Unusual prism adaptation reveals how grasping is controlled

Abstract

There are three main theories on how human grasping movements are controlled. Two of them state that grip aperture and the movement of the hand are controlled. They differ in whether the wrist or the thumb of the hand is controlled. We have proposed a third theory, which states that grasping is a combination of two goal-directed single-digit movements, each directed at a specific position on the object. In this study, we test predictions based on each of the theories by examining the transfer of prism adaptation during single-digit pointing movements to grasping movements. We show that adaptation acquired during single-digit movements transfers to the hand opening when subsequently grasping objects, leaving the movement of the hand unaffected. Our results provide strong evidence for our theory that grasping with the thumb and index finger is based on a combination of two goal-directed single-digit movements.

Keywords: coordination; grasping; human; neuroscience; prehension; prism adaptation; visuomotor.

Figure 1.. The prisms’ effects on the individual digits, grip aperture and grip position.

Overview of the individual digits throughout the experiment (A) and a detailed view of the grip aperture (B) and grip position (C) for the grasping movements performed in the pre- and post- adaptation phases. In panel A the symbols show the overall mean effect of the prisms on the position of the digits for each block of 6 trials during the three phases of the experiment. In the adaptation phase (white background), the digits partially adapt to the prisms during pointing movements. When switching to grasping movements under normal vision (grey background on the right) we see an aftereffect. In panels B and C, the symbols show the trial-by-trial time course averaged over all participants. The bars in the center of each panel show the average values (Mean ±SEM of the individual participants’ median values within each phase; source file available as Figure 1—source data 1). A positive grip position is to the right. The inset shows one participant’s time course of grip aperture during the last movement towards the target cube in one of the pre-adaptation phases (black curve) and during the first movements towards the target cube in both post-adaptation phases (dashed blue and solid red curves). Time 0 is the moment at which we determined the digits’ positions for calculating grip aperture and grip position. The horizontal dashed line is the grip aperture at which the digits touch each other.

Figure 2.. Top and side views of the experimental setup.

The subject performs a single-digit pointing trial with the index finger. During single-digit trials, participants viewed the target block monocularly through a prism that was in front of the shutter glasses and moved their hand from the starting cube to touch the left side of the target cube with their thumb or to the right side of the target cube with their index finger. During grasping trials, participants were not wearing the prisms and viewed the target block binocularly. On these trials, participants grasped either the small target cube or the large target block (cuboid).

Appendix 1—figure 1.. Data of the control experiment on the transfer of adaptation from single-digit pointing movements to the grip position in grasping.

Participants started with 6 grasping trials (pre-adaptation; grey background). Subsequently, they made 24 pointing movements with either the index finger or thumb while wearing leftward deviating prisms (adaptation; white background)., Finally, participants performed 6 more grasping trials after removing the prisms (post-adaptation; grey background). Each dot is based on 3 trials per participant, and shows the average (±SEM) across participants. For the grasping trials, we first averaged the grip positions in the three trials for each participant. For the pointing trials, we first averaged the positions for each digit (if there was more than one value), and then averaged across index finger and thumb. If there were no values for one of the digits in the three trials, that participant’s data does not contribute to that point.

Appendix 2—figure 1.. Data of the control experiment on the effect of digit-eye pairing.

(A) The participants made pointing movements with either the unseen index finger (purple) or thumb (green) of their dominant hand (the right hand for 7 of the 8 participants). During adaptation (central part with a white background), participants received feedback about the endpoint of their movement. The feedback was shifted 3 cm to the left or the right. Before and after the adaptation trials they received no feedback (grey background). During adaptation, there was a fixed pairing between viewing eye and digit (filled symbols). Before and after the feedback trials, half the trials had the opposite pairing between viewing eye and digit (open symbols). Negative values on the y-axis represent the direction in which the feedback was shifted. So although the perturbation was always in opposite directions for the two digits (and sessions), the expected response is always in the positive direction. Each symbol indicates the median lateral error of all cases in which that digit was used in combination with that eye on that trial. (B) The after-effect of the adaptation: the mean difference between the individual differences between the median lateral errors before and after feedback, separately for the thumb (green) and index finger (purple), and the same digit-eye pairing as was used during adaptation (filled bars) and the opposite pairing (open bars).