Ignasi Cos

The influence of predicted arm biomechanics on decision-making

There is considerable debate on the extent to which biomechanical properties of movements are taken into account before and during voluntary movements. For example, while several models have described reach planning as primarily kinematic, some studies have suggested that implicit knowledge about biomechanics may also exert some influence on the planning of reaching movements. Here, we investigated whether decisions about reaching movements are influenced by biomechanical factors and whether these factors are taken into account before movement onset. To this end, we designed an experimental paradigm in which humans made free choices between two potential reaching movements where the options varied in path distance as well as biomechanical factors related to movement energy and stability. Our results suggest that the biomechanical properties of potential actions strongly influence the selection between them. In particular, in our task, subjects preferred movements whose final trajectory was better aligned with the major axis of the arms mobility ellipse, even when the launching properties were very similar. This reveals that the nervous system can predict biomechanical properties of potential actions before movement onset and that these predictions, in addition to purely abstract criteria, may influence the decision-making process.

Rapid prediction of biomechanical costs during action decisions.

When given a choice between actions that yield the same reward, we tend to prefer the one that requires the least effort. Recent studies have shown that humans are remarkably accurate at evaluating the effort of potential reaching actions and can predict the subtle energetic demand caused by the nonisotropic biomechanical properties of the arm. In the present study, we investigated the time course over which such information is computed and comes to influence decisions. Two independent approaches were used. First, subjects performed a reach decision task in which the time interval for deciding between two candidate reaching actions was varied from 200 to 800 ms. Second, we measured motor-evoked potential (MEPs) to single-pulse transcranial magnetic stimulation (TMS) over the primary motor cortex (M1) to probe the evolving decision at different times after stimulus presentation. Both studies yielded a consistent conclusion: that a prediction of the effort associated with candidate movements is computed very quickly and influences decisions within 200 ms after presentation of the candidate actions. Furthermore, whereas the MEPs measured 150 ms after stimulus presentation were well correlated with the choices that subjects ultimately made, later in the trial the MEP amplitudes were primarily related to the muscular requirements of the chosen movement. This suggests that corticospinal excitability (CSE) initially reflects a competition between candidate actions and later changes to reflect the processes of preparing to implement the winning action choice.

Context-Dependent Urgency Influences Speed–Accuracy Trade-Offs in Decision-Making and Movement Execution

Speed–accuracy tradeoffs (SATs) exist in both decision-making and movement control, and are generally studied separately. However, in natural behavior animals are free to adjust the time invested in deciding and moving so as to maximize their reward rate. Here, we investigate whether shared mechanisms exist for SAT adjustment in both decisions and actions. Two monkeys performed a reach decision task in which they watched 15 tokens jump, one every 200 ms, from a central circle to one of two peripheral targets, and had to guess which target would ultimately receive the majority of tokens. The monkeys could decide at any time, and once a target was reached, the remaining token movements accelerated to either 50 ms (“fast” block) or 150 ms (“slow” block). Decisions were generally earlier and less accurate in fast than slow blocks, and in both blocks, the criterion of accuracy decreased over time within each trial. This could be explained by a simple model in which sensory information is combined with a linearly growing urgency signal. Remarkably, the duration of the reaching movements produced after the decision decreased over time in a similar block-dependent manner as the criterion of accuracy estimated by the model. This suggests that SATs for deciding and acting are influenced by a shared urgency/vigor signal. Consistent with this, we observed that the vigor of saccades performed during the decision process was higher in fast than in slow blocks, suggesting the influence of a context-dependent global arousal.

Motor cost influences perceptual decisions

Perceptual decision making has been widely studied using tasks in which subjects are asked to discriminate a visual stimulus and instructed to report their decision with a movement. In these studies, performance is measured by assessing the accuracy of the participants’ choices as a function of the ambiguity of the visual stimulus. Typically, the reporting movement is considered as a mere means of reporting the decision with no influence on the decision-making process. However, recent studies have shown that even subtle differences of biomechanical costs between movements may influence how we select between them. Here we investigated whether this purely motor cost could also influence decisions in a perceptual discrimination task in detriment of accuracy. In other words, are perceptual decisions only dependent on the visual stimulus and entirely orthogonal to motor costs? Here we show the results of a psychophysical experiment in which human subjects were presented with a random dot motion discrimination task and asked to report the perceived motion direction using movements of different biomechanical cost. We found that the pattern of decisions exhibited a significant bias towards the movement of lower cost, even when this bias reduced performance accuracy. This strongly suggests that motor costs influence decision making in visual discrimination tasks for which its contribution is neither instructed nor beneficial.

Adaptation for multisensory relative timing

Perception of relative timing for signals arising from different sensory modalities depends on the recent history of experienced asynchrony between the signals. Recent findings suggest that the changes in perceived relative timing following asynchrony exposure parallel the perceptual changes caused by adaptation to non-temporal attributes. In both cases, previous sensory stimulation changes discriminability and briefly presented adaptors are sufficient to produce perceptual changes that, functionally, can be consistent with repulsion and recalibration. Furthermore, a new class of after-effects in which reports are biased in the direction of the adaptor also occur for both temporal and non-temporal attributes. Computationally, the effects of previous sensory stimulation on behavior have been assessed using Bayesian and population code models.

Beta-Band Oscillations without Pathways: the opposing Roles of D2 and D5 Receptors

Parkinson’s disease is characterized by the death of dopaminergic neurons and the emergence of strong β-band oscillations throughout the basal ganglia nuclei. According to the mainstream theory, this synchrony is mediated by a dopamine deficit within the striatum creating a functional imbalance between the D1-expressing medium spiny neurons, which project to the internal segment of the globus pallidus, and D2-expressing one, which target its external segment, and ultimately leads to oscillatory activity. However, anatomical evidence gathered in rodents and primates has shown that striatal neurons are for the most part not organized into independent populations differentially targeting the two segments of the globus pallidus, nor alternatively expressing D1 or D2 receptors, thus calling for an alternative mechanism through which the lack of dopamine may cause oscillations. Here we adopt a computational approach in which we investigate a model whose parameters are fit to an extensive set of anatomical and physiological constraints from non-human primates, including axonal transmission delays gathered from eight experimental studies. Investigating the lack of dopamine in this model revealed that in the absence of segregated pathways, β-band oscillations emerge as a consequence of the extra-striate dopaminergic receptors reduced activity. These oscillations are caused by synchronous activity within the external globus pallidus-subthalamic nucleus loop, and their frequency are modulated by the transmission delays between these nuclei. Our model delivers a parsimonious explanation of oscillations that does not require any external driving influence from cortex, nor specific medium spiny neuron properties.

Perceived effort for motor control and decision-making

How effort is internally quantified and how it influences both movement generation and decisions between potential movements are 2 difficult questions to answer. Physical costs are known to influence motor control and decision-making, yet we lack a general, principled characterization of how the perception of effort operates across tasks and conditions. Morel and colleagues introduce an insightful approach to that end, assessing effort indifference points and presenting a quadratic law between perceived effort and force production.

Learning a sequence of motor responses to attain reward: a speed-accuracy trade-off

The study of decision-making between goal directed actions with rodents has been often based on experimental tasks in which animals were trained to perform specific sequences of actions, such as lever presses or nose pokes [4], to attain reward. This supported the hypothesis of reinforcement learning as the underlying mechanism to acquire those behavioural sequences, putatively implemented by the basal-ganglia circuitry [1,3]. However, experimental evidence suggests that whenever we extend the complexity of the motor responses towards timely constrained behaviour, it starts reflecting an influence of costs related not only to reward, but rather a compromise between the motor factors relevant to the task, and the timely requirements to attain the goal [6]. To investigate this further, we took advantage of new behavioral protocol in which rats running on a treadmill need to estimate a fixed-temporal interval to obtain a reward [5]. Interestingly rats became proficients in this task by developping very stereotyped running trajectories. The establishment of these precise running kinematics occured progressively in a trial-and-error process that lasted between 2 to 3 months. At this point if we shortened the treadmill length, animals persisted in reproducing the previously learned kinematics even if doing so they stopped receiving reward. This is consistent with that these stereotyped running kinematics are motor habit [8]. To provide a theoretical backend for these results, we developed a model-free reinforcement learning model [7]. We excluded model-based algorithms because of the inability of the rats to exploit the previously learned behavior to accelerate their learning rate when the task changes. The specificity of this model is to count reward delivery as positive reward, but also efforts generated at each time step as negative rewards. The problem is thus a speed-accuracy trade-off process: the goal of the model is to generate the motor sequence that optimizes the ratio discounted reward/effort. The main result shows that, as long as the local time and speed are included into the characterization of the kinematic state, the model can replicate the same motor sequences. This suggests that these two pieces information are required to learn time-constrained motor sequences, and predicts that if a brain structure indeed learns these habitual sequences as the model does (our suggestion would be the sensorimotor circuits of the basal ganglia [2]), it should exhibit correlates with the same variables during the entire sequence.

Correction: Perceived Effort for Motor Control and Decision-Making

[This corrects the article DOI: 10.1371/journal.pbio.2002885.].