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Thura, D.

Publications and source records attributed to Thura, D..

13 recordsLinked to original sources

Internal perturbation reveals the flexible and adaptive nature of the coordination between decisions and movements

Although growing evidence indicates that decision-making and movement control are tightly coordinated, the functional significance of this coordination remains poorly understood. In particular, it is unclear whether changes in the animals arousal are sufficient to reorganize decision-action coordination in a manner that preserves behavioral efficiency. To address this question, we pharmacologically slowed behavior in rhesus monkeys performing a reaching-based foraging task while leaving task demands unchanged. Under this internal perturbation, prolonged decisions were initially associated with shorter movement durations, revealing a compensatory coordination that reduced the additional temporal cost of slower deliberation. As animals progressively adapted across sessions, decision durations decreased, reward rates increased, and compensatory coordination became less prevalent, giving way to patterns of decision-movement co-regulation. This observation suggests that compensatory adjustments are recruited transiently during adaptation rather than representing a constitutive mode of behavioral control. These findings provide causal evidence that an internally-induced slowing of decision-making is sufficient to reorganize the temporal relationship between decisions and movements. More broadly, they support the view that decision-making and movement execution are regulated as complementary components of a unified adaptive control process that flexibly adjusts the temporal organization of behavior in response to changes in internal state, thereby contributing to the maintenance of efficient reward acquisition.

neuroscience↗

Quantitative evaluation of enrichment protocols on rhesus macaques welfare in laboratory environment.

Non-human primates are crucial animal models in biomedical research including neurosciences. Legal frameworks ensure that participation of monkeys in biomedical research follows an ethical assessment, driven by specific guidelines for ensuring animal well-being. Those guidelines promote continued refinement of practices to improve animal wellbeing, yet quantitative data to inform such refinements is limited. In this context, we investigated the impact of modifications to the housing that created either navigational complexity or visual access to neighbouring animals on the behaviour of rhesus macaques. Then we quantified the value of different enrichment programmes based on manipulable objects. We showed that making navigation within a modular housing more complex, or adding transparent separations between housing units is associated with significant reduction of severe aggression, stereotypical behaviours and a significant increase of appeasing behaviours. We also observed a positive effect of manipulable objects with an increase in the expression of appeasing behaviours and a decrease in abnormal or stereotypical behaviours. Finally, our study revealed significant inter-individual variability that was not explained by sex, age, social network size or social status. Overall, our results point to the importance and benefits of environmental changes and enrichment protocols, and of the critical need for personalised enrichment programmes.

animal behavior and cognition↗

Optimal foraging requires coordinating decisions with movements

Decision-making and motor execution are both constrained by time and energy, and their optimization depends on cost-benefit trade-offs. While many studies suggest that decisions and movements follow common economic principles and can be jointly regulated to maximize reward rate, recent findings indicate that these two processes can also be decoupled or modulated in compensatory ways. This variability raises the question of whether decision-action coordination reflects an optimal strategy aimed at maximizing reward rate, or rather a flexible but suboptimal adaptation to contextual constraints. To address this issue, we trained three macaque monkeys to perform a reaching-based foraging task. The observed adjustments in decision-action coordination of the three monkeys are consistent with the pursuit of a strategy that approximates the theoretical optimum of reward intake rate at the single trial level. The present findings indicate, both behaviorally and theoretically, that coordination between decision and movement is required to optimize behavior in economic terms.

animal behavior and cognition↗

Humans anticipate the consequences of motor control demands when making perceptual decisions between actions

Animals, including humans, are often faced with situations where they must decide between potential actions to perform based on various sources of information, including movement parameters that incur time and energy costs. Consistent with this fact, many behavioral studies indicate that decisions and actions show a high level of integration during goal-directed behavior. In particular, motor costs very often bias the choice process of human and non-human subjects facing successive decisions between actions. However, it appears as well that depending on the design in which the experiment occurs, the effect of motor costs on decisions can vary or even vanish. This suggests a contextual dependence of the influence of motor costs on decision-making. Moreover, it is not currently known whether or not the impact of motor costs on perceptual decisions depend on the difficulty of the decision. We addressed these two important issues by studying the behavior of healthy human subjects engaged in a new perceptual decision-making paradigm in which the constraint level associated with the movement executed to report a choice was volitionally chosen by the participants, and in which the difficulty of the perceptual decision to make continuously evolved depending on their motor performance. The results indicate that the level of constraint associated with a movement executed to express a perceptual decision strongly impacts the duration of these decisions, with a shortening of decisions when these are expressed by demanding movements. This influence appears most important when the decisions are difficult, but it is also present for easy decisions. We interpret this strategy as an adaptive way to optimize the participants overall rate of success at the session level.

neuroscience↗

Evidence for interacting but decoupled controls of decisions and movements in non-human primates

Many recent studies indicate that control of decisions and actions is integrated during interactive behavior. Among these, several carried out in humans and monkeys conclude that there is a co-regulation of choices and movements. Another perspective, based on human data only, proposes a decoupled control of decision duration and movement speed, allowing for instance to trade decision duration for movement duration when time pressure increases. Crucially, it is not currently known whether this ability to flexibly dissociate decision duration from movement speed is specific to humans, whether it can vary depending on the context in which a task is performed, and whether it is stable over time. These are important questions to address, especially to rely on monkey electrophysiology to infer the neural mechanisms of decision-action coordination in humans. To do so, we trained two macaque monkeys in a perceptual decision-making task and analyzed data collected over multiple behavioral sessions. Our findings reveal a strong and complex relationship between decision duration and movement vigor. Decision duration and action duration can co-vary but also "compensate" each other. Such integrated but decoupled control of decisions and actions aligns with recent studies in humans, validating the monkey model in electrophysiology as a means of inferring neural mechanisms in humans. Crucially, we demonstrate for the first time that this control can evolve with experience, in an adapted manner. Together, the present findings contribute to deepening our understanding of the integrated control of decisions and actions during interactive behavior. New & noteworthyThe mechanism by which the integrated control of decisions and actions occurs, coupled or interactive but decoupled, is debated. In the present study, we show in monkeys that decisions and actions influence each other in a decoupled way. For the first time, we also demonstrate that this control can evolve depending the subjects experience, allowing to trade movement time for decision time and limit the temporal discounting of reward value.

animal behavior and cognition↗

Integrated control of non-motor and motor efforts during decision between actions

Humans daily life is characterized by a succession of voluntary actions. Since energy resources are limited, the ability to invest the appropriate amount of effort for selecting and executing these actions is a hallmark of adapted behavior. Recent studies indicate that decisions and actions share important principles, including the exchange of temporal resources when the context requires it. In the present study, we test the hypothesis that the management of energy resources is shared between decision and action too. Healthy human subjects performed a perceptual decision task where they had to choose between two levels of effort to invest in making the decision, and report it with a reaching movement. Crucially, motor difficulty gradually increased from trial to trial depending on participants decision performance. Results indicate a relatively mild impact of the increasing motor difficulty on the choice of the non-motor (decision) effort to invest in each trial and on decision performance. By contrast, motor performance strongly decreased depending on both the motor and decisional difficulties. Together, the results support the hypothesis of an integrated management of energy resources between decision and action. They also suggest that in the context of the present task, the mutualized resources are primarily allocated to the decision-making process to the detriment of movements.

neuroscience↗

Impact of decision and action outcomes on subsequent decision and action behaviors

Speed-accuracy tradeoff adjustments in decision-making have been mainly studied separately from those in motor control. In the wild however, animals coordinate their decision and action, freely investing time in choosing versus moving given specific contexts. Recent behavioral studies support this view, indicating that humans trade decision time for movement time to maximize their global rate of reward during experimental sessions. Besides, it is established that choice outcomes impact subsequent decisions. Crucially though, whether and how a decision also influences the subsequent motor behavior, and whether and how a motor error influences the next decision is unknown. Here we address these questions by analyzing trial-to-trial changes of choice and motor behaviors in healthy human participants instructed to perform successive perceptual decisions expressed with reaching movements whose duration was either bounded or unconstrained in separate tasks. Results indicate that after a bad decision, subjects who were not constrained in their action duration decided more slowly and more accurately. Interestingly, they also shortened their subsequent movement duration by moving faster. Conversely, we found that movement errors not only influenced the speed and the accuracy of the following movement, but those of the decision as well. If the movement had to be slowed down, the decision that precedes that movement was accelerated, and vice versa. Together, these results indicate that from one trial to the next, humans are primarily concerned about determining a behavioral duration as a whole instead of optimizing each of the decision and action speed-accuracy trade-offs independently of each other.

neuroscience↗

Overlapping influences shape motor activity during hasty sensorimotor decisions

Humans and other animals are able to adjust their speed-accuracy tradeoff (SAT) at will depending on the urge to act, favoring either cautious or hasty decision policies in different contexts. An emerging view is that SAT regulation relies on influences exerting broad changes on the motor system, tuning its activity up globally when hastiness is at premium. The present study aimed to test this hypothesis. Fifty subjects performed a task involving choices between left and right index fingers, in which incorrect choices led either to a high or to a low penalty in two contexts, inciting them to emphasize either cautious or hasty policies. We applied transcranial magnetic stimulation on multiple motor representations, eliciting motor evoked potentials (MEP) in nine finger and leg muscles. MEP amplitudes allowed us to probe activity changes in the corresponding finger and leg representations, while subjects were deliberating about which index to choose. Our data indicate that hastiness entails a broad amplification of motor activity, though this amplification was limited to the chosen side. On top of this effect, we identified a local suppression of motor activity, surrounding the chosen index representation. Hence, a decision policy favoring speed over accuracy appears to rely on overlapping processes producing a broad (but not global) amplification and a surround suppression of motor activity. The latter effect may help to increase the signal-to-noise ratio of the chosen representation, as supported by single-trial correlation analyses indicating a stronger differentiation of activity changes in finger representations in the hasty context.

neuroscience↗

Dissociating the impact of movement time and energy costs on decision-making and action initiation in humans

Recent theories and data suggest that adapted behavior involves economic computations during which multiple trade-offs between reward value, accuracy requirement, energy expenditure and elapsing time are solved so as to obtain rewards as soon as possible while spending the least possible amount of energy. However, the relative impact of movement energy and duration costs on perceptual decision-making and movement initiation is poorly understood. Here, we tested 31 healthy subjects on a perceptual decision-making task in which they executed reaching movements to report probabilistic choices. In three distinct blocks of trials, the reaching time and energy costs were independently varied while decision difficulty was maintained similar at the block level. Participants also performed a fully instructed delayed-reaching (DR) task in each motor condition. Results in that DR task show that time-consuming movements extended reaction times (RTs) in most subjects, whereas energy-consuming movements led to mixed effects on RTs. In the choice task, about half of the subjects decreased their decision durations (DDs) in the time consuming condition, while the impact of energy costs on DDs were again mixed across subjects. Decision accuracy was overall similar across motor conditions. These results indicate that movement duration and, to a lesser extent, energy expenditure, idiosyncratically affect perceptual decision-making and action initiation. We propose that subjects who shortened their decisions in the time consuming condition of the choice task did so to limit a drop of their rate of reward.

neuroscience↗

Unified neural dynamics of decisions and actions in the cerebral cortex and basal ganglia

Several theoretical models suggest that deciding about actions and executing them are not completely distinct neural mechanisms but instead two modes of an integrated dynamical system. Here, we investigate this proposal by examining how neural activity unfolds during a dynamic decision-making task within the high-dimensional space defined by the activity of cells in monkey dorsal premotor (PMd), primary motor (M1), and dorsolateral prefrontal cortex (dlPFC) as well as the external and internal segments of the globus pallidus (GPe, GPi). Dimensionality reduction shows that the four strongest components of neural activity are functionally interpretable, reflecting a state transition between deliberation and commitment, the transformation of sensory evidence into a choice, and the baseline and slope of the rising urgency to decide. Analysis of the contribution of each population to these components shows differences between regions but no distinct clusters within each region. During deliberation, cortical activity unfolds on a two-dimensional "decision manifold" defined by sensory evidence and urgency, and falls off this manifold at the moment of commitment into a choice-dependent trajectory leading to movement initiation. The structure of the manifold varies between regions: In PMd it is curved, in M1 it is nearly perfectly flat, and in dlPFC it is almost entirely confined to the sensory evidence dimension. In contrast, pallidal activity during deliberation is primarily defined by urgency. We suggest that these findings reveal the distinct dynamics of different regions, supporting a unified recurrent attractor model of action selection and execution.

neuroscience↗

Humans sacrifice decision-making for action execution when a demanding control of movement is required

A growing body of evidence suggests that decision-making and action execution are governed by partly overlapping operating principles. Especially, previous work proposed that a shared decision urgency/movement vigor signal, possibly computed in the basal ganglia, coordinates both deliberation and movement durations in a way that maximizes the reward rate. Recent data support one aspect of this hypothesis, indicating that the urgency level at which a decision is made influences the vigor of the movement produced to express this choice. Here we investigated whether conversely, the motor context in which a movement is executed determines decision speed and accuracy. Twenty human subjects performed a probabilistic decision task in which perceptual choices were expressed by reaching movements toward targets whose size and distance from a starting position varied in distinct blocks of trials. We found strong evidence for an influence of the motor context on most of the subjects decision policy but contrary to the predictions of the "shared regulation" hypothesis, we observed that slow movements executed in the most demanding motor blocks in terms of accuracy were often preceded by faster and less accurate decisions compared to blocks of trials in which big targets allowed expression of choices with fast and inaccurate movements. These results suggest that decision-making and motor control are not regulated by one unique "invigoration" signal determining both decision urgency and action vigor, but more likely by independent, yet interacting, decision urgency and movement vigor signals. NEW & NOTEWORTHYRecent hypotheses propose that choices and movements share optimization principles derived from economy, possibly implemented by one unique context-dependent regulation signal determining both processes speed. In the present behavioral study conducted on human subjects, we demonstrate that action properties indeed influence perceptual decision-making, but that decision duration and action vigor are actually independently set depending on the difficulty of the movement executed to report a choice.

neuroscience↗

Dynamic changes in urgency over the course of a decision

Humans and other animals often need to balance the desire to gather sensory information (to make the best choice) with the urgency to act, facing a speed-accuracy tradeoff (SAT). Given the ubiquity of SAT across species, extensive research has been devoted to understanding the computational mechanisms allowing its regulation at different timescales, including from one context to another, and from one decision to another. However, animals must frequently change their SAT on even shorter timescales - i.e., over the course of an ongoing decision - and little is known about the mechanisms that allow such rapid adaptations. The present study aimed at addressing this issue. Human subjects performed a decision task with changing evidence. In this task, subjects received rewards for correct answers but incurred penalties for mistakes. An increase or a decrease in penalty occurring halfway through the trial promoted rapid SAT shifts, favoring speeded decisions either in the early or in the late stage of the trial. Importantly, these shifts were associated with stage-specific adjustments in the accuracy criterion exploited for committing to a choice. Those subjects who decreased the most their accuracy criterion at a given decision stage exhibited the highest gain in speed, but also the highest cost in terms of performance accuracy at that time. Altogether, the current findings offer a unique extension of previous work, by suggesting that dynamic changes in accuracy criterion allow the regulation of the SAT within the timescale of a single decision. New and noteworthyExtensive research has been devoted to understanding the mechanisms allowing the regulation of the speed-accuracy tradeoff (SAT) from one context to another and from one decision to another. Here, we show that humans can voluntarily change their SAT on even shorter timescales - i.e., over the course of a decision. These rapid SAT shifts are associated with dynamic adjustments in the accuracy criterion exploited for committing to a choice.

animal behavior and cognition↗

M1 disruption delays motor processes but not deliberation about action choices

Decisions about actions typically involve a period of deliberation that ends with the commitment to a choice and the motor processes overtly expressing that choice. Previous studies have shown that neural activity in sensorimotor areas, including the primary motor cortex (M1), correlates with deliberation features during action selection. Yet, the causal contribution of these areas to the decision process remains unclear. Here, we investigated whether M1 determines choice commitment, or whether it simply reflects decision signals coming from upstream structures and instead mainly contributes to the motor processes that follow commitment. To do so, we tested the impact of a disruption of M1 activity, induced by continuous theta burst stimulation (cTBS), on the behavior of human subjects in (1) a simple reaction time (SRT) task allowing us to estimate the duration of the motor processes and (2) a modified version of the tokens task (Cisek et al., 2009), which allowed us to estimate subjects time of commitment as well as accuracy criterion. The efficiency of cTBS was attested by a reduction in motor evoked potential amplitudes following M1 disruption, as compared to those following a sham stimulation. Furthermore, M1 cTBS lengthened SRTs, indicating that motor processes were perturbed by the intervention. Importantly, all of the behavioral results in the tokens task were similar following M1 disruption and sham stimulation, suggesting that the contribution of M1 to the deliberation process is potentially negligible. Taken together, these findings favor the view that M1 contribution is downstream of the decision process.\n\nNew and noteworthyDecisions between actions are ubiquitous in the animal realm. Deliberation during action choices entails changes in the activity of the sensorimotor areas controlling those actions, but the causal role of these areas is still often debated. Using continuous theta burst stimulation, we show that disrupting the primary motor cortex (M1) delays the motor processes that follow instructed commitment but does not alter volitional deliberation, suggesting that M1 contribution may be downstream of the decision process.

neuroscience↗