The neural basis of consciousness.

Consciousness has evolved and is a feature of all animals with sufficiently complex nervous systems. It is, therefore, primarily a problem for biology, rather than physics. In this review, I will consider three aspects of consciousness: level of consciousness, whether we are awake or in a coma; the contents of consciousness, what determines how a small amount of sensory information is associated with subjective experience, while the rest is not; and meta-consciousness, the ability to reflect upon our subjective experiences and, importantly, to share them with others. I will discuss and compare current theories of the neural and cognitive mechanisms involved in producing these three aspects of consciousness and conclude that the research in this area is flourishing and has already succeeded to delineate these mechanisms in surprising detail.

Independent Neural Computation of Value from Other People's Confidence.

Expectation of reward can be shaped by the observation of actions and expressions of other people in one's environment. A person's apparent confidence in the likely reward of an action, for instance, makes qualities of their evidence, not observed directly, socially accessible. This strategy is computationally distinguished from associative learning methods that rely on direct observation, by its use of inference from indirect evidence. In twenty-three healthy human subjects, we isolated effects of first-hand experience, other people's choices, and the mediating effect of their confidence, on decision-making and neural correlates of value within ventromedial prefrontal cortex (vmPFC). Value derived from first-hand experience and other people's choices (regardless of confidence) were indiscriminately represented across vmPFC. However, value computed from agent choices weighted by their associated confidence was represented with specificity for ventromedial area 10. This pattern corresponds to shifts of connectivity and overlapping cognitive processes along a posterior-anterior vmPFC axis. Task behavior and self-reported self-reliance for decision-making in other social contexts correlated. The tendency to conform in other social contexts corresponded to increased activation in cortical regions previously shown to respond to social conflict in proportion to subsequent conformity (Campbell-Meiklejohn et al., 2010). The tendency to self-monitor predicted a selectively enhanced response to accordance with others in the right temporoparietal junction (rTPJ). The findings anatomically decompose vmPFC value representations according to computational requirements and provide biological insight into the social transmission of preference and reassurance gained from the confidence of others. SIGNIFICANCE STATEMENT: Decades of research have provided evidence that the ventromedial prefrontal cortex (vmPFC) signals the satisfaction we expect from imminent actions. However, we have a surprisingly modest understanding of the organization of value across this substantial and varied region. This study finds that using cues of the reliability of other peoples' knowledge to enhance expectation of personal success generates value correlates that are anatomically distinct from those concurrently computed from direct, personal experience. This suggests that representation of decision values in vmPFC is suborganized according to the underlying computation, consistent with what we know about the anatomical heterogeneity of the region. These results also provide insight into the observational learning process by which someone else's confidence can sway and reassure our choices.

Equality bias impairs collective decision-making across cultures.

We tend to think that everyone deserves an equal say in a debate. This seemingly innocuous assumption can be damaging when we make decisions together as part of a group. To make optimal decisions, group members should weight their differing opinions according to how competent they are relative to one another; whenever they differ in competence, an equal weighting is suboptimal. Here, we asked how people deal with individual differences in competence in the context of a collective perceptual decision-making task. We developed a metric for estimating how participants weight their partner's opinion relative to their own and compared this weighting to an optimal benchmark. Replicated across three countries (Denmark, Iran, and China), we show that participants assigned nearly equal weights to each other's opinions regardless of true differences in their competence-even when informed by explicit feedback about their competence gap or under monetary incentives to maximize collective accuracy. This equality bias, whereby people behave as if they are as good or as bad as their partner, is particularly costly for a group when a competence gap separates its members.

Interplay Between Conceptual Expectations and Movement Predictions Underlies Action Understanding.

Recent accounts of understanding goal-directed action underline the importance of a hierarchical predictive architecture. However, the neural implementation of such an architecture remains elusive. In the present study, we used functional neuroimaging to quantify brain activity associated with predicting physical movements, as they were modulated by conceptual-expectations regarding the purpose of the object involved in the action. Participants observed object-related actions preceded by a cue that generated both conceptual goal expectations and movement goal predictions. In 2 tasks, observers judged whether conceptual or movement goals matched or mismatched the cue. At the conceptual level, expected goals specifically recruited the posterior cingulate cortex, irrespectively of the task and the perceived movement goal. At the movement level, neural activation of the parieto-frontal circuit, including inferior frontal gyrus and the inferior parietal lobe, reflected unpredicted movement goals. Crucially, this movement prediction error was only present when the purpose of the involved object was expected. These findings provide neural evidence that prior conceptual expectations influence processing of physical movement goals and thereby support the hierarchical predictive account of action processing.

Ten years of Nature Reviews Neuroscience: insights from the highly cited.

To celebrate the first 10 years of Nature Reviews Neuroscience, we invited the authors of the most cited article of each year to look back on the state of their field of research at the time of publication and the impact their article has had, and to discuss the questions that might be answered in the next 10 years. This selection of highly cited articles provides interesting snapshots of the progress that has been made in diverse areas of neuroscience. They show the enormous influence of neuroimaging techniques and highlight concepts that have generated substantial interest in the past decade, such as neuroimmunology, social neuroscience and the 'network approach' to brain function. These advancements will pave the way for further exciting discoveries that lie ahead.

Frontal alpha oscillations distinguish leaders from followers: multivariate decoding of mutually interacting brains.

Successful social interactions rely upon the abilities of two or more people to mutually exchange information in real-time, while simultaneously adapting to one another. The neural basis of social cognition has mostly been investigated in isolated individuals, and more recently using two-person paradigms to quantify the neuronal dynamics underlying social interaction. While several studies have shown the relevance of understanding complementary and mutually adaptive processes, the neural mechanisms underlying such coordinative behavioral patterns during joint action remain largely unknown. Here, we employed a synchronized finger-tapping task while measuring dual-EEG from pairs of human participants who either mutually adjusted to each other in an interactive task or followed a computer metronome. Neurophysiologically, the interactive condition was characterized by a stronger suppression of alpha and low-beta oscillations over motor and frontal areas in contrast to the non-interactive computer condition. A multivariate analysis of two-brain activity to classify interactive versus non-interactive trials revealed asymmetric patterns of the frontal alpha-suppression in each pair, during both task anticipation and execution, such that only one member showed the frontal component. Analysis of the behavioral data showed that this distinction coincided with the leader-follower relationship in 8/9 pairs, with the leaders characterized by the stronger frontal alpha-suppression. This suggests that leaders invest more resources in prospective planning and control. Hence our results show that the spontaneous emergence of leader-follower relationships in dyadic interactions can be predicted from EEG recordings of brain activity prior to and during interaction. Furthermore, this emphasizes the importance of investigating complementarity in joint action.

Perceiving is believing: a Bayesian approach to explaining the positive symptoms of schizophrenia.

Advances in cognitive neuroscience offer us new ways to understand the symptoms of mental illness by uniting basic neurochemical and neurophysiological observations with the conscious experiences that characterize these symptoms. Cognitive theories about the positive symptoms of schizophrenia--hallucinations and delusions--have tended to treat perception and belief formation as distinct processes. However, recent advances in computational neuroscience have led us to consider the unusual perceptual experiences of patients and their sometimes bizarre beliefs as part of the same core abnormality--a disturbance in error-dependent updating of inferences and beliefs about the world. We suggest that it is possible to understand these symptoms in terms of a disturbed hierarchical Bayesian framework, without recourse to separate considerations of experience and belief.

Continuous theta-burst stimulation demonstrates a causal role of premotor homunculus in action understanding.

Although it is well established that regions of premotor cortex (PMC) are active during action observation, it remains controversial whether they play a causal role in action understanding. In the experiment reported here, we used off-line continuous theta-burst stimulation (cTBS) to investigate this question. Participants received cTBS over the hand and lip areas of left PMC, in separate sessions, before completing a pantomime-recognition task in which half of the trials contained pantomimed hand actions, and half contained pantomimed mouth actions. The results reveal a double dissociation: Participants were less accurate in recognizing pantomimed hand actions after receiving cTBS over the hand area than over the lip area and less accurate in recognizing pantomimed mouth actions after receiving cTBS over the lip area than over the hand area. This finding constrains theories of action understanding by showing that somatotopically organized regions of PMC contribute causally to action understanding and, thus, that the mechanisms underpinning action understanding and action performance overlap.

Does interaction matter? Testing whether a confidence heuristic can replace interaction in collective decision-making.

In a range of contexts, individuals arrive at collective decisions by sharing confidence in their judgements. This tendency to evaluate the reliability of information by the confidence with which it is expressed has been termed the 'confidence heuristic'. We tested two ways of implementing the confidence heuristic in the context of a collective perceptual decision-making task: either directly, by opting for the judgement made with higher confidence, or indirectly, by opting for the faster judgement, exploiting an inverse correlation between confidence and reaction time. We found that the success of these heuristics depends on how similar individuals are in terms of the reliability of their judgements and, more importantly, that for dissimilar individuals such heuristics are dramatically inferior to interaction. Interaction allows individuals to alleviate, but not fully resolve, differences in the reliability of their judgements. We discuss the implications of these findings for models of confidence and collective decision-making.

In for a penny, in for a pound: methylphenidate reduces the inhibitory effect of high stakes on persistent risky choice.

Methylphenidate (MPH) is a stimulant that increases extracellular levels of dopamine and noradrenaline. It can diminish risky decision-making tendencies in certain clinical populations. MPH is also used, without license, by healthy adults, but the impact on their decision-making is not well established. Previous work has found that dopamine receptor activity of healthy adults can modulate the influence of stake magnitude on decisions to persistently gamble after incurring a loss. In this study, we tested for modulation of this effect by MPH in 40 healthy human adults. In a double-blind experiment, 20 subjects received 20 mg of MPH, while 20 matched controls received a placebo. All were provided with 30 rounds of opportunities to accept an incurred loss from their assets or opt for a "double-or-nothing" gamble that would either avoid or double it. Rounds began with a variable loss that would double with every failed gamble until it was accepted, recovered, or reached a specified maximum. Probability of recovery on any gamble was low and ambiguous. Subjects receiving placebo gambled less as the magnitude of the stake was raised and as the magnitude of accumulated loss escalated over the course of the task. In contrast, subjects treated with MPH gambled at a consistent rate, well above chance, across all stakes and trials. Trait reward responsiveness also reduced the impact of high stakes. The findings suggest that elevated catecholamine activity by MPH can disrupt inhibitory influences on persistent risky choice in healthy adults.

Modulation of somatosensory processing by action.

Psychophysical evidence suggests that sensations arising from our own movements are diminished when predicted by motor forward models and that these models may also encode the timing and intensity of movement. Here we report a functional magnetic resonance imaging study in which the effects on sensation of varying the occurrence, timing and force of movements were measured. We observed that tactile-related activity in a region of secondary somatosensory cortex is reduced when sensation is associated with movement and further that this reduction is maximal when movement and sensation occur synchronously. Motor force is not represented in the degree of attenuation but rather in the magnitude of this region's response. These findings provide neurophysiological correlates of previously-observed behavioural forward-model phenomena, and advocate the adopted approach for the study of clinical conditions in which forward-model deficits have been posited to play a crucial role.

Rostral prefrontal cortex and the focus of attention in prospective memory.

Prospective memory (PM) denotes the function to realize intentions after a delay while being immersed in distracting ongoing (OG) activity. Here, we scrutinize the often-reported involvement of rostral prefrontal cortex (rPFC; approximating Brodmann area 10) in such situations: This region might mediate attention between external stimuli and the internally maintained intention, that is, between stimulus-oriented (SO) and stimulus-independent (SI) processing. Using functional magnetic resonance imaging (fMRI) we orthogonally crossed 1) PM versus OG activity only, with 2) SO versus SI attention. In support of the hypothesis, common regions of medial rPFC exhibited greater blood oxygen level-dependent (BOLD) signal for the contrasts of both OG task only versus PM and SO versus SI attending. However, activation related to the former contrast extended more superiorly, suggesting a functional gradient along a dorsal-ventral axis within this region. Moreover, region-of-interest analyses revealed that PM versus OG task only was associated with greater BOLD signal in left lateral rPFC, reflecting the requirement to maintain delayed intentions. Distinct aspects of this region were also transiently engaged at transitions between SO and SI conditions. These results are consistent with the hypothesis that some of the rostral prefrontal signal changes associated with PM performance reflect relative differences in SO versus SI processing.

Mechanisms of social cognition.

Social animals including humans share a range of social mechanisms that are automatic and implicit and enable learning by observation. Learning from others includes imitation of actions and mirroring of emotions. Learning about others, such as their group membership and reputation, is crucial for social interactions that depend on trust. For accurate prediction of others' changeable dispositions, mentalizing is required, i.e., tracking of intentions, desires, and beliefs. Implicit mentalizing is present in infants less than one year old as well as in some nonhuman species. Explicit mentalizing is a meta-cognitive process and enhances the ability to learn about the world through self-monitoring and reflection, and may be uniquely human. Meta-cognitive processes can also exert control over automatic behavior, for instance, when short-term gains oppose long-term aims or when selfish and prosocial interests collide. We suggest that they also underlie the ability to explicitly share experiences with other agents, as in reflective discussion and teaching. These are key in increasing the accuracy of the models of the world that we construct.

Consciousness, (meta)cognition, and culture.

Our conscious experience is determined by a combination of top-down processes (e.g., prior beliefs) and bottom-up processes (e.g., sensations). The balance between these two processes depends on estimates of their reliability (precision), so that the estimate considered more reliable is given more weight. We can modify these estimates at the metacognitive level, changing the relative weights of priors and sensations. This enables us, for example, to direct our attention to weak stimuli. But there is a cost to this malleability. For example, excessive weighting of top-down processes, as in schizophrenia, can lead to perceiving things that are not there and believing things that are not true. It is only at the top of the brain's cognitive hierarchy that metacognitive control becomes conscious. At this level, our beliefs concern complex, abstract entities with which we have limited direct experience. Estimates of the precision of such beliefs are more uncertain and more malleable. However, at this level, we do not need to rely on our own limited experience. We can rely instead on the experiences of others. Explicit metacognition plays a unique role, enabling us to share our experiences. We acquire our beliefs about the world from our immediate social group and from our wider culture. And the same sources provide us with better estimates of the precision of these beliefs. Our confidence in our high-level beliefs is heavily influenced by culture at the expense of direct experience.

The self and its reputation in autism.

In this issue of Neuron, a study by Chiu et al. examines the brain responses of autistic volunteers in a trust game. The findings reveal an unusual lack of brain activity in mid cingulate cortex when they make their investments. We speculate that this may arise because autistic individuals are unaware that they will also gain or lose reputation in their partner's eyes.

Dopamine-dependent prediction errors underpin reward-seeking behaviour in humans.

Theories of instrumental learning are centred on understanding how success and failure are used to improve future decisions. These theories highlight a central role for reward prediction errors in updating the values associated with available actions. In animals, substantial evidence indicates that the neurotransmitter dopamine might have a key function in this type of learning, through its ability to modulate cortico-striatal synaptic efficacy. However, no direct evidence links dopamine, striatal activity and behavioural choice in humans. Here we show that, during instrumental learning, the magnitude of reward prediction error expressed in the striatum is modulated by the administration of drugs enhancing (3,4-dihydroxy-L-phenylalanine; L-DOPA) or reducing (haloperidol) dopaminergic function. Accordingly, subjects treated with L-DOPA have a greater propensity to choose the most rewarding action relative to subjects treated with haloperidol. Furthermore, incorporating the magnitude of the prediction errors into a standard action-value learning algorithm accurately reproduced subjects' behavioural choices under the different drug conditions. We conclude that dopamine-dependent modulation of striatal activity can account for how the human brain uses reward prediction errors to improve future decisions.

Empathic neural responses are modulated by the perceived fairness of others.

The neural processes underlying empathy are a subject of intense interest within the social neurosciences. However, very little is known about how brain empathic responses are modulated by the affective link between individuals. We show here that empathic responses are modulated by learned preferences, a result consistent with economic models of social preferences. We engaged male and female volunteers in an economic game, in which two confederates played fairly or unfairly, and then measured brain activity with functional magnetic resonance imaging while these same volunteers observed the confederates receiving pain. Both sexes exhibited empathy-related activation in pain-related brain areas (fronto-insular and anterior cingulate cortices) towards fair players. However, these empathy-related responses were significantly reduced in males when observing an unfair person receiving pain. This effect was accompanied by increased activation in reward-related areas, correlated with an expressed desire for revenge. We conclude that in men (at least) empathic responses are shaped by valuation of other people's social behaviour, such that they empathize with fair opponents while favouring the physical punishment of unfair opponents, a finding that echoes recent evidence for altruistic punishment.

Animacy and the prediction of behaviour.

To survive, all animals need to predict what other agents are going to do next. We review neural mechanisms involved in the steps required for this ability. The first step is to determine whether an object is an agent, and if so, how sophisticated it is. This involves brain regions carrying representations of animate agents. The movements of the agent can then be anticipated in the short term based solely on physical constraints. In the longer term, taking into account the agent's goals and intentions is useful. Observing goal directed behaviour activates the neural action observation network, and predicting future goal directed behaviour is helped by the observer's own action generating mechanisms. Intentions are critically important in determining actions when interacting with other agents, as several intentions can lie behind an action. Here, interpretation is helped by prior beliefs about the agent and the brain's mentalising system is engaged. Biologically-constrained computational models of action recognition exist, but equivalent models for understanding intentional agents remain to be developed.

The mystery of the brain-culture interface.

Nature and culture work together to shape who we are. We are embedded in culture and are profoundly influenced by what those around us say and do. The interface between minds occurs at the level of explicit metacognition, which is at the top of our brain's control hierarchy. But how do our brains do this?