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

Abstract

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.

Keywords: edible; grasp; grip aperture; hand; mouth.

Fig. 1.

Closed-mouth (A) and open-container conditions (B) used in experiment 2.

Fig. 2.

Grip aperture differences between conditions in experiment 1. Left, average grip aperture over time for grasps directed toward large targets for a typical participant (participant TFO). Trials have been reaction time (RT)-aligned to best show differences in maximum grip aperture (MGA) between conditions. Right, MGAs (means and SE), collapsed across target size (small, larger), in the mouth and container goal conditions for edible and inedible objects. Difference between goal conditions was significant for both target types (*P < 0.01). Avg., average.

Fig. 3.

Grip aperture differences between conditions in experiment 2. Left, average grip aperture over time during grasps directed toward large targets for a single typical participant (participant MMS). Trials have been RT-aligned to best show MGA differences between conditions. Right, MGAs, (means and SE), collapsed across size, for open- and closed-state conditions in mouth and container goal conditions. MGAs during the open-mouth condition (i.e., when participants ate the target) were significantly smaller than MGAs in both closed-mouth (*P < 0.001) and closed-container conditions (*P < 0.008). No other conditions were significantly different from one another following Bonferroni correction (P > 0.0083).