Stephen M Fleming

California Institute of Technology, Pasadena, CA, USA

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Publications (21)129.91 Total impact

  • Article: The development of metacognitive ability in adolescence.
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    ABSTRACT: Introspection, or metacognition, is the capacity to reflect on our own thoughts and behaviours. Here, we investigated how one specific metacognitive ability (the relationship between task performance and confidence) develops in adolescence, a period of life associated with the emergence of self-concept and enhanced self-awareness. We employed a task that dissociates objective performance on a visual task from metacognitive ability in a group of 56 participants aged between 11 and 41years. Metacognitive ability improved significantly with age during adolescence, was highest in late adolescence and plateaued going into adulthood. Our results suggest that awareness of one's own perceptual decisions shows a prolonged developmental trajectory during adolescence.
    Consciousness and Cognition 01/2013; 22(1):264-271. · 2.31 Impact Factor
  • Article: Confidence in value-based choice.
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    ABSTRACT: Decisions are never perfect, with confidence in one's choices fluctuating over time. How subjective confidence and valuation of choice options interact at the level of brain and behavior is unknown. Using a dynamic model of the decision process, we show that confidence reflects the evolution of a decision variable over time, explaining the observed relation between confidence, value, accuracy and reaction time. As predicted by our dynamic model, we show that a functional magnetic resonance imaging signal in human ventromedial prefrontal cortex (vmPFC) reflects both value comparison and confidence in the value comparison process. Crucially, individuals varied in how they related confidence to accuracy, allowing us to show that this introspective ability is predicted by a measure of functional connectivity between vmPFC and rostrolateral prefrontal cortex. Our findings provide a mechanistic link between noise in value comparison and metacognitive awareness of choice, enabling us both to want and to express knowledge of what we want.
    Nature Neuroscience 12/2012; · 15.53 Impact Factor
  • Article: Is choice-induced preference change long lasting?
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    ABSTRACT: The idea that decisions alter preferences has had a considerable influence on the field of psychology and underpins cognitive dissonance theory. Yet it is unknown whether choice-induced changes in preferences are long lasting or are transient manifestations seen in the immediate aftermath of decisions. In the research reported here, we investigated whether these changes in preferences are fleeting or stable. Participants rated vacation destinations before making hypothetical choices between destinations, immediately afterward, and 2.5 to 3 years later. We found that choices altered preferences both immediately after being made and after the delay. These changes could not be accounted for by participants' preexisting preferences, and they occurred only when participants made the choices themselves. Our findings provide evidence that making a decision can lead to enduring change in preferences.
    Psychological Science 08/2012; 23(10):1123-9. · 4.43 Impact Factor
  • Article: Testosterone induces off-line perceptual learning.
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    ABSTRACT: RATIONALE: Perceptual learning operates on distinct timescales. How different neuromodulatory systems impact on learning across these different timescales is poorly understood. OBJECTIVES: Here, we test the causal impact of a novel influence on perceptual learning, the androgen hormone testosterone, across distinct timescales. METHODS: In a double-blind, placebo- controlled, cross-over study with testosterone, subjects undertook a simple contrast detection task during training sessions on two separate days. RESULTS: On placebo, there was no learning either within training sessions or between days, except for a fast, rapidly saturating, improvement early on each testing day. However, testosterone caused "off-line" learning, with no learning seen within training sessions, but a marked performance improvement over the days between sessions. This testosterone-induced learning occurred in the absence of changes in subjective confidence or introspective accuracy. CONCLUSIONS: Our findings show that testosterone influences perceptual learning on a timescale consistent with an influence on "off-line" consolidation processes.
    Psychopharmacologia 06/2012; · 4.08 Impact Factor
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    Article: Metacognition: computation, biology and function.
    Stephen M Fleming, Raymond J Dolan, Christopher D Frith
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    ABSTRACT: Many complex systems maintain a self-referential check and balance. In animals, such reflective monitoring and control processes have been grouped under the rubric of metacognition. In this introductory article to a Theme Issue on metacognition, we review recent and rapidly progressing developments from neuroscience, cognitive psychology, computer science and philosophy of mind. While each of these areas is represented in detail by individual contributions to the volume, we take this opportunity to draw links between disciplines, and highlight areas where further integration is needed. Specifically, we cover the definition, measurement, neurobiology and possible functions of metacognition, and assess the relationship between metacognition and consciousness. We propose a framework in which level of representation, order of behaviour and access consciousness are orthogonal dimensions of the conceptual landscape.
    Philosophical Transactions of The Royal Society B Biological Sciences 05/2012; 367(1594):1280-6. · 6.40 Impact Factor
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    Article: The neural basis of metacognitive ability.
    Stephen M Fleming, Raymond J Dolan
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    ABSTRACT: Ability in various cognitive domains is often assessed by measuring task performance, such as the accuracy of a perceptual categorization. A similar analysis can be applied to metacognitive reports about a task to quantify the degree to which an individual is aware of his or her success or failure. Here, we review the psychological and neural underpinnings of metacognitive accuracy, drawing on research in memory and decision-making. These data show that metacognitive accuracy is dissociable from task performance and varies across individuals. Convergent evidence indicates that the function of the rostral and dorsal aspect of the lateral prefrontal cortex (PFC) is important for the accuracy of retrospective judgements of performance. In contrast, prospective judgements of performance may depend upon medial PFC. We close with a discussion of how metacognitive processes relate to concepts of cognitive control, and propose a neural synthesis in which dorsolateral and anterior prefrontal cortical subregions interact with interoceptive cortices (cingulate and insula) to promote accurate judgements of performance.
    Philosophical Transactions of The Royal Society B Biological Sciences 05/2012; 367(1594):1338-49. · 6.40 Impact Factor
  • Article: Prefrontal contributions to metacognition in perceptual decision making.
    Stephen M Fleming, Josefien Huijgen, Raymond J Dolan
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    ABSTRACT: Neuroscience has made considerable progress in understanding the neural substrates supporting cognitive performance in a number of domains, including memory, perception, and decision making. In contrast, how the human brain generates metacognitive awareness of task performance remains unclear. Here, we address this question by asking participants to perform perceptual decisions while providing concurrent metacognitive reports during fMRI scanning. We show that activity in right rostrolateral prefrontal cortex (rlPFC) satisfies three constraints for a role in metacognitive aspects of decision-making. Right rlPFC showed greater activity during self-report compared to a matched control condition, activity in this region correlated with reported confidence, and the strength of the relationship between activity and confidence predicted metacognitive ability across individuals. In addition, functional connectivity between right rlPFC and both contralateral PFC and visual cortex increased during metacognitive reports. We discuss these findings in a theoretical framework where rlPFC re-represents object-level decision uncertainty to facilitate metacognitive report.
    Journal of Neuroscience 05/2012; 32(18):6117-25. · 7.11 Impact Factor
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    Article: An Online Neural Substrate for Sense of Agency.
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    ABSTRACT: "Sense of agency" refers to the feeling of controlling an external event through one's own action. On one influential view, sense of agency is inferred after an action, by "retrospectively" comparing actual effects of actions against their intended effects. In contrast, a "prospective" component of agency, generated during action selection, and in advance of knowing the actual effect, has received less attention. Here, we used functional magnetic resonance imaging to investigate prospective contributions of action selection processes to sense of agency. To do so, we dissociated action selection processes from action-outcome matching, by subliminally priming responses to a target. We found that participants experienced greater control over action effects when the action was compatibly versus incompatibly primed. Thus, compatible primes facilitated action selection processing, in turn boosting sense of agency over a subsequent effect. This prospective contribution of action selection processes to sense of agency was accounted for by exchange of signals across a prefrontal-parietal network. Specifically, we found that the angular gyrus (AG) monitors signals relating to action selection in dorsolateral prefrontal cortex, to prospectively inform subjective judgments of control over action outcomes. Online monitoring of these signals by AG might provide the subject with a subjective marker of volition, prior to action itself.
    Cerebral Cortex 04/2012; · 6.54 Impact Factor
  • Article: Human responses to unfairness with primary rewards and their biological limits.
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    ABSTRACT: Humans bargaining over money tend to reject unfair offers, whilst chimpanzees bargaining over primary rewards of food do not show this same motivation to reject. Whether such reciprocal fairness represents a predominantly human motivation has generated considerable recent interest. We induced either moderate or severe thirst in humans using intravenous saline, and examined responses to unfairness in an Ultimatum Game with water. We ask if humans also reject unfair offers for primary rewards. Despite the induction of even severe thirst, our subjects rejected unfair offers. Further, our data provide tentative evidence that this fairness motivation was traded-off against the value of the primary reward to the individual, a trade-off determined by the subjective value of water rather than by an objective physiological metric of value. Our data demonstrate humans care about fairness during bargaining with primary rewards, but that subjective self-interest may limit this fairness motivation.
    Scientific Reports 01/2012; 2:593.
  • Article: Neural segregation of objective and contextual aspects of fairness.
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    ABSTRACT: Perception of fairness can influence outcomes in human exchange. However, an inherent subjectivity in attribution renders it difficult to manipulate fairness experimentally. Here using a modified ultimatum game, within a varying social context, we induced a bias in human subjects' acceptance of objectively identical offers. To explain this fairness-related behavior, we use a computational model to specify metrics for the objective and contextual aspects of fairness, testing for correlations between these model parameters and brain activity determined using functional magnetic resonance imaging. We show that objective social inequality, as defined by our model, is tracked in posterior insula cortex. Crucially, this inequality is integrated with social context in posterior and mid-insula, consistent with construction of a fairness motivation that flexibly adapted to the social environment. We suggest that the dual importance of objective and contextual aspects to fairness we highlight might explain seemingly inconsistent societal phenomena, including public attitudes to income disparities.
    Journal of Neuroscience 04/2011; 31(14):5244-52. · 7.11 Impact Factor
  • Article: A regret-induced status quo bias.
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    ABSTRACT: A suboptimal bias toward accepting the status quo option in decision-making is well established behaviorally, but the underlying neural mechanisms are less clear. Behavioral evidence suggests the emotion of regret is higher when errors arise from rejection rather than acceptance of a status quo option. Such asymmetry in the genesis of regret might drive the status quo bias on subsequent decisions, if indeed erroneous status quo rejections have a greater neuronal impact than erroneous status quo acceptances. To test this, we acquired human fMRI data during a difficult perceptual decision task that incorporated a trial-to-trial intrinsic status quo option, with explicit signaling of outcomes (error or correct). Behaviorally, experienced regret was higher after an erroneous status quo rejection compared with acceptance. Anterior insula and medial prefrontal cortex showed increased blood oxygenation level-dependent signal after such status quo rejection errors. In line with our hypothesis, a similar pattern of signal change predicted acceptance of the status quo on a subsequent trial. Thus, our data link a regret-induced status quo bias to error-related activity on the preceding trial.
    Journal of Neuroscience 03/2011; 31(9):3320-7. · 7.11 Impact Factor
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    Article: Relating inter-individual differences in metacognitive performance on different perceptual tasks.
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    ABSTRACT: Human behavior depends on the ability to effectively introspect about our performance. For simple perceptual decisions, this introspective or metacognitive ability varies substantially across individuals and is correlated with the structure of focal areas in prefrontal cortex. This raises the possibility that the ability to introspect about different perceptual decisions might be mediated by a common cognitive process. To test this hypothesis, we examined whether inter-individual differences in metacognitive ability were correlated across two different perceptual tasks where individuals made judgments about different and unrelated visual stimulus properties. We found that inter-individual differences were strongly correlated between the two tasks for metacognitive ability but not objective performance. Such stability of an individual's metacognitive ability across different perceptual tasks indicates a general mechanism supporting metacognition independent of the specific task.
    Consciousness and Cognition 01/2011; 20(4):1787-92. · 2.31 Impact Factor
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    Article: Effects of emotional preferences on value-based decision-making are mediated by mentalizing and not reward networks.
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    ABSTRACT: Real-world decision-making often involves social considerations. Consequently, the social value of stimuli can induce preferences in choice behavior. However, it is unknown how financial and social values are integrated in the brain. Here, we investigated how smiling and angry face stimuli interacted with financial reward feedback in a stochastically rewarded decision-making task. Subjects reliably preferred the smiling faces despite equivalent reward feedback, demonstrating a socially driven bias. We fit a Bayesian reinforcement learning model to factor the effects of financial rewards and emotion preferences in individual subjects, and regressed model predictions on the trial-by-trial fMRI signal. Activity in the subcallosal cingulate and the ventral striatum, both involved in reward learning, correlated with financial reward feedback, whereas the differential contribution of social value activated dorsal temporo-parietal junction and dorsal anterior cingulate cortex, previously proposed as components of a mentalizing network. We conclude that the impact of social stimuli on value-based decision processes is mediated by effects in brain regions partially separable from classical reward circuitry.
    Journal of Cognitive Neuroscience 10/2010; 23(9):2197-210. · 5.18 Impact Factor
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    Article: Relating introspective accuracy to individual differences in brain structure.
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    ABSTRACT: The ability to introspect about self-performance is key to human subjective experience, but the neuroanatomical basis of this ability is unknown. Such accurate introspection requires discriminating correct decisions from incorrect ones, a capacity that varies substantially across individuals. We dissociated variation in introspective ability from objective performance in a simple perceptual-decision task, allowing us to determine whether this interindividual variability was associated with a distinct neural basis. We show that introspective ability is correlated with gray matter volume in the anterior prefrontal cortex, a region that shows marked evolutionary development in humans. Moreover, interindividual variation in introspective ability is also correlated with white-matter microstructure connected with this area of the prefrontal cortex. Our findings point to a focal neuroanatomical substrate for introspective ability, a substrate distinct from that supporting primary perception.
    Science 09/2010; 329(5998):1541-3. · 31.20 Impact Factor
  • Article: Effects of category-specific costs on neural systems for perceptual decision-making.
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    ABSTRACT: Perceptual judgments are often biased by prospective losses, leading to changes in decision criteria. Little is known about how and where sensory evidence and cost information interact in the brain to influence perceptual categorization. Here we show that prospective losses systematically bias the perception of noisy face-house images. Asymmetries in category-specific cost were associated with enhanced blood-oxygen-level-dependent signal in a frontoparietal network. We observed selective activation of parahippocampal gyrus for changes in category-specific cost in keeping with the hypothesis that loss functions enact a particular task set that is communicated to visual regions. Across subjects, greater shifts in decision criteria were associated with greater activation of the anterior cingulate cortex (ACC). Our results support a hypothesis that costs bias an intermediate representation between perception and action, expressed via general effects on frontal cortex, and selective effects on extrastriate cortex. These findings indicate that asymmetric costs may affect a neural implementation of perceptual decision making in a similar manner to changes in category expectation, constituting a step toward accounting for how prospective losses are flexibly integrated with sensory evidence in the brain.
    Journal of Neurophysiology 03/2010; 103(6):3238-47. · 3.32 Impact Factor
  • Article: Overcoming status quo bias in the human brain.
    Stephen M Fleming, Charlotte L Thomas, Raymond J Dolan
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    ABSTRACT: Humans often accept the status quo when faced with conflicting choice alternatives. However, it is unknown how neural pathways connecting cognition with action modulate this status quo acceptance. Here we developed a visual detection task in which subjects tended to favor the default when making difficult, but not easy, decisions. This bias was suboptimal in that more errors were made when the default was accepted. A selective increase in subthalamic nucleus (STN) activity was found when the status quo was rejected in the face of heightened decision difficulty. Analysis of effective connectivity showed that inferior frontal cortex, a region more active for difficult decisions, exerted an enhanced modulatory influence on the STN during switches away from the status quo. These data suggest that the neural circuits required to initiate controlled, nondefault actions are similar to those previously shown to mediate outright response suppression. We conclude that specific prefrontal-basal ganglia dynamics are involved in rejecting the default, a mechanism that may be important in a range of difficult choice scenarios.
    Proceedings of the National Academy of Sciences 03/2010; 107(13):6005-9. · 9.68 Impact Factor
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    Article: Effects of loss aversion on post-decision wagering: implications for measures of awareness.
    Stephen M Fleming, Raymond J Dolan
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    ABSTRACT: Wagering contingent on a previous decision, or post-decision wagering, has recently been proposed to measure conscious awareness. Whilst intuitively appealing, it remains unclear whether economic context interacts with subjective confidence and how such interactions might impact on the measurement of awareness. Here we propose a signal detection model which predicts that advantageous wagers placed on the identity of preceding stimuli are affected by loss aversion, despite stimulus visibility remaining constant. This pattern of predicted results was evident in a psychophysical task where we independently manipulated perceptual and economic factors. Changes in wagering behaviour induced by changes in wager size were largely driven by changes in criterion, consistent with the model. However, for near-threshold stimuli, a reduction in wagering efficiency was also evident, consistent with an apparent but potentially illusory decrease in awareness of the stimulus. These findings challenge an assertion that post-decision wagering provides a direct index of subjective awareness.
    Consciousness and Cognition 12/2009; 19(1):352-63. · 2.31 Impact Factor
  • Article: When the brain changes its mind: flexibility of action selection in instructed and free choices.
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    ABSTRACT: The neural mechanisms underlying the selection and initiation of voluntary actions in the absence of external instructions are poorly understood. These mechanisms are usually investigated using a paradigm where different movement choices are self-generated by a participant on each trial. These "free choices" are compared with "instructed choices," in which a stimulus informs subjects which action to make on each trial. Here, we introduce a novel paradigm to investigate these modes of action selection, by measuring brain processes evoked by an instruction to either reverse or maintain free and instructed choices in the period before a "go" signal. An unpredictable instruction to change a response plan had different effects on free and instructed choices. In instructed trials, change cues evoked a larger P300 than no-change cues, leading to a significant interaction of choice and change condition. Free-choice trials displayed a trend toward the opposite pattern. These results suggest a difference between updating of free and instructed action choices. We propose a theoretical framework for internally generated action in which representations of alternative actions remain available until a late stage in motor preparation. This framework emphasizes the high modifiability of voluntary action.
    Cerebral Cortex 03/2009; 19(10):2352-60. · 6.54 Impact Factor
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    Article: Shaping what we see: pinning down the influence of value on perceptual judgements.
    Stephen M Fleming
    Frontiers in Human Neuroscience 02/2009; 3:9. · 2.34 Impact Factor
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    Article: Subliminal priming of actions influences sense of control over effects of action
    Dorit Wenke, Stephen M. Fleming, Patrick Haggard
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    ABSTRACT: The experience of controlling one’s own actions, and through them events in the outside world, is a pervasive feature of human mental life. Two experiments investigated the relation between this sense of control and the internal processes involved in action selection and cognitive control. Action selection was manipulated by subliminally priming left or right keypress actions in response to a supraliminal visual target. The action caused the display of one of several colours as an action effect. The specific colour shown depended on whether the participant’s action was compatible or incompatible with the preceding subliminal prime, and not on the prime identity alone. Unlike previous studies, therefore, the primes did not predict the to-be-expected action effects. Participants rated how much control they experienced over the different colours. Replicating previous results, compatible primes facilitated responding, whereas incompatible primes interfered with response selection. Crucially, priming also modulated the sense of control over action effects: participants experienced more control over colours produced by actions that were compatible with the preceding prime than over colours associated with prime-incompatible actions. Experiment 2 showed that this effect was not solely due to priming modulating action–effect contingencies. These results suggest that sense of control is linked to processes of selection between alternative actions, being strongest when selection is smooth and uncontested.
    Cognition.