Neural fatigue by passive induction: repeated stimulus exposure results in cognitive fatigue and altered representations in task-relevant networks.

Cognitive fatigue is defined by a reduced capacity to perform mental tasks. Despite its pervasiveness, the underlying neural mechanisms remain elusive. Specifically, it is unclear whether prolonged effort affects performance through alterations in over-worked task-relevant neuronal assemblies. Our paradigm based on repeated passive visual stimulation discerns fatigue effects from the influence of motivation, skill and boredom. We induced performance loss and observed parallel alterations in the neural blueprint of the task, by mirroring behavioral performance with multivariate neuroimaging techniques (MVPA) that afford a subject-specific approach. Crucially, functional areas that responded the most to repeated stimulation were also the most affected. Finally, univariate analysis revealed clusters displaying significant disruption within the extrastriate visual cortex. In sum, here we show that repeated stimulation impacts the implicated brain areas' activity and causes tangible behavioral repercussions, providing evidence that cognitive fatigue can result from local, functional, disruptions in the neural signal induced by protracted recruitment.

Fatigue and Human Performance: An Updated Framework.

Fatigue has been defined differently in the literature depending on the field of research. The inconsistent use of the term fatigue complicated scientific communication, thereby limiting progress towards a more in-depth understanding of the phenomenon. Therefore, Enoka and Duchateau (Med Sci Sports Exerc 48:2228-38, 2016, [3]) proposed a fatigue framework that distinguishes between trait fatigue (i.e., fatigue experienced by an individual over a longer period of time) and motor or cognitive task-induced state fatigue (i.e., self-reported disabling symptom derived from the two interdependent attributes performance fatigability and perceived fatigability). Thereby, performance fatigability describes a decrease in an objective performance measure, while perceived fatigability refers to the sensations that regulate the integrity of the performer. Although this framework served as a good starting point to unravel the psychophysiology of fatigue, several important aspects were not included and the interdependence of the mechanisms driving performance fatigability and perceived fatigability were not comprehensively discussed. Therefore, the present narrative review aimed to (1) update the fatigue framework suggested by Enoka and Duchateau (Med Sci Sports Exerc 48:2228-38, 2016, [3]) pertaining the taxonomy (i.e., cognitive performance fatigue and perceived cognitive fatigue were added) and important determinants that were not considered previously (e.g., effort perception, affective valence, self-regulation), (2) discuss the mechanisms underlying performance fatigue and perceived fatigue in response to motor and cognitive tasks as well as their interdependence, and (3) provide recommendations for future research on these interactions. We propose to define motor or cognitive task-induced state fatigue as a psychophysiological condition characterized by a decrease in motor or cognitive performance (i.e., motor or cognitive performance fatigue, respectively) and/or an increased perception of fatigue (i.e., perceived motor or cognitive fatigue). These dimensions are interdependent, hinge on different determinants, and depend on body homeostasis (e.g., wakefulness, core temperature) as well as several modulating factors (e.g., age, sex, diseases, characteristics of the motor or cognitive task). Consequently, there is no single factor primarily determining performance fatigue and perceived fatigue in response to motor or cognitive tasks. Instead, the relative weight of each determinant and their interaction are modulated by several factors.

Passive visual stimulation induces fatigue under conditions of high arousal elicited by auditory tasks.

Theories of cognitive fatigue disagree on whether performance decrement is caused by motivational or functional alterations. Here, drawing inspiration from the habituation and visual adaptation literature, we tested the assumption that keeping neural networks active for an extensive period of time entails consequences at the subjective and objective level-the defining characteristics of fatigue-when confounds such as motivation, boredom, and level of skill are controlled. In Experiment 1, we revealed that passive visual stimulation affected the performance of a subsequent task that was carried out in the same portion of visual space. While under conditions of low cognitive load and arousal, participants improved their performance in the stimulated quadrant; the reverse was observed under high arousal conditions. This latter performance decrement correlated also with the reported subjective level of fatigue and occurred while neural responses to the saturating stimulus remained constant, as assessed through steady-state EEG. In subsequent experiments, we replicated and further characterized this performance deterioration effect, revealing its specificity to the stimulated eye and stimulus orientation. Across the three experiments, the decrease in performance was correlated with pupil-linked arousal, suggesting its mediating effect in this phenomenon. In sum, we show that repeated stimulation of neural networks under high-arousal conditions leads to their altered functional performance, a mechanism which may play a role in the development of global cognitive fatigue. (PsycInfo Database Record (c) 2022 APA, all rights reserved).

Pupil size variations reveal covert shifts of attention induced by numbers.

The pupil light response is more than a pure reflexive mechanism that reacts to the amount of light entering the eye. The pupil size may also react to the luminance of objects lying in the visual periphery, revealing the locus of covert attention. In the present study, we took advantage of this response to study the spatial coding of abstract concepts with no physical counterpart: numbers. The participants' gaze was maintained fixed in the middle of a screen whose left and right parts were dark or bright, and variations in pupil size were recorded during an auditory number comparison task. The results showed that small numbers accentuated pupil dilation when the darker part of the screen was on the left, while large numbers accentuated pupil dilation when the darker part of the screen was on the right. This finding provides direct evidence for covert attention shifts on a left-to-right oriented mental spatial representation of numbers. From a more general perspective, it shows that the pupillary response to light is subject to modulation from spatial attention mechanisms operating on mental contents.

The predictive role of eye movements in mental arithmetic.

Behavioural studies have suggested that number manipulation involves shifting attention along a left-to-right oriented continuum. However, these studies provide little evidence about the time course of attention shifts during number processing. We used an eye-tracker with high spatio-temporal resolution to measure eye movements during the mental solving of addition (e.g., 43 + 4) and subtraction problems (e.g., 53 - 6), as a proxy for the rightward and leftward attention shifts that accompany these operations. A first difference in eye position was observed as soon as the operator was heard: the hearing of "plus" shifted the eye rightward compared to "minus". A second difference was observed later between problem offset and response onset: addition shifted the eye rightward and upward compared to subtraction, suggesting that the space used to represent the problem is bidimensional. Further analyses confirmed the fast deployment of spatial attention and evidenced its relationship with the carrying and borrowing procedures triggered by the problem presentation. The predictive role of horizontal eye movements, in particular, is essential to understand how attention contributes to narrow down the range of plausible answers. We propose that attention illuminates significant portions of the numerical continuum anticipatively to guide the search of the answer and facilitate the implementation of solving procedures in verbal working memory.

Subthalamic stimulation breaks the balance between distal and axial signs in Parkinson's disease.

In Parkinson's disease (PD), the effects of both Ldopa and subthalamic deep brain stimulation (STN-DBS) are known to change cost-valuation. However, this was mostly studied through reward-effort task involving distal movements, while axial effort, less responsive to treatments, have been barely studied. Thus, our objective was to compare the influence of both Ldopa and STN-DBS on cost-valuation between two efforts modalities: vowel production (as an example of axial movement) and hand squeezing (as an example of distal movement). Twelve PD patients were recruited to participate in this study. The task consisted in deciding whether to accept or reject trials based on a reward-effort trade-off. Participants performed two blocks with hand squeezing, and two with vowel production, in the four treatment conditions (Ldopa On/Off; STN-DBS On/Off). We found that STN-DBS changed the ratio difference between hand and phonation efforts. Vowel production effort was estimated easier to perform with STN-DBS alone, and harder when associated with Ldopa. The difference between hand and phonation efforts was correlated with quality of life in Off/Off and On Ldopa alone conditions, and with impulsive assessment On STN-DBS alone. We highlighted that STN-DBS could introduce an imbalance between the actual motor impairments and their subjective costs. With this finding, we also suggest paying particular attention to the different treatment effects that should be expected for axial and distal movement dysfunctions.

Conscious awareness of motor fluidity improves performance and decreases cognitive effort in sequence learning.

Motor skill learning is improved when participants are instructed to judge after each trial whether their performed movements have reached maximal fluidity. Consequently, the conscious awareness of this maximal fluidity can be classified as a genuine learning factor for motor sequences. However, it is unknown whether this effect of conscious awareness on motor learning could be mediated by the increased cognitive effort that may accompany such judgment making. The main aim of this study was to test this hypothesis in comparing two groups with, and without, the conscious awareness of the maximal fluidity. To assess the possible involvement of cognitive effort, we have recorded the pupillary dilation to the task, which is well-known to increase in proportion to cognitive effort. Results confirmed that conscious awareness indeed improved motor sequence learning of the trained sequence specifically. Pupil dilation was smaller during trained than during novel sequence performance, indicating that sequence learning decreased the cognitive cost of sequence execution. However, we found that in the group that had to judge on their maximal fluidity, pupil dilation during sequence production was smaller than in the control group, indicating that the motor improvement induced by the fluidity judgment does not involve additional cognitive effort. We discuss these results in the context of motor learning and cognitive effort theories.

Mental fatigue correlates with depression of task-related network and augmented DMN activity but spares the reward circuit.

Long-lasting and demanding cognitive activity typically leads to mental fatigue (MF). Indirect evidence suggests that MF may be caused by altered motivational processes. Here, we hypothesized that if MF consists in an alteration of motivational states, brain functional changes induced by MF could specifically affect the brain motivation circuit. In order to test this hypothesis, we devised a functional neuroimaging protocol to detect altered brain activity in reward-related brain regions in relation to cognitively induced mental fatigue. Twenty-five healthy participants underwent a FATIGUE and a CONTROL session on different days. In the FATIGUE session, MF was induced by performing a demanding cognitive task (adapted Stroop task) during 90 min, whereas in the CONTROL session, participants were asked to read magazines for the same period of time. We measured the neural consequences of the MF induction during a working memory task (Missing Number task) while modulating extrinsic motivation with block-wise variations in monetary reward. We also tracked participants' momentary fatigue, anxiety state and intrinsic motivation prior to and following the MF inducement and measurement. Accuracy on the Missing Number Task was lower in the FATIGUE than in the CONTROL condition. Furthermore, subjective MF, but not its behavioral manifestations, was associated with hypoactivity of the task-evoked neural responses. Importantly, activity in regions modulated by reward showed no differences between FATIGUE and CONTROL sessions. In parallel, subjective MF correlated with increased on-task activity and resting-state functional connectivity in the default mode network. These results indicate that subjective mental fatigue is not associated with altered activity in the brain motivation circuit but rather with hypoactivity in task-specific brain regions as well as relative increases of activity and connectivity in the default mode network during and after the task.

Active sensing with artificial neural networks.

The fitness of behaving agents depends on their knowledge of the environment, which demands efficient exploration strategies. Active sensing formalizes exploration as reduction of uncertainty about the current state of the environment. Despite strong theoretical justifications, active sensing has had limited applicability due to difficulty in estimating information gain. Here we address this issue by proposing a linear approximation to information gain and by implementing efficient gradient-based action selection within an artificial neural network setting. We compare information gain estimation with state of the art, and validate our model on an active sensing task based on MNIST dataset. We also propose an approximation that exploits the amortized inference network, and performs equally well in certain contexts.

Preparing to React: A Behavioral Study on the Interplay between Proactive and Reactive Action Inhibition.

Motor preparation, based on one's goals and expectations, allows for prompt reactions to stimulations from the environment. Proactive and reactive inhibitory mechanisms modulate this preparation and interact to allow a flexible control of responses. In this study, we investigate these two control mechanisms with an ad hoc cued Go/NoGo Simon paradigm in a within-subjects design, and by measuring subliminal motor activities through electromyographic recordings. Go cues instructed participants to prepare a response and wait for target onset to execute it (Go target) or inhibit it (NoGo target). Proactive inhibition keeps the prepared response in check, hence preventing false alarms. Preparing the cue-coherent effector in advance speeded up responses, even when it turned out to be the incorrect effector and reactive inhibition was needed to perform the action with the contralateral one. These results suggest that informative cues allow for the investigation of the interaction between proactive and reactive action inhibition. Partial errors' analysis suggests that their appearance in compatible conflict-free trials depends on cue type and prior preparatory motor activity. Motor preparation plays a key role in determining whether proactive inhibition is needed to flexibly control behavior, and it should be considered when investigating proactive/reactive inhibition.

Information Rate in Humans during Visuomotor Tracking.

Previous investigations concluded that the human brain's information processing rate remains fundamentally constant, irrespective of task demands. However, their conclusion rested in analyses of simple discrete-choice tasks. The present contribution recasts the question of human information rate within the context of visuomotor tasks, which provides a more ecologically relevant arena, albeit a more complex one. We argue that, while predictable aspects of inputs can be encoded virtually free of charge, real-time information transfer should be identified with the processing of surprises. We formalise this intuition by deriving from first principles a decomposition of the total information shared by inputs and outputs into a feedforward, predictive component and a feedback, error-correcting component. We find that the information measured by the feedback component, a proxy for the brain's information processing rate, scales with the difficulty of the task at hand, in agreement with cost-benefit models of cognitive effort.

Eye pupil signals information gain.

In conditions of constant illumination, the eye pupil diameter indexes the modulation of arousal state and responds to a large breadth of cognitive processes, including mental effort, attention, surprise, decision processes, decision biases, value beliefs, uncertainty, volatility, exploitation/exploration trade-off, or learning rate. Here, I propose an information theoretic framework that has the potential to explain the ensemble of these findings as reflecting pupillary response to information processing. In short, updates of the brain's internal model, quantified formally as the Kullback-Leibler (KL) divergence between prior and posterior beliefs, would be the common denominator to all these instances of pupillary dilation to cognition. I show that stimulus presentation leads to pupillary response that is proportional to the amount of information the stimulus carries about itself and to the quantity of information it provides about other task variables. In the context of decision making, pupil dilation in relation to uncertainty is explained by the wandering of the evidence accumulation process, leading to large summed KL divergences. Finally, pupillary response to mental effort and variations in tonic pupil size are also formalized in terms of information theory. On the basis of this framework, I compare pupillary data from past studies to simple information-theoretic simulations of task designs and show good correspondance with data across studies. The present framework has the potential to unify the large set of results reported on pupillary dilation to cognition and to provide a theory to guide future research.

Pupil-Linked Arousal Responds to Unconscious Surprisal.

Pupil size under constant illumination reflects brain arousal state, and dilates in response to novel information, or surprisal. Whether this response can be observed regardless of conscious perception is still unknown. In the present study, male and female adult humans performed an implicit learning task across a series of three experiments. We measured pupil and brain-evoked potentials to stimuli that violated transition statistics but were not relevant to the task. We found that pupil size dilated following these surprising events, in the absence of awareness of transition statistics, and only when attention was allocated to the stimulus. These pupil responses correlated with central potentials, evoking an anterior cingulate origin. Arousal response to surprisal outside the scope of conscious perception points to the fundamental relationship between arousal and information processing and indicates that pupil size can be used to track the progression of implicit learning.SIGNIFICANCE STATEMENT Pupil size dilates following increase in mental effort, surprise, or more generally global arousal. However, whether this response arises as a conscious response or reflects a more fundamental mechanism outside the scrutiny of awareness is still unknown. Here, we demonstrate that unexpected changes in the environment, even when processed unconsciously and without being relevant to the task, lead to an increase in arousal levels as reflected by the pupillary response. Further, we show that the concurrent electrophysiological response shares similarities with mismatch negativity, suggesting the involvement of anterior cingulate cortex. All in all, our results establish novel insights about the mechanisms driving global arousal levels, and it provides new possibilities for reliably measuring unconscious processes.

Learning and forgetting using reinforced Bayesian change detection.

Agents living in volatile environments must be able to detect changes in contingencies while refraining to adapt to unexpected events that are caused by noise. In Reinforcement Learning (RL) frameworks, this requires learning rates that adapt to past reliability of the model. The observation that behavioural flexibility in animals tends to decrease following prolonged training in stable environment provides experimental evidence for such adaptive learning rates. However, in classical RL models, learning rate is either fixed or scheduled and can thus not adapt dynamically to environmental changes. Here, we propose a new Bayesian learning model, using variational inference, that achieves adaptive change detection by the use of Stabilized Forgetting, updating its current belief based on a mixture of fixed, initial priors and previous posterior beliefs. The weight given to these two sources is optimized alongside the other parameters, allowing the model to adapt dynamically to changes in environmental volatility and to unexpected observations. This approach is used to implement the "critic" of an actor-critic RL model, while the actor samples the resulting value distributions to choose which action to undertake. We show that our model can emulate different adaptation strategies to contingency changes, depending on its prior assumptions of environmental stability, and that model parameters can be fit to real data with high accuracy. The model also exhibits trade-offs between flexibility and computational costs that mirror those observed in real data. Overall, the proposed method provides a general framework to study learning flexibility and decision making in RL contexts.

Effects of subthalamic nucleus stimulation and levodopa on decision-making in Parkinson's disease.

BACKGROUND: Parkinson's disease (PD) is frequently associated with behavioral disorders, particularly within the spectrum of motivated behaviors such as apathy or impulsivity. Both pharmacological and neurosurgical treatments have an impact on these impairments. However, there still is controversy as to whether subthalamic nucleus deep brain stimulation (STN-DBS) can cause or reduce impulsive behaviors. OBJECTIVES: We aimed to identify the influence of functional surgery on decision-making processes in PD. METHODS: We studied 13 PD patients and 13 healthy controls. The experimental task involved squeezing a dynamometer with variable force to obtain rewards of various values under four conditions: without treatment, with l-dopa or subthalamic stimulation alone, and with both l-dopa and subthalamic stimulation. Statistical analyses consisted of generalized linear mixed models including treatment condition, reward value, level of effort, and their interactions. We analyzed acceptance rate (the percentage of accepted trials), decision time, and force applied. RESULTS: Comparatively to controls, patients without treatment exhibited lower acceptance rate and force applied. Patients under l-dopa alone did not exhibit increased acceptance rate. With subthalamic stimulation, either with or without added l-dopa, all measures were improved so that patients' behaviors were undistinguishable from healthy controls'. CONCLUSIONS: Our study shows that l-dopa administration does not fully restore cost-benefit decision-making processes, whereas STN-DBS fully normalizes patients' behaviors. These findings suggest that dopamine is partly involved in cost-benefit valuation, and that STN-DBS can have a beneficial effect on motivated behaviors in PD and may improve certain forms of impulsive behaviors. © 2019 International Parkinson and Movement Disorder Society.

Implicit visual cues tune oscillatory motor activity during decision-making.

Motor decisions entails a buildup of choice-selective activity in the motor cortex. The rate of this buildup crucially depends on the amount of evidence favoring the selection of each action choice in the visual environment. Though numerous studies have characterized how sensory evidence drives motor activity when processed consciously, very little is known about the neural mechanisms that underlie the integration of implicit sources of information. Here, we used electroencephalography to investigate the impact of implicit visual cues on response-locked potentials and oscillatory activity in the motor cortex during decision-making. Subjects were required to select between left and right index finger responses according to the motion direction of a cloud of dots presented in one of three possible colors. Unbeknown to the participants, the color cue could bring evidence either in favor of or against the selection of the correct response. Implicit color cues tuned choice-selective oscillatory activity in the low beta range (16-25 Hz), boosting the buildup of contralateral activity when evidence favored the selection of the correct action, while weakening it when evidence biased against the correct response. This modulation of oscillatory activity influenced the speed at which the correct action was eventually chosen. Implicit cues also altered oscillatory activity in a non-selective way in the low frequency oscillation (1-7 Hz) and high beta ranges (25-35 Hz), impacting both contralateral and ipsilateral activity. The current findings yield a critical extension of prior observations by indicating that the integration of both explicit and implicit sources of evidence tunes oscillatory motor activity during decision-making.

Cognitive task avoidance correlates with fatigue-induced performance decrement but not with subjective fatigue.

Mentally demanding tasks feel effortful and are usually avoided. Furthermore, prolonged cognitive engagement leads to mental fatigue, consisting of subjective feeling of exhaustion and decline in performance. Despite the intuitive characterization of fatigue as an increase in subjective effort perception, the effect of fatigue on effort cost has never been tested experimentally. To this end, sixty participants in 2 separate experiments underwent a forced-choice working memory task following either a fatigue-inducing (i.e. cognitive task involving working memory, conflict and switch costs) or a control manipulation. We measured fatigue in terms of subjective feeling and performance decrement and assessed effort in terms of subjective perception and task avoidance. Subjects exhibited only weak avoidance of the working memory task, with stronger influence of reward than task difficulty on their decisions. In addition, we found that task avoidance did not systematically change following the fatigue manipulation but that variations in task avoidance correlated with fatigue-induced performance decline. The other measures of fatigue and effort were unrelated to each other. Our findings suggest that subjective fatigue may develop independently of task avoidance and suggest an "anticipatory regulation" model in which fatigue urges subjects to stop in anticipation of possible, future adverse consequences.

An information-theoretic perspective on the costs of cognition.

In statistics and machine learning, model accuracy is traded off with complexity, which can be viewed as the amount of information extracted from the data. Here, we discuss how cognitive costs can be expressed in terms of similar information costs, i.e. as a function of the amount of information required to update a person's prior knowledge (or internal model) to effectively solve a task. We then examine the theoretical consequences that ensue from this assumption. This framework naturally explains why some tasks - for example, unfamiliar or dual tasks - are costly and permits to quantify these costs using information-theoretic measures. Finally, we discuss brain implementation of this principle and show that subjective cognitive costs can originate either from local or global capacity limitations on information processing or from increased rate of metabolic alterations. These views shed light on the potential adaptive value of cost-avoidance mechanisms.

Strong Conscious Cues Suppress Preferential Gaze Allocation to Unconscious Cues.

Visual attention allows relevant information to be selected for further processing. Both conscious and unconscious visual stimuli can bias attentional allocation, but how these two types of visual information interact to guide attention remains unclear. In this study, we explored attentional allocation during a motion discrimination task with varied motion strength and unconscious associations between stimuli and cues. Participants were instructed to report the motion direction of two colored patches of dots. Unbeknown to participants, dot colors were sometimes informative of the correct response. We found that subjects learnt the associations between colors and motion direction but failed to report this association using the questionnaire filled at the end of the experiment, confirming that learning remained unconscious. The eye movement analyses revealed that allocation of attention to unconscious sources of information occurred mostly when motion coherence was low, indicating that unconscious cues influence attentional allocation only in the absence of strong conscious cues. All in all, our results reveal that conscious and unconscious sources of information interact with each other to influence attentional allocation and suggest a selection process that weights cues in proportion to their reliability.

Visuomotor Correlates of Conflict Expectation in the Context of Motor Decisions.

Many behaviors require choosing between conflicting options competing against each other in visuomotor areas. Such choices can benefit from top-down control processes engaging frontal areas in advance of conflict when it is anticipated. Yet, very little is known about how this proactive control system shapes the visuomotor competition. Here, we used electroencephalography in human subjects (male and female) to identify the visual and motor correlates of conflict expectation in a version of the Eriksen Flanker task that required left or right responses according to the direction of a central target arrow surrounded by congruent or incongruent (conflicting) flankers. Visual conflict was either highly expected (it occurred in 80% of trials; mostly incongruent blocks) or very unlikely (20% of trials; mostly congruent blocks). We evaluated selective attention in the visual cortex by recording target- and flanker-related steady-state visual-evoked potentials (SSVEPs) and probed action selection by measuring response-locked potentials (RLPs) in the motor cortex. Conflict expectation enhanced accuracy in incongruent trials, but this improvement occurred at the cost of speed in congruent trials. Intriguingly, this behavioral adjustment occurred while visuomotor activity was less finely tuned: target-related SSVEPs were smaller while flanker-related SSVEPs were higher in mostly incongruent blocks than in mostly congruent blocks, and incongruent trials were associated with larger RLPs in the ipsilateral (nonselected) motor cortex. Hence, our data suggest that conflict expectation recruits control processes that augment the tolerance for inappropriate visuomotor activations (rather than processes that downregulate their amplitude), allowing for overflow activity to occur without having it turn into the selection of an incorrect response.SIGNIFICANCE STATEMENT Motor choices made in front of discordant visual information are more accurate when conflict can be anticipated, probably due to the engagement of top-down control from frontal areas. How this control system modulates activity within visual and motor areas is unknown. Here, we show that, when control processes are recruited in anticipation of conflict, as evidenced by higher midfrontal theta activity, visuomotor activity is less finely tuned: visual processing of the goal-relevant location was reduced and the motor cortex displayed more inappropriate activations, compared with when conflict was unlikely. We argue that conflict expectation is associated with an expansion of the distance-to-selection threshold, improving accuracy while the need for online control of visuomotor activity is reduced.