implications for functional lateralization and neural organization.