Short-term motor plasticity revealed in a visuomotor decision-making task

Abstract

Selecting and executing an action toward only one object in our complex environments presents the visuomotor system with a significant challenge. To overcome this problem, the motor system is thought to simultaneously encode multiple motor plans, which then compete for selection. The decision between motor plans is influenced both by incoming sensory information and previous experience—which itself is comprised of long-term (e.g. weeks, months) and recent (seconds, minutes, hours) information. In this study, we were interested in how the recent trial-to-trial visuomotor experience would be factored into upcoming movement decisions made between competing potential targets. To this aim, we used a unique rapid reaching task to investigate how reach trajectories would be spatially influenced by previous decisions. Our task required subjects to initiate speeded reaches toward multiple potential targets before one was cued in-flight. A novel statistical analysis of the reach trajectories revealed that in cases of target uncertainty, subjects initiated a spatially averaged trajectory toward the midpoint of potential target locations before correcting to the selected target location. Interestingly, when the same target location was consecutively cued, reaches were biased toward that location on the next trial and this effect accumulated across trials. Beyond providing supporting evidence that potential reach locations are encoded and compete in parallel, our results strongly suggest that this motor competition is biased by recent trial history.

Introduction

Among the most challenging problems faced by our visuomotor system is the selection of targets in a cluttered world filled with many objects that could be acted upon. One possible solution to this problem is revealed by neurophysiological studies that suggest the brain plans multiple motor programs in parallel [1], [2], [3], [4], [5], allowing for several targets to compete for action selection at any one time. This strategy facilitates and simplifies target selection. Because all the potential actions are simultaneously coded, selection of the final action becomes the more straightforward process of one action plan ‘winning out’ over the others. This motor competition requires that each potential plan be associated with levels of activation reflecting its likelihood of being selected [e.g. [1]], but it is rather poorly understood what specific target and task properties modulate this competitive process.

In a recent experiment, we found that when subjects performed rapid reaches toward two equally likely targets before one target was cued in-flight, subjects initiated a ‘spatially’ averaged trajectory toward the midpoint of the potential target locations [6]. This is consistent with other eye-movement and reach paradigms demonstrating that movements made in the presence of competing stimuli tend to deviate between the stimulus locations [7], [8], [9], [10]. In a second experiment, we also showed that reach trajectories were biased both by the spatial location of the potential targets and by the number of targets on each side of space, suggesting that location and probability are factors that influence motor plan competition [6]. This pattern of results, however, is consistent with the idea that all the potential targets (and actions) have identical weights. Yet it is necessary to have a visuomotor system that can independently adjust the weightings of each potential target and action. Indeed, motor decisions are based not only on the information currently available to the sensory system, but also on previous visuomotor experience [e.g. [11]]. Visuomotor experience and the changes associated with that experience can accrue over timescales of weeks or months [12], [13] but can also be seen to operate over much shorter intervals [e.g. [9], [14], [15], [16]]. Specifically, it has been shown that the parameters of a current movement are influenced by the characteristics and intentions of the previous movement. It is precisely this trial-to-trial motor plasticity that we investigated in the current experiment: how the selection of a given target on one trial alters its weighting in the competition between targets on the subsequent trial.

Trial history effects reveal how visuomotor decision-making processes evolve across multiple movements [e.g. [14], [15], [17], [18]] and have been investigated in a wide range of paradigms. For example, subjects are faster to detect targets when the location is repeated [19], and grasping kinematics are affected by the recent availability of visual feedback [20], [21]. Target-directed eye movements provide a particularly good illustration of the effects of trial history: the colour, shape and location of the target on a previous trial influences both the neural activity in eye-movement-related structures during motor planning and the subsequent behavioural response [e.g. [7], [22], [23]]. In addition, behavioural studies have shown that reach targets embedded among distractors that vary in colour from trial-to-trial produce more variable reach trajectories than targets that maintain a colour across trials [24]. Of particular relevance is recent work investigating the effects of previously performed arm movements on subsequently performed actions. For example, avoiding a virtual obstacle on one trial will result in a more curved trajectory on the next trial even when no obstacle is present [25], [26]. These results suggest that successive movements in a sequence are not programmed de novo but instead are created by slightly modifying the blueprints of the preceding movement(s) [27]. In the current study, we wanted to capitalize on this proposed holdover of motor parameters from trial-to-trial as a way of creating a disparity in the weightings assigned to two potential targets. As such, we tested if the spatial averaging between potential targets that we have previously reported [6] would be biased toward the location of a previously cued target, and if so, whether this bias would accumulate across multiple trials.