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1.  Precision and neuronal dynamics in the human posterior parietal cortex during evidence accumulation 
Neuroimage  2015;107:219-228.
Primate studies show slow ramping activity in posterior parietal cortex (PPC) neurons during perceptual decision-making. These findings have inspired a rich theoretical literature to account for this activity. These accounts are largely unrelated to Bayesian theories of perception and predictive coding, a related formulation of perceptual inference in the cortical hierarchy. Here, we tested a key prediction of such hierarchical inference, namely that the estimated precision (reliability) of information ascending the cortical hierarchy plays a key role in determining both the speed of decision-making and the rate of increase of PPC activity. Using dynamic causal modelling of magnetoencephalographic (MEG) evoked responses, recorded during a simple perceptual decision-making task, we recover ramping-activity from an anatomically and functionally plausible network of regions, including early visual cortex, the middle temporal area (MT) and PPC. Precision, as reflected by the gain on pyramidal cell activity, was strongly correlated with both the speed of decision making and the slope of PPC ramping activity. Our findings indicate that the dynamics of neuronal activity in the human PPC during perceptual decision-making recapitulate those observed in the macaque, and in so doing we link observations from primate electrophysiology and human choice behaviour. Moreover, the synaptic gain control modulating these dynamics is consistent with predictive coding formulations of evidence accumulation.
Highlights
•MEG and DCM used to characterise neuronal dynamics during decision making.•DCM suggested plausible hierarchical network architecture.•Rate of accumulation best explained by pyramidal cell gain.•Results support predictive coding models of evidence accumulation.
doi:10.1016/j.neuroimage.2014.12.015
PMCID: PMC4306525  PMID: 25512038
2.  Impaired threat prioritisation after selective bilateral amygdala lesions 
The amygdala is proposed to process threat-related information in non-human animals. In humans, empirical evidence from lesion studies has provided the strongest evidence for a role in emotional face recognition and social judgement. Here we use a face-in-the-crowd (FITC) task which in healthy control individuals reveals prioritised threat processing, evident in faster serial search for angry compared to happy target faces. We investigate AM and BG, two individuals with bilateral amygdala lesions due to Urbach–Wiethe syndrome, and 16 control individuals. In lesion patients we show a reversal of a threat detection advantage indicating a profound impairment in prioritising threat information. This is the first direct demonstration that human amygdala lesions impair prioritisation of threatening faces, providing evidence that this structure has a causal role in responding to imminent danger.
doi:10.1016/j.cortex.2014.08.017
PMCID: PMC4317193  PMID: 25282058
Amygdala lesion; Threat; Fear; Urbach–Wiethe; Facial expression; Serial search
3.  Learning-Induced Plasticity in Medial Prefrontal Cortex Predicts Preference Malleability 
Neuron  2015;85(2):418-428.
Summary
Learning induces plasticity in neuronal networks. As neuronal populations contribute to multiple representations, we reasoned plasticity in one representation might influence others. We used human fMRI repetition suppression to show that plasticity induced by learning another individual’s values impacts upon a value representation for oneself in medial prefrontal cortex (mPFC), a plasticity also evident behaviorally in a preference shift. We show this plasticity is driven by a striatal “prediction error,” signaling the discrepancy between the other’s choice and a subject’s own preferences. Thus, our data highlight that mPFC encodes agent-independent representations of subjective value, such that prediction errors simultaneously update multiple agents’ value representations. As the resulting change in representational similarity predicts interindividual differences in the malleability of subjective preferences, our findings shed mechanistic light on complex human processes such as the powerful influence of social interaction on beliefs and preferences.
Highlights
•Learning the values of another causes plasticity in a mPFC value representation•This plasticity predicts how much subjects’ own preferences change•Plasticity is explained by a striatal surprise signal•Value coding in mPFC occurs independently of the agent for whom a decision is made
Garvert et al. demonstrate that learning the preferences of another person increases the similarity between neural value representations for self and other. This plasticity in medial prefrontal cortex predicts how much one’s own preferences shift toward those of the other.
doi:10.1016/j.neuron.2014.12.033
PMCID: PMC4306543  PMID: 25611512
4.  Integration of Retinal and Extraretinal Information across Eye Movements 
PLoS ONE  2015;10(1):e0116810.
Visual perception is burdened with a highly discontinuous input stream arising from saccadic eye movements. For successful integration into a coherent representation, the visuomotor system needs to deal with these self-induced perceptual changes and distinguish them from external motion. Forward models are one way to solve this problem where the brain uses internal monitoring signals associated with oculomotor commands to predict the visual consequences of corresponding eye movements during active exploration. Visual scenes typically contain a rich structure of spatial relational information, providing additional cues that may help disambiguate self-induced from external changes of perceptual input. We reasoned that a weighted integration of these two inherently noisy sources of information should lead to better perceptual estimates. Volunteer subjects performed a simple perceptual decision on the apparent displacement of a visual target, jumping unpredictably in sync with a saccadic eye movement. In a critical test condition, the target was presented together with a flanker object, where perceptual decisions could take into account the spatial distance between target and flanker object. Here, precision was better compared to control conditions in which target displacements could only be estimated from either extraretinal or visual relational information alone. Our findings suggest that under natural conditions, integration of visual space across eye movements is based upon close to optimal integration of both retinal and extraretinal pieces of information.
doi:10.1371/journal.pone.0116810
PMCID: PMC4300226  PMID: 25602956
5.  Free energy, precision and learning: the role of cholinergic neuromodulation 
Acetylcholine (ACh) is a neuromodulatory transmitter implicated in perception and learning under uncertainty. This study combined computational simulations and pharmaco-electroencephalography in humans, to test a formulation of perceptual inference based upon the free energy principle. This formulation suggests that acetylcholine enhances the precision of bottom-up synaptic transmission in cortical hierarchies by optimising the gain of supragranular pyramidal cells. Simulations of a mismatch negativity paradigm predicted a rapid trial-by-trial suppression of evoked sensory prediction error (PE) responses that is attenuated by cholinergic neuromodulation. We confirmed this prediction empirically with a placebo-controlled study of cholinesterase inhibition. Furthermore – using dynamic causal modelling – we found that drug-induced differences in PE responses could be explained by gain modulation in supragranular pyramidal cells in primary sensory cortex. This suggests that acetylcholine adaptively enhances sensory precision by boosting bottom-up signalling when stimuli are predictable, enabling the brain to respond optimally under different levels of environmental uncertainty.
doi:10.1523/JNEUROSCI.4255-12.2013
PMCID: PMC4235126  PMID: 23658161
Free Energy Principle; Predictive Coding; Neuromodulation; Acetylcholine; Galantamine; Oddball Response; Precision; Dynamic Causal Modelling
6.  Subcortical amygdala pathways enable rapid face processing 
Neuroimage  2014;102:309-316.
Human faces may signal relevant information and are therefore analysed rapidly and effectively by the brain. However, the precise mechanisms and pathways involved in rapid face processing are unclear. One view posits a role for a subcortical connection between early visual sensory regions and the amygdala, while an alternative account emphasises cortical mediation. To adjudicate between these functional architectures, we recorded magnetoencephalographic (MEG) evoked fields in human subjects to presentation of faces with varying emotional valence. Early brain activity was better explained by dynamic causal models containing a direct subcortical connection to the amygdala irrespective of emotional modulation. At longer latencies, models without a subcortical connection had comparable evidence. Hence, our results support the hypothesis that a subcortical pathway to the amygdala plays a role in rapid sensory processing of faces, in particular during early stimulus processing. This finding contributes to an understanding of the amygdala as a behavioural relevance detector.
Highlights
•Face processing involves a functional subcortical route to amygdala.•Subcortical visual pathway to amygdala is crucial during early visual processing.•Visual processing of late time‐periods can also be explained by cortical connectivity.
doi:10.1016/j.neuroimage.2014.07.047
PMCID: PMC4229499  PMID: 25108179
Dynamic causal modelling; Subcortical processing; Amygdala; Connectivity; MEG
7.  The neural basis of metacognitive ability 
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.
doi:10.1098/rstb.2011.0417
PMCID: PMC3318765  PMID: 22492751
metacognition; confidence; conflict; prefrontal cortex; functional magnetic resonance imaging; individual differences
8.  Metacognition: computation, biology and function 
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.
doi:10.1098/rstb.2012.0021
PMCID: PMC3318771  PMID: 22492746
metacognition; neurobiology; computational modelling; consciousness
9.  The anatomy of choice: dopamine and decision-making 
This paper considers goal-directed decision-making in terms of embodied or active inference. We associate bounded rationality with approximate Bayesian inference that optimizes a free energy bound on model evidence. Several constructs such as expected utility, exploration or novelty bonuses, softmax choice rules and optimism bias emerge as natural consequences of free energy minimization. Previous accounts of active inference have focused on predictive coding. In this paper, we consider variational Bayes as a scheme that the brain might use for approximate Bayesian inference. This scheme provides formal constraints on the computational anatomy of inference and action, which appear to be remarkably consistent with neuroanatomy. Active inference contextualizes optimal decision theory within embodied inference, where goals become prior beliefs. For example, expected utility theory emerges as a special case of free energy minimization, where the sensitivity or inverse temperature (associated with softmax functions and quantal response equilibria) has a unique and Bayes-optimal solution. Crucially, this sensitivity corresponds to the precision of beliefs about behaviour. The changes in precision during variational updates are remarkably reminiscent of empirical dopaminergic responses—and they may provide a new perspective on the role of dopamine in assimilating reward prediction errors to optimize decision-making.
doi:10.1098/rstb.2013.0481
PMCID: PMC4186234  PMID: 25267823
active inference; agency; Bayesian inference; bounded rationality; free energy; utility theory
10.  Competition strength influences individual preferences in an auction game 
Cognition  2014;133(2):480-487.
Highlights
•We conducted a repeated all-pay auction experiment with real items.•Participants exhibited dynamic bidding strategies.•Bidding dynamics clearly affected preferences for auctioned items.•Preference changes depended on the effort exerted when winning.
Competitive interactions between individuals are ubiquitous in human societies. Auctions represent an institutionalized context for these interactions, a context where individuals frequently make non-optimal decisions. In particular, competition in auctions can lead to overbidding, resulting in the so-called winner’s curse, often explained by invoking emotional arousal. In this study, we investigated an alternative possibility, namely that competitors’ bids are construed as a source of information about the good’s common value thereby influencing an individuals’ private value estimate. We tested this hypothesis by asking participants to bid in a repeated all-pay auction game for five different real items. Crucially, participants had to rank the auction items for their preference before and after the experiment. We observed a clear relation between auction dynamics and preference change. We found that low competition reduced preference while high competition increased preference. Our findings support a view that competitors’ bids in auction games are perceived as valid social signal for the common value of an item. We suggest that this influence of social information constitutes a major cause for the frequently observed deviations from optimality in auctions.
doi:10.1016/j.cognition.2014.07.010
PMCID: PMC4175410  PMID: 25168161
Social information; All pay auction; Decision-making; Preference formation; Competition
11.  Relative Valuation of Pain in Human Orbitofrontal Cortex 
The Journal of Neuroscience  2014;34(44):14526-14535.
The valuation of health-related states, including pain, is a critical issue in clinical practice, health economics, and pain neuroscience. Surprisingly the monetary value people associate with pain is highly context-dependent, with participants willing to pay more to avoid medium-level pain when presented in a context of low-intensity, rather than high-intensity, pain. Here, we ask whether context impacts upon the neural representation of pain itself, or alternatively the transformation of pain into valuation-driven behavior. While undergoing fMRI, human participants declared how much money they would be willing to pay to avoid repeated instances of painful cutaneous electrical stimuli delivered to the foot. We also implemented a contextual manipulation that involved presenting medium-level painful stimuli in blocks with either low- or high-level stimuli. We found no evidence of context-dependent activity within a conventional “pain matrix,” where pain-evoked activity reflected absolute stimulus intensity. By contrast, in right lateral orbitofrontal cortex, a strong contextual dependency was evident, and here activity tracked the contextual rank of the pain. The findings are in keeping with an architecture where an absolute pain valuation system and a rank-dependent system interact to influence willing to pay to avoid pain, with context impacting value-based behavior high in a processing hierarchy. This segregated processing hints that distinct neural representations reflect sensory aspects of pain and components that are less directly nociceptive whose integration also guides pain-related actions. A dominance of the latter might account for puzzling phenomena seen in somatization disorders where perceived pain is a dominant driver of behavior.
doi:10.1523/JNEUROSCI.1706-14.2014
PMCID: PMC4212059  PMID: 25355207
context sensitivity; neuroeconomics; pain; subjective health complaints; valuation
12.  Anterior Cingulate Cortex Instigates Adaptive Switches in Choice by Integrating Immediate and Delayed Components of Value in Ventromedial Prefrontal Cortex 
The Journal of Neuroscience  2014;34(9):3340-3349.
Actions can lead to an immediate reward or punishment and a complex set of delayed outcomes. Adaptive choice necessitates the brain track and integrate both of these potential consequences. Here, we designed a sequential task whereby the decision to exploit or forego an available offer was contingent on comparing immediate value and a state-dependent future cost of expending a limited resource. Crucially, the dynamics of the task demanded frequent switches in policy based on an online computation of changing delayed consequences. We found that human subjects choose on the basis of a near-optimal integration of immediate reward and delayed consequences, with the latter computed in a prefrontal network. Within this network, anterior cingulate cortex (ACC) was dynamically coupled to ventromedial prefrontal cortex (vmPFC) when adaptive switches in choice were required. Our results suggest a choice architecture whereby interactions between ACC and vmPFC underpin an integration of immediate and delayed components of value to support flexible policy switching that accommodates the potential delayed consequences of an action.
doi:10.1523/JNEUROSCI.4313-13.2014
PMCID: PMC3935091  PMID: 24573291
fMRI; decision-making; value; control; computational modeling; prefrontal cortex
13.  The effects of life stress and neural learning signals on fluid intelligence 
Fluid intelligence (fluid IQ), defined as the capacity for rapid problem solving and behavioral adaptation, is known to be modulated by learning and experience. Both stressful life events (SLES) and neural correlates of learning [specifically, a key mediator of adaptive learning in the brain, namely the ventral striatal representation of prediction errors (PE)] have been shown to be associated with individual differences in fluid IQ. Here, we examine the interaction between adaptive learning signals (using a well-characterized probabilistic reversal learning task in combination with fMRI) and SLES on fluid IQ measures. We find that the correlation between ventral striatal BOLD PE and fluid IQ, which we have previously reported, is quantitatively modulated by the amount of reported SLES. Thus, after experiencing adversity, basic neuronal learning signatures appear to align more closely with a general measure of flexible learning (fluid IQ), a finding complementing studies on the effects of acute stress on learning. The results suggest that an understanding of the neurobiological correlates of trait variables like fluid IQ needs to take socioemotional influences such as chronic stress into account.
Electronic supplementary material
The online version of this article (doi:10.1007/s00406-014-0519-3) contains supplementary material, which is available to authorized users.
doi:10.1007/s00406-014-0519-3
PMCID: PMC4311068  PMID: 25142177
Reinforcement learning; Prediction error signal; Ventral striatum; Stress; Intelligence
14.  Reward-Related Activity in Ventral Striatum Is Action Contingent and Modulated by Behavioral Relevance 
The Journal of Neuroscience  2014;34(4):1271-1279.
Multiple features of the environment are often imbued with motivational significance, and the relative importance of these can change across contexts. The ability to flexibly adjust evaluative processes so that currently important features of the environment alone drive behavior is critical to adaptive routines. We know relatively little about the neural mechanisms involved, including whether motivationally significant features are obligatorily evaluated or whether current relevance gates access to value-sensitive regions. We addressed these questions using functional magnetic resonance imaging data and a task design where human subjects had to choose whether to accept or reject an offer indicated by visual and auditory stimuli. By manipulating, on a trial-by-trial basis, which stimulus determined the value of the offer, we show choice activity in the ventral striatum solely reflects the value of the currently relevant stimulus, consistent with a model wherein behavioral relevance modulates the impact of sensory stimuli on value processing. Choice outcome signals in this same region covaried positively with wins on accept trials, and negatively with wins on reject trials, consistent with striatal activity at feedback reflecting correctness of response rather than reward processing per se. We conclude that ventral striatum activity during decision making is dynamically modulated by behavioral context, indexed here by task relevance and action selection.
doi:10.1523/JNEUROSCI.4389-13.2014
PMCID: PMC3898287  PMID: 24453318
action value; multisensory; policy selection; reward; ventral striatum
15.  Crowdsourcing for Cognitive Science – The Utility of Smartphones 
PLoS ONE  2014;9(7):e100662.
By 2015, there will be an estimated two billion smartphone users worldwide. This technology presents exciting opportunities for cognitive science as a medium for rapid, large-scale experimentation and data collection. At present, cost and logistics limit most study populations to small samples, restricting the experimental questions that can be addressed. In this study we investigated whether the mass collection of experimental data using smartphone technology is valid, given the variability of data collection outside of a laboratory setting. We presented four classic experimental paradigms as short games, available as a free app and over the first month 20,800 users submitted data. We found that the large sample size vastly outweighed the noise inherent in collecting data outside a controlled laboratory setting, and show that for all four games canonical results were reproduced. For the first time, we provide experimental validation for the use of smartphones for data collection in cognitive science, which can lead to the collection of richer data sets and a significant cost reduction as well as provide an opportunity for efficient phenotypic screening of large populations.
doi:10.1371/journal.pone.0100662
PMCID: PMC4099129  PMID: 25025865
16.  Dimensional psychiatry: reward dysfunction and depressive mood across psychiatric disorders 
Psychopharmacology  2014;232:331-341.
Rationale
A dimensional approach in psychiatry aims to identify core mechanisms of mental disorders across nosological boundaries.
Objectives
We compared anticipation of reward between major psychiatric disorders, and investigated whether reward anticipation is impaired in several mental disorders and whether there is a common psychopathological correlate (negative mood) of such an impairment.
Methods
We used functional magnetic resonance imaging (fMRI) and a monetary incentive delay (MID) task to study the functional correlates of reward anticipation across major psychiatric disorders in 184 subjects, with the diagnoses of alcohol dependence (n = 26), schizophrenia (n = 44), major depressive disorder (MDD, n = 24), bipolar disorder (acute manic episode, n = 13), attention deficit/hyperactivity disorder (ADHD, n = 23), and healthy controls (n = 54). Subjects’ individual Beck Depression Inventory-and State-Trait Anxiety Inventory-scores were correlated with clusters showing significant activation during reward anticipation.
Results
During reward anticipation, we observed significant group differences in ventral striatal (VS) activation: patients with schizophrenia, alcohol dependence, and major depression showed significantly less ventral striatal activation compared to healthy controls. Depressive symptoms correlated with dysfunction in reward anticipation regardless of diagnostic entity. There was no significant correlation between anxiety symptoms and VS functional activation.
Conclusion
Our findings demonstrate a neurobiological dysfunction related to reward prediction that transcended disorder categories and was related to measures of depressed mood. The findings underline the potential of a dimensional approach in psychiatry and strengthen the hypothesis that neurobiological research in psychiatric disorders can be targeted at core mechanisms that are likely to be implicated in a range of clinical entities.
Electronic supplementary material
The online version of this article (doi:10.1007/s00213-014-3662-7) contains supplementary material, which is available to authorized users.
doi:10.1007/s00213-014-3662-7
PMCID: PMC4297301  PMID: 24973896
Dimensional; fMRI; Reward system; Ventral striatum; Monetary incentive delay task; Depressive symptoms
17.  Brain Substrates of Recovery from Misleading Influence 
The Journal of Neuroscience  2014;34(23):7744-7753.
Humans are strongly influenced by their environment, a dependence that can lead to errors in judgment. Although a rich literature describes how people are influenced by others, little is known regarding the factors that predict subsequent rectification of misleading influence. Using a mediation model in combination with brain imaging, we propose a model for the correction of misinformation. Specifically, our data suggest that amygdala modulation of hippocampal mnemonic representations, during the time of misleading social influence, is associated with reduced subsequent anterior–lateral prefrontal cortex activity that reflects correction. These findings illuminate the process by which erroneous beliefs are, or fail to be, rectified and highlight how past influence constrains subsequent correction.
doi:10.1523/JNEUROSCI.4720-13.2014
PMCID: PMC4044241  PMID: 24899698
brain; fMRI; memory; recovery; social
18.  A Genetically Mediated Bias in Decision Making Driven by Failure of Amygdala Control 
Genetic variation at the serotonin transporter-linked polymorphic region (5-HTTLPR) is associated with altered amygdala reactivity and lack of prefrontal regulatory control. Similar regions mediate decision-making biases driven by contextual cues and ambiguity, for example the “framing effect.” We hypothesized that individuals hemozygous for the short (s) allele at the 5-HTTLPR would be more susceptible to framing. Participants, selected as homozygous for either the long (la) or s allele, performed a decision-making task where they made choices between receiving an amount of money for certain and taking a gamble. A strong bias was evident toward choosing the certain option when the option was phrased in terms of gains and toward gambling when the decision was phrased in terms of losses (the frame effect). Critically, this bias was significantly greater in the ss group compared with the lala group. In simultaneously acquired functional magnetic resonance imaging data, the ss group showed greater amygdala during choices made in accord, compared with those made counter to the frame, an effect not seen in the lala group. These differences were also mirrored by differences in anterior cingulate–amygdala coupling between the genotype groups during decision making. Specifically, lala participants showed increased coupling during choices made counter to, relative to those made in accord with, the frame, with no such effect evident in ss participants. These data suggest that genetically mediated differences in prefrontal-amygdala interactions underpin interindividual differences in economic decision making.
doi:10.1523/JNEUROSCI.0407-09.2009
PMCID: PMC2686091  PMID: 19420264
19.  Preparing for Selective Inhibition within Frontostriatal Loops 
The Journal of Neuroscience  2013;33(46):18087-18097.
Action inhibition can globally prevent all motor output or selectively cancel specific actions during concurrent motor output. Here we examine the behavioral and neural basis of selective inhibition focusing on the role of preparation. In 18 healthy human participants we manipulated the extent to which they could prepare for selective inhibition by providing or withholding information on what actions might need to be stopped. We show that, on average, information improves both speed and selectivity of inhibition. Functional magnetic resonance imaging data show that preparation for selective inhibition engages the inferior frontal gyrus, supplementary motor area, and striatum. Examining interindividual differences, we find the benefit of proactive control to speed and selectivity of inhibition trade off against each other, such that an improvement in stopping speed leads to a deterioration of selectivity of inhibition, and vice versa. This trade-off is implemented through engagement of the dorsolateral prefrontal cortex and putamen. Our results suggest proactive selective inhibition is implemented within frontostriatal structures, and we provide evidence that a speed-selectivity trade-off might underlie a range of findings reported previously.
doi:10.1523/JNEUROSCI.2167-13.2013
PMCID: PMC3828462  PMID: 24227719
20.  Fear from the Heart: Sensitivity to Fear Stimuli Depends on Individual Heartbeats 
The Journal of Neuroscience  2014;34(19):6573-6582.
Cognitions and emotions can be influenced by bodily physiology. Here, we investigated whether the processing of brief fear stimuli is selectively gated by their timing in relation to individual heartbeats. Emotional and neutral faces were presented to human volunteers at cardiac systole, when ejection of blood from the heart causes arterial baroreceptors to signal centrally the strength and timing of each heartbeat, and at diastole, the period between heartbeats when baroreceptors are quiescent. Participants performed behavioral and neuroimaging tasks to determine whether these interoceptive signals influence the detection of emotional stimuli at the threshold of conscious awareness and alter judgments of emotionality of fearful and neutral faces. Our results show that fearful faces were detected more easily and were rated as more intense at systole than at diastole. Correspondingly, amygdala responses were greater to fearful faces presented at systole relative to diastole. These novel findings highlight a major channel by which short-term interoceptive fluctuations enhance perceptual and evaluative processes specifically related to the processing of fear and threat and counter the view that baroreceptor afferent signaling is always inhibitory to sensory perception.
doi:10.1523/JNEUROSCI.3507-13.2014
PMCID: PMC4012313  PMID: 24806682
amygdala; anxiety; attention; baroreceptor; emotion; fMRI
21.  Online evaluation of novel choices by simultaneous representation of multiple memories 
Nature neuroscience  2013;16(10):1492-1498.
Prior experience plays a critical role in decision making. It enables explicit representation of potential outcomes and provides training to valuation mechanisms. However, we can also make choices in the absence of prior experience, by merely imagining the consequences of a new experience. Here, using fMRI repetition suppression in humans, we show how neuronal representations of novel rewards can be constructed and evaluated. A likely novel experience is constructed by invoking multiple independent memories within hippocampus and medial prefrontal cortex. This construction persists for only a short time period, during which new associations are observed between the memories for component items. Together these findings suggest that in the absence of direct experience, co-activation of multiple relevant memories can provide a training signal to the valuation system which allows the consequences of new experiences to be imagined and acted upon.
doi:10.1038/nn.3515
PMCID: PMC4001211  PMID: 24013592
22.  Bayesian inferences about the self (and others): A review 
Consciousness and Cognition  2014;25(100):67-76.
Highlights
•People may use Bayesian inference to update their own self-representation.•Self- and other-representations may help predict outcomes of social interactions.•The value of an outcome is essentially the prior belief that it can be achieved.•‘Active inference’ uses free-energy-minimization to achieve desirable outcomes.•A positive self-representation may be a desirable outcome of active inference.
Viewing the brain as an organ of approximate Bayesian inference can help us understand how it represents the self. We suggest that inferred representations of the self have a normative function: to predict and optimise the likely outcomes of social interactions. Technically, we cast this predict-and-optimise as maximising the chance of favourable outcomes through active inference. Here the utility of outcomes can be conceptualised as prior beliefs about final states. Actions based on interpersonal representations can therefore be understood as minimising surprise – under the prior belief that one will end up in states with high utility. Interpersonal representations thus serve to render interactions more predictable, while the affective valence of interpersonal inference renders self-perception evaluative. Distortions of self-representation contribute to major psychiatric disorders such as depression, personality disorder and paranoia. The approach we review may therefore operationalise the study of interpersonal representations in pathological states.
doi:10.1016/j.concog.2014.01.009
PMCID: PMC3989044  PMID: 24583455
Self-representation; Other-representation; Free energy minimisation; Active inference; Personality disorder; Paranoia
23.  Re-construction of action awareness depends on an internal model of action-outcome timing 
Consciousness and Cognition  2014;25(100):11-16.
Highlights
•Action awareness can shift retrospectively at the time of an action-outcome.•In principle, this could reflect bottom-up interference and not subjective agency.•We keep bottom-up drive constant and manipulate temporal outcome variability instead.•Action awareness is shifted retrospectively in a context of variable outcome timing.•This top-down process may bias subjective agency when an outcome is unpredictable.
The subjective time of an instrumental action is shifted towards its outcome. This temporal binding effect is partially retrospective, i.e., occurs upon outcome perception. Retrospective binding is thought to reflect post-hoc inference on agency based on sensory evidence of the action – outcome association. However, many previous binding paradigms cannot exclude the possibility that retrospective binding results from bottom-up interference of sensory outcome processing with action awareness and is functionally unrelated to the processing of the action – outcome association. Here, we keep bottom-up interference constant and use a contextual manipulation instead. We demonstrate a shift of subjective action time by its outcome in a context of variable outcome timing. Crucially, this shift is absent when there is no such variability. Thus, retrospective action binding reflects a context-dependent, model-based phenomenon. Such top-down re-construction of action awareness seems to bias agency attribution when outcome predictability is low.
doi:10.1016/j.concog.2014.01.007
PMCID: PMC3989060  PMID: 24555983
Action awareness; Temporal binding; Sense of agency
24.  Human Hippocampus Arbitrates Approach-Avoidance Conflict 
Current Biology  2014;24(5):541-547.
Summary
Animal models of human anxiety often invoke a conflict between approach and avoidance [1, 2]. In these, a key behavioral assay comprises passive avoidance of potential threat and inhibition, both thought to be controlled by ventral hippocampus [2–6]. Efforts to translate these approaches to clinical contexts [7, 8] are hampered by the fact that it is not known whether humans manifest analogous approach-avoidance dispositions and, if so, whether they share a homologous neurobiological substrate [9]. Here, we developed a paradigm to investigate the role of human hippocampus in arbitrating an approach-avoidance conflict under varying levels of potential threat. Across four experiments, subjects showed analogous behavior by adapting both passive avoidance behavior and behavioral inhibition to threat level. Using functional magnetic resonance imaging (fMRI), we observe that threat level engages the anterior hippocampus, the human homolog of rodent ventral hippocampus [10]. Testing patients with selective hippocampal lesions, we demonstrate a causal role for the hippocampus with patients showing reduced passive avoidance behavior and inhibition across all threat levels. Our data provide the first human assay for approach-avoidance conflict akin to that of animal anxiety models. The findings bridge rodent and human research on passive avoidance and behavioral inhibition and furnish a framework for addressing the neuronal underpinnings of human anxiety disorders, where our data indicate a major role for the hippocampus.
Highlights
•Human behavior in a spatial approach-avoidance conflict resembles animal behavior•Threat level in this context specifically engages anterior hippocampus•Hippocampal lesions reduce passive avoidance and inhibition•The study provides human evidence for an anterior hippocampus role in anxiety
Using a combined functional magnetic resonance imaging and hippocampus lesion approach, Bach et al. demonstrate that the human anterior hippocampus is engaged in monitoring threat level during approach-avoidance conflict, replicating and extending a rodent literature on models of anxiety.
doi:10.1016/j.cub.2014.01.046
PMCID: PMC3969259  PMID: 24560572
25.  Keep focussing: striatal dopamine multiple functions resolved in a single mechanism tested in a simulated humanoid robot 
The effects of striatal dopamine (DA) on behavior have been widely investigated over the past decades, with “phasic” burst firings considered as the key expression of a reward prediction error responsible for reinforcement learning. Less well studied is “tonic” DA, where putative functions include the idea that it is a regulator of vigor, incentive salience, disposition to exert an effort and a modulator of approach strategies. We present a model combining tonic and phasic DA to show how different outflows triggered by either intrinsically or extrinsically motivating stimuli dynamically affect the basal ganglia by impacting on a selection process this system performs on its cortical input. The model, which has been tested on the simulated humanoid robot iCub interacting with a mechatronic board, shows the putative functions ascribed to DA emerging from the combination of a standard computational mechanism coupled to a differential sensitivity to the presence of DA across the striatum.
doi:10.3389/fpsyg.2014.00124
PMCID: PMC3930917  PMID: 24600422
basal ganglia; dopamine; selection; novelty; iCub; intrinsic motivation

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