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Estimation errors (difference between estimated and true ball position) plotted against performance errors (difference between true ball position and target) for a typical participant. The slope of the regression across conditions (black line) indicates the degree to which estimates of performance were biased.
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Apathy is a debilitating syndrome that is associated with reduced goal-directed behavior. Although apathy is common and detrimental to prognosis in many neuropsychiatric diseases, its underlying mechanisms remain controversial. We propose a new model of apathy, in the context of Bayesian theories of brain function, whereby actions require predictio...
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The current literature has largely highlighted a deficit of effort-based decision-making for reward in schizophrenia. However, not all studies have dissociated effort from reward, while other studies emphasize that difficulty is the main determinant of effort rather than reward. In this study, 33 individuals with schizophrenia and 32 heal...
Apathy and fatigue have distinct aetiologies, yet can manifest in phenotypically similar ways. In particular, each can give rise to diminished goal-directed behaviour, which is often cited as a key characteristic of both traits. An important issue therefore is whether currently available approaches are capable of distinguishing between them. Here,...
Deficits in goal-directed decision making and motivation are hallmark characteristics of several neuropsychiatric disorders, including schizophrenia (SZ) and major depressive disorder (MDD). Studies using effort based decision making tasks have shown that both patients with SZ and MDD invest less physical effort in order to obtain rewards. However,...
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... In both the physical and cognitive domains, a particular set of tasks may be experienced as more or less effortful depending on several factors that are independent from the actual work required: 1) self-motivational determinants (19,20), 2) affective and emotional determinants (21,22), 3) an individual's own sense of competence or self-efficacy (23,24), 4) an individual's levels of fatigue (25)(26)(27), 5) the subjective attitude to the task or to its potential outcome (28), 6) the anticipation of how worthwhile the activity is (29,30), 7) the amount of time available for the task (31,32), 8) the ongoing feedback provided about task performance (33), and 9) one's beliefs about the outcome of their actions (34)(35)(36). Therefore, a given level of cognitive work may be associated with varying subjective experiences of effort, which suggests that these are two separate constructs ( Figure 1). ...
... The aforementioned interlocking mechanisms play a role in real social interaction; for example, counterfactually overthinking potential interpersonal actions and their consequences might diminish one's confidence in interpersonal actions, leading to more passive or apathetic behavior (Hezemans et al., 2020). This, in turn, would lead to experiencing the social situation as more volatile, which in turn promotes the propensity to enact behaviors whose action outcomes are highly predictable. ...
Social neuroscience has often been criticized for approaching the investigation of the neural processes that enable social interaction and cognition from a passive, detached, third-person perspective, without involving any real-time social interaction. With the emergence of second-person neuroscience, investigators have uncovered the unique complexity of neural-activation patterns in actual, real-time interaction. Social cognition that occurs during social interaction is fundamentally different from that unfolding during social observation. However, it remains unclear how the neural correlates of social interaction are to be interpreted. Here, we leverage the active-inference framework to shed light on the mechanisms at play during social interaction in second-person neuroscience studies. Specifically, we show how counterfactually rich mutual predictions, real-time bodily adaptation, and policy selection explain activation in components of the default mode, salience, and frontoparietal networks of the brain, as well as in the basal ganglia. We further argue that these processes constitute the crucial neural processes that underwrite bona fide social interaction. By placing the experimental approach of second-person neuroscience on the theoretical foundation of the active-inference framework, we inform the field of social neuroscience about the mechanisms of real-life interactions. We thereby contribute to the theoretical foundations of empirical second-person neuroscience.
... Could a failure to monitor the outcome of their actions, reflected in a shift from exploitation to exploration, be driven by a pure disorder of encoding the outcome of their decisions in the task? If the precision of the outcome's value signal is degraded 40 , exploration is likely to be a passive, secondary consequence of greater decision noise 52 . Alternatively, an inability to exploit knowledge gained from learning the value of each option could arise from a failure of using this at the point at which the decision is being made. ...
Apathy is a common and disabling complication of Parkinson's disease characterised by reduced goal-directed behaviour. Several studies have reported dysfunction within pre-frontal cortical regions and projections from brainstem nuclei whose neuromodulators include dopamine, serotonin and noradrenaline. Work in animal and human neuroscience have confirmed contributions of these neuromodulators on aspects of motivated decision making. Specifically, non-dopaminergic neuromodulators, influence decisions to explore alternative courses of action or persist in an existing strategy to achieve a rewarding goal.
Building upon this work, we hypothesised that Apathy in Parkinson's disease should be associated with a failure to adequately monitor and make adaptive choices when the rewarding outcome of decisions are uncertain. Using a 4-armed restless bandit reinforcement learning task, we studied decision making in 75 volunteers; 53 patients with Parkinson's disease, with and without clinical apathy, and 22 age matched healthy controls. Patients with Apathy exhibited impaired ability to choose the highest value bandit. Task performance predicted an individual patient's apathy severity measured using the Lille Apathy Rating scale (R = -0.46, p<0.001). Computational modelling of the patient's choices confirmed the apathy group made decisions that that were indifferent to the learnt value of the options, consistent with previous reports of reward insensitivity. Further analysis demonstrated a shift away from exploiting the highest value option and a reduction in perseveration which also correlated with apathy scores (R = -0.5, p<0.001).
We went on to acquire fMRI in 59 volunteers; a group of 19 patients with and 20 without apathy and 20 age matched controls performing the restless bandit task. Analysis of the fMRI signal at the point of reward feedback confirmed diminished signal within ventromedial prefrontal cortex in Parkinson's disease, which was more marked in Apathy, but not predictive of their individual Apathy severity. Using a model-based categorisation of choice type, decisions to explore lower value bandits in the apathy group activated pre-frontal cortex to a similar degree to the age-matched controls. In contrast, Parkinson's patients without apathy demonstrated significantly increased activation across a distributed thalamo-cortical network. Enhanced activity in the thalamus predicted individual apathy severity across both patient groups and exhibited functional connectivity with dorsal anterior cingulate cortex and anterior insula.
Given that task performance in patients without apathy was no different to the age-matched controls, we interpret the recruitment of this network as a possible compensatory mechanism, which compensates against symptomatic manifestation of apathy in Parkinson's disease.
... 115 For example, apathy would result from reduced precision in the predicted consequences of actions, leading to diminished goal-directed behaviour. 115,117 Impulsive behaviours would follow from reduced precision in the amount of information sampled before a decision is made. 118 The degradation of conceptual knowledge, including social context, would by analogy impair initiation or selection of socially appropriate actions. ...
Running title: Impaired social behaviour in frontotemporal dementia Keywords: frontotemporal dementia, semantic dementia, social-semantic knowledge, social control, social behaviour, anterior temporal lobe, orbitofrontal cortex 2 Abbreviations: bvFTD = behavioural-variant frontotemporal dementia; SD = semantic dementia; ATL = anterior temporal lobe; OFC = orbitofrontal cortex, ACC = anterior cingulate cortex 3 Abstract Impaired social cognition is a core deficit of frontotemporal dementia (FTD). It is most commonly associated with the behavioural-variant of FTD, with atrophy of the orbitofrontal and ventromedial prefrontal cortex. However, social cognitive changes are also common in semantic dementia, with atrophy centred on the anterior temporal lobes. The impairment of social behaviour in FTD has typically been attributed to damage to the orbitofrontal cortex and/or temporal poles and/or the uncinate fasciculus that connects them. However, the relative contribution of each region is unresolved. In this review, we present a unified neurocognitive model of controlled social behaviour that not only explains the observed impairment of social behaviours in FTD, but also assimilates findings from other patient groups, comparative neurology, and normative cognitive neuroscience. We propose that impaired social behaviour results from damage to two cognitively-and anatomically-distinct components. The first component is social-semantic knowledge, supported by the anterior temporal lobes bilaterally. The second component is social control, supported by the orbitofrontal cortex, medial frontal cortex and ventrolateral frontal cortex, which interact with social-semantic knowledge to guide and shape social behaviour. 4
... We believe that this concept is applicable both for an individual psychological characteristic or personality state, and to denote a common objectified social line that characterizes certain anomic transformations of modern society. These transformations are often manifested through: changes in the value system, inconsistencies of social behavior by cultural, social and legal norms adopted in society, social stratification or polarization of society, maintaining tension in interpersonal relationships, the prevalence of various forms of deviation, deepening a sense of uncertainty, depreciation of significant norms of behavior (Hezemans et al., 2020;Zhelnina, 2020). The use of the concept of "social apathy" will also allow us to consider the problems of anomie at another, more global, interdisciplinary level. ...
The key to the successful and effective development of any society is the socio-psychological well-being of the population and personality, based on certain legal and philosophical concepts. Modern society experiences a kind of civilizational, philosophical, legal and socio-psychological crisis - the transformation of norms and behavior, against the background of which various forms of deviation are clearly manifested. As a result, in the context of the transformation of society, for a more complete and deeper study of the characteristics of human behavior, it becomes necessary to understand the causes of their occurrence. This methodological position allows first of all describing the mental world of a person who acts in the frames of the certain understanding and perception of social-psychological and legal norms of behavior. In this context, the procedure of psychological and legal-philosophical reconstruction of scientific concept of anomie is used as a methodological tool, which is aimed at analyzing various manifestations of the psyche of the personality and its anomic characteristics.
... We previously proposed that apathy is a result of the dependence of motivated behaviour on the relative precision of prior beliefs about action outcomes [43]. With predictive processing, the brain optimises a probabilistic model of its environment, minimising 'surprise' or prediction error via action and perception [44,45]. ...
... There would be an apparent 'acceptance' of the state of the world, even if discordant with goals. In support of this hypothesis, trait apathy is negatively correlated with prior precision of outcomes: more apathetic individuals have less precise prior beliefs [43]. Crucially, precision weighting has been associated with neurotransmitter systems that include noradrenaline [50][51][52][53]. ...
... We administered a visuomotor task (adapted from Hezemans et al. [43]) that involved effortful, goal-directed behaviour, and required participants to estimate their own performance. For each trial, participants pressed on a force sensor for 3 seconds using the index finger of their dominant hand, to subsequently trigger a ballistic ball movement on the screen, aiming for the ball to stop on the target. ...
Apathy is a debilitating feature of many neuropsychiatric diseases, that is typically described as a reduction of goal-directed behaviour. Despite its prevalence and prognostic importance, the mechanisms underlying apathy remain controversial. Degeneration of the locus coeruleus-noradrenaline system is known to contribute to motivational deficits, including apathy. In healthy people, noradrenaline has been implicated in signalling the uncertainty of expectations about the environment. We proposed that noradrenergic deficits contribute to apathy by modulating the relative weighting of prior beliefs about action outcomes. We tested this hypothesis in the clinical context of Parkinson’s disease, given its associations with apathy and noradrenergic dysfunction. Participants with mild-to-moderate Parkinson’s disease ( N = 17) completed a randomised double-blind, placebo-controlled, crossover study with 40 mg of the noradrenaline reuptake inhibitor atomoxetine. Prior weighting was inferred from psychophysical analysis of performance in an effort-based visuomotor task, and was confirmed as negatively correlated with apathy. Locus coeruleus integrity was assessed in vivo using magnetisation transfer imaging at ultra-high field 7T. The effect of atomoxetine depended on locus coeruleus integrity: participants with a more degenerate locus coeruleus showed a greater increase in prior weighting on atomoxetine versus placebo. The results indicate a contribution of the noradrenergic system to apathy and potential benefit from noradrenergic treatment of people with Parkinson’s disease, subject to stratification according to locus coeruleus integrity. More broadly, these results reconcile emerging predictive processing accounts of the role of noradrenaline in goal-directed behaviour with the clinical symptom of apathy and its potential pharmacological treatment.
... However, illustrating the interconnectedness between phases of goal-directed behavior, noradrenergic activity also signals information about effort costs (to influence the value of a potential behavioral option) 76 and plays a role in learned expectations and beliefs about action costs. 77 Furthermore, it modulates shifting behavior between exploitative or exploratory modes, 78 with widespread noradrenergic activity reconfiguring brain networks to promote changes in goal-directed behavior. 79 ...
A caregiver's all‐too‐familiar narrative ‐ “He doesn't think through what he does, but mostly he does nothing.” Apathy and impulsivity, debilitating and poorly understood, commonly co‐occur in Huntington's disease (HD). HD is a neurodegenerative disease with manifestations bridging clinical neurology and psychiatry. In addition to movement and cognitive symptoms, neurobehavioral disturbances, particularly apathy and impulsivity, are prevalent features of HD, occurring early in the disease course, often worsening with disease progression, and substantially reducing quality of life. Treatments remain limited, in part because of limited mechanistic understanding of these behavioral disturbances. However, emerging work within the field of decision‐making neuroscience and beyond points to common neurobiological mechanisms underpinning these seemingly disparate problems. These insights bridge the gap between underlying disease pathology and clinical phenotype, offering new treatment strategies, novel behavioral and physiological biomarkers of HD, and deeper understanding of human behavior. In this review, we apply the neurobiological framework of cost‐benefit decision making to the problems of apathy and impulsivity in HD. Through this decision‐making lens, we develop a mechanistic model that elucidates the occurrence of these behavioral disturbances and points to potential treatment strategies and crucial research priorities. © 2022 The Authors. Movement Disorders published by Wiley Periodicals LLC on behalf of International Parkinson Movement Disorder Society.
... The idea that aberrant precision control disrupts the ability to infer accurate self-and world models-thereby triggering abnormal perceptions and beliefs-has been linked to various conditions such as depressions, autism and apathy(see Heinz & Schlagenhauf, 2010; Van de Cruys, Evers, Van der Hallen, Van Eylen, & Boets, Corlett & Fletcher, 2015Friston, 2017, Sterzer et al., 2018, Smith, Lane, Parr, & Friston, 2019Stephan, Manjaly, Mathys, Weber, Paliwal, & Gard, 2016;Hezemans, Wolpe, & Rowe, 2020). ...
This paper considers the phenomenology of depersonalisation disorder, in relation to predictive processing and its associated pathophysiology. To do this, we first establish a few mechanistic tenets of predictive processing that are necessary to talk about phenomenal transparency, mental action, and self as subject. We briefly review the important role of ‘predicting precision’ and how this affords mental action and the loss of phenomenal transparency. We then turn to sensory attenuation and the phenomenal consequences of (pathophysiological) failures to attenuate or modulate sensory precision. We then consider this failure in the context of depersonalisation disorder. The key idea here is that depersonalisation disorder reflects the remarkable capacity to explain perceptual engagement with the world via the hypothesis that “I am an embodied perceiver, but I am not in control of my perception”. We suggest that individuals with depersonalisation may believe that ‘another agent’ is controlling their thoughts, perceptions or actions, while maintaining full insight that the ‘other agent’ is ‘me’ (the self). Finally, we rehearse the predictions of this formal analysis, with a special focus on the psychophysical and physiological abnormalities that may underwrite the phenomenology of depersonalisation.
... The take home message is that motivational processes, and consequently behavior and learning, will be modulated according to the degree of confidence in action-outcome contingencies (control). A recent active inference model tested this hypothesis further to show that apathy (or lack of motivated action) results from reduced prior precision about the consequences of actions (Hezemans et al., 2020). ...
Survival requires the implementation of adaptive changes that demand energy resources. The efficient regulation of energetic resources thus plays a critical role in enabling systems to adapt to the demands of their internal and external environments. The framework of active inference explains how living organisms can build probabilistic models that enable them to predict, track, and regulate energy expenditure in the short and long run. The aim of the paper is to characterize the physiological changes that accompany stress, and the relationship between these changes and the loss of confidence in a system’s predictions about its internal and external milieu—ultimately manifesting as depressive symptomatology. We identify the systems that underwrite goal-directed behavior, and the neuroendocrine and immunological systems, as the hierarchical controller that regulates energy resources. In doing so, we establish an etiological pathway from allostatic overload to depression via active inference.
... Presently, few studies have directly examined the effect of physical exertion on metacognitive function (Palmer et al., 2019), despite recognition that it is a process fundamental to self-regulation during prolonged physical exertion (Brick et al., 2015;Brick et al., 2020;see Brick et al., 2016). Future examination of the metacognitive basis of exertional fatigue under the present proposal could see the use of a combination of metacognitive assessments alongside the modelling of precision estimates from behavioural responses (Hezemans et al., 2020;Wolpe et al., 2014). Interestingly, using this behavioural modelling approach, apathy-a construct often correlated with fatiguehas recently been associated with a low precision-weighting of performance predictions (Hezemans et al., 2020). ...
... Future examination of the metacognitive basis of exertional fatigue under the present proposal could see the use of a combination of metacognitive assessments alongside the modelling of precision estimates from behavioural responses (Hezemans et al., 2020;Wolpe et al., 2014). Interestingly, using this behavioural modelling approach, apathy-a construct often correlated with fatiguehas recently been associated with a low precision-weighting of performance predictions (Hezemans et al., 2020). ...
Fatigue is a common experience in both health and disease. Yet, pathological (i.e., prolonged or chronic) and transient (i.e., exertional) fatigue symptoms are traditionally considered distinct, compounding a separation between interested research fields within the study of fatigue. Within the clinical neurosciences, nascent frameworks position pathological fatigue as a product of inference derived through hierarchical predictive processing. The metacognitive theory of dyshomeostasis (Stephan et al., 2016) states that pathological fatigue emerges from the metacognitive mechanism in which the detection of persistent mismatches between prior interoceptive predictions and ascending sensory evidence (i.e., prediction error) signals low evidence for internal generative models, which undermine an agent’s feeling of mastery over the body and is thus experienced phenomenologically as fatigue. Although acute, transient subjective symptoms of exertional fatigue have also been associated with increasing interoceptive prediction error, the dynamic computations that underlie its development have not been clearly defined. Here, drawing on the metacognitive theory of dyshomeostasis, we extend this account to offer an explicit description of the development of fatigue during extended periods of (physical) exertion. Accordingly, it is proposed that a loss of certainty or confidence in control predictions in response to persistent detection of prediction error features as a common foundation for the conscious experience of both pathological and nonpathological fatigue.
