Proactive and reactive accumulation-to-bound processes compete during perceptual decisions

Standard models of perceptual decision-making postulate that a response is triggered in reaction to stimulus presentation when the accumulated stimulus evidence reaches a decision threshold. This framework excludes however the possibility that informed responses are generated proactively at a time independent of stimulus. Here, we find that, in a free reaction time auditory task in rats, reactive and proactive responses coexist, suggesting that choice selection and motor initiation, commonly viewed as serial processes, are decoupled in general. We capture this behavior by a novel model in which proactive and reactive responses are triggered whenever either of two competing processes, respectively Action Initiation or Evidence Accumulation, reaches a bound. In both types of response, the choice is ultimately informed by the Evidence Accumulation process. The Action Initiation process readily explains premature responses, contributes to urgency effects at long reaction times and mediates the slowing of the responses as animals get satiated and tired during sessions. Moreover, it successfully predicts reaction time distributions when the stimulus was either delayed, advanced or omitted. Overall, these results fundamentally extend standard models of evidence accumulation in decision making by showing that proactive and reactive processes compete for the generation of responses.

5-HT2C receptor perturbation has bidirectional influence over instrumental vigour and restraint

The serotonin (5-HT) system, particularly the 5-HT2C receptor, has consistently been implicated in behavioural control. However, while some studies have focused on the role 5-HT2C receptors play in regulating motivation to work for reward, others have highlighted its importance in response restraint. To date, it is unclear how 5-HT transmission at this receptor regulates the balance of response invigoration and restraint in anticipation of future reward. In addition, it remains to be established how 5-HT2C receptors gate the influence of internal versus cue-driven processes over reward-guided actions. To elucidate these issues, we investigated the effects of administering the 5-HT2C receptor antagonist SB242084, both systemically and directly into the nucleus accumbens core (NAcC), in rats performing a Go/No-Go task for small or large rewards. The results were compared to the administration of d-amphetamine into the NAcC, which has previously been shown to promote behavioural activation. Systemic perturbation of 5-HT2C receptors—but crucially not intra-NAcC infusions—consistently boosted rats’ performance and instrumental vigour on Go trials when they were required to act. Concomitantly, systemic administration also reduced their ability to withhold responding for rewards on No-Go trials, particularly late in the holding period. Notably, these effects were often apparent only when the reward on offer was small. By contrast, inducing a hyperdopaminergic state in the NAcC with d-amphetamine strongly impaired response restraint on No-Go trials both early and late in the holding period, as well as speeding action initiation. Together, these findings suggest that 5-HT2C receptor transmission, outside the NAcC, shapes the vigour of ongoing goal-directed action as well as the likelihood of responding as a function of expected reward.

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 distinct blocks of trials, the reaching duration (“Time” condition) and energy (“Effort” condition) costs were independently varied compared to a “Reference” block, while decision difficulty was maintained similar at the block level. Participants also performed a simple delayed-reaching (DR) task aimed at estimating movement initiation duration in each motor condition. Results in that DR task show that long duration movements extended reaction times (RTs) in most subjects, whereas energy-consuming movements led to mixed effects on RTs. In the decision task, about half of the subjects decreased their decision durations (DDs) in the Time condition, while the impact of energy 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 choices in the time-consuming condition of the decision task did so to limit a drop of reward rate.

Opportunity cost determines free-operant action initiation latency and predicts apathy

Background Apathy, a disabling and poorly understood neuropsychiatric symptom, is characterised by impaired self-initiated behaviour. It has been hypothesised that the opportunity cost of time (OCT) may be a key computational variable linking self-initiated behaviour with motivational status. OCT represents the amount of reward which is foregone per second if no action is taken. Using a novel behavioural task and computational modelling, we investigated the relationship between OCT, self-initiation and apathy. We predicted that higher OCT would engender shorter action latencies, and that individuals with greater sensitivity to OCT would have higher behavioural apathy. Methods We modulated the OCT in a novel task called the ‘Fisherman Game’, Participants freely chose when to self-initiate actions to either collect rewards, or on occasion, to complete non-rewarding actions. We measured the relationship between action latencies, OCT and apathy for each participant across two independent non-clinical studies, one under laboratory conditions (n = 21) and one online (n = 90). ‘Average-reward’ reinforcement learning was used to model our data. We replicated our findings across both studies. Results We show that the latency of self-initiation is driven by changes in the OCT. Furthermore, we demonstrate, for the first time, that participants with higher apathy showed greater sensitivity to changes in OCT in younger adults. Our model shows that apathetic individuals experienced greatest change in subjective OCT during our task as a consequence of being more sensitive to rewards. Conclusions Our results suggest that OCT is an important variable for determining free-operant action initiation and understanding apathy.

Realism Matters. Eye movements in VR reveal prior tool knowledge, intended interaction, and end-state comfort planning

Seminal studies on human cognitive behavior have been conducted in controlled laboratory settings, demonstrating that visual attention is mainly goal-directed and allocated based on the action performed. However, it is unclear how far these results generalize to cognition in more naturalistic settings. The present study investigates active inference processes revealed by eye movements during interaction with familiar and novel tools with two levels of realism of the performed action. We presented participants with 3D tool models that were either familiar or unfamiliar, oriented congruent or incongruent to their handedness, and asked participants to interact with them by either lifting or using. Importantly, we used the same experimental design in two setups. In the first experiment, participants interacted with a VR controller; in the second, they performed the task with a more realistic interaction setup that allowed differentiated hand and finger movements. We used linear mixed models to determine the odds of fixations on the tool effector vs. handle before action initiation. The results show that participants fixate more on the tool's effector part before action initiation during the use task for unfamiliar tools. Furthermore, under more natural interaction conditions, subjects fixate more on the tool's handle as a function of the tool's orientation, well before the action was executed. Secondly, the spatial viewing bias on the tool reveals early fixations are associated with the task and familiarity of the tools. In contrast, later fixations are associated with the manual planning of the interaction. In sum, the findings from the experiments suggest that fixations are made in a task-oriented way to extract the mechanical properties of the tools to plan the intended action well before action initiation. Further, in more natural conditions, fixations are made towards proximal goals of optimally planning the grasp even when the perceived action on the tools is identical. Thus, the realism of the action in a virtual environment seems to be as important as the sensory stimulation.

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.

Developmental differences across the lifespan in the use of perceptual information to guide action-based decisions

Perceptual information about unfolding events is important for guiding decisions about when and how to move in real-world action situations. As an exemplary case, road-crossing is a perceptual-motor task where age has been shown to be a strong predictor of risk due to errors in action-based decisions. The present study investigated age differences between three age groups (Children: 10–12 years old; Adults: 19–39 years old; Older Adults: 65 + year olds) in the use of perceptual information for selection, timing, and control of action when crossing a two-way street in an immersive, interactive virtual reality environment. Adults and children selected gaps to cross that were consistent with the use of a time-based information variable (tau), whereas older adults tuned less into the time-based variable (tau) to guide road-crossing decisions. For action initiation and control, children and adults also showed a strong ability to precisely time their entry with respect to the lead vehicle maximising the available time to cross and coordinating walking movements with the tail vehicle to ensure they were not on a collision course. In contrast, older adults delayed action initiation and showed difficulty coordinating self-movement with the approaching vehicle. This study and its results tie together age-based differences in the three components of action decision-making (selection, timing and control) within a unified framework based on perceptual information. The implications of these age-related differences in action decisions and crossing behaviours are discussed in the context of road safety.