Showing papers by "Raymond J. Dolan published in 2008"
TL;DR: The data suggest that oxytocin modulates the expression of evaluative conditioning for socially relevant faces via influences on amygdala and fusiform gyrus, an effect that may explain its prosocial effects.
Abstract: Social relations between humans critically depend on our affective experiences of others. Oxytocin enhances prosocial behavior, but its effect on humans' affective experience of others is not known. We tested whether oxytocin influences affective ratings, and underlying brain activity, of faces that have been aversively conditioned. Using a standard conditioning procedure, we induced differential negative affective ratings in faces exposed to an aversive conditioning compared with nonconditioning manipulation. This differential negative evaluative effect was abolished by treatment with oxytocin, an effect associated with an attenuation of activity in anterior medial temporal and anterior cingulate cortices. In amygdala and fusiform gyrus, this modulation was stronger for faces with direct gaze, relative to averted gaze, consistent with a relative specificity for socially relevant cues. The data suggest that oxytocin modulates the expression of evaluative conditioning for socially relevant faces via influences on amygdala and fusiform gyrus, an effect that may explain its prosocial effects.
425 citations
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TL;DR: It is shown it is possible to deduce whether players make inferences about each other and quantify their sophistication on the basis of choices in sequential games, and exactly the same sophisticated behaviour can be achieved by optimising the utility function itself (through prosocial utility), producing unsophisticated but apparently altruistic agents.
Abstract: This paper introduces a model of ‘theory of mind’, namely, how we represent the intentions and goals of others to optimise our mutual interactions. We draw on ideas from optimum control and game theory to provide a ‘game theory of mind’. First, we consider the representations of goals in terms of value functions that are prescribed by utility or rewards. Critically, the joint value functions and ensuing behaviour are optimised recursively, under the assumption that I represent your value function, your representation of mine, your representation of my representation of yours, and so on ad infinitum. However, if we assume that the degree of recursion is bounded, then players need to estimate the opponent's degree of recursion (i.e., sophistication) to respond optimally. This induces a problem of inferring the opponent's sophistication, given behavioural exchanges. We show it is possible to deduce whether players make inferences about each other and quantify their sophistication on the basis of choices in sequential games. This rests on comparing generative models of choices with, and without, inference. Model comparison is demonstrated using simulated and real data from a ‘stag-hunt’. Finally, we note that exactly the same sophisticated behaviour can be achieved by optimising the utility function itself (through prosocial utility), producing unsophisticated but apparently altruistic agents. This may be relevant ethologically in hierarchal game theory and coevolution.
315 citations
TL;DR: This work provides a demonstration of behavioral pavlovian–instrumental transfer in humans, with an audiovisual predictor of the noncontingent delivery of money inducing participants to perform more avidly an action involving squeezing a handgrip to earn money.
Abstract: The vigor with which a participant performs actions that produce valuable outcomes is subject to a complex set of motivational influences. Many of these are believed to involve the amygdala and the nucleus accumbens, which act as an interface between limbic and motor systems. One prominent class of influences is called pavlovian-instrumental transfer (PIT), in which the motivational characteristics of a predictor influence the vigor of an action with respect to which it is formally completely independent. We provide a demonstration of behavioral PIT in humans, with an audiovisual predictor of the noncontingent delivery of money inducing participants to perform more avidly an action involving squeezing a handgrip to earn money. Furthermore, using functional magnetic resonance imaging, we show that this enhanced motivation was associated with a trial-by-trial correlation with the blood oxygenation level-dependent (BOLD) signal in the nucleus accumbens and a subject-by-subject correlation with the BOLD signal in the amygdala. Our data dovetails well with the animal literature and sheds light on the neural control of vigor.
293 citations
TL;DR: Behavioral studies that suggest that Pavlovian processes can exert an important influence over choice and may account for many effects that have traditionally been attributed to emotion are reviewed.
262 citations
TL;DR: It is concluded that, even without conscious processing of contextual cues, the brain can learn their reward value and use them to provide a bias on decision making.
251 citations
TL;DR: The results suggest that selfish individuals may not be as rational and unemotional as usually suggested, their actions being determined by their feeling anxious rather than by reason.
Abstract: In this study, we tested the validity of 2 popular assumptions about empathy: (a) empathy can be enhanced by oxytocin, a neuropeptide known to be crucial in affiliative behavior, and (b) individual differences in prosocial behavior are positively associated with empathic brain responses. To do so, we measured brain activity in a double-blind placebo-controlled study of 20 male participants either receiving painful stimulation to their own hand (self condition) or observing their female partner receiving painful stimulation to her hand (other condition). Prosocial behavior was measured using a monetary economic interaction game with which participants classified as prosocial (N 12) or selfish (N 6), depending on whether they cooperated with another player. Empathy-relevant brain activation (anterior insula) was neither enhanced by oxytocin nor positively associated with prosocial behavior. However, oxytocin reduced amygdala activation when participants received painful stimulation themselves (in the nonsocial condition). Surprisingly, this effect was driven by “selfish” participants. The results suggest that selfish individuals may not be as rational and unemotional as usually suggested, their actions being determined by their feeling anxious rather than by reason.
239 citations
TL;DR: It is shown that, even when the degree of perceptual familiarity of an option is unrelated to choice outcome, novelty nevertheless drives choice behavior, and the brain uses perceptual novelty to approximate choice uncertainty in decision making.
223 citations
TL;DR: This study investigates subjects with autism spectrum disorder using a financial task in which the monetary prospects were presented as either loss or gain and reports both behavioral evidence that ASD subjects show a reduced susceptibility to the framing effect and psycho-physiological evidence that they fail to incorporate emotional context into the decision-making process.
Abstract: The emotional responses elicited by the way options are framed often results in lack of logical consistency in human decision making. In this study, we investigated subjects with autism spectrum disorder (ASD) using a financial task in which the monetary prospects were presented as either loss or gain. We report both behavioral evidence that ASD subjects show a reduced susceptibility to the framing effect and psycho-physiological evidence that they fail to incorporate emotional context into the decision-making process. On this basis, we suggest that this insensitivity to contextual frame, although enhancing choice consistency in ASD, may also underpin core deficits in this disorder. These data highlight both benefits and costs arising from multiple decision processes in human cognition.
187 citations
TL;DR: These findings provide the first evidence that direct evoked fMRI activity patterns in the LOC can be different for individual object exemplars (within a single category), and propose that pattern recognition methods as used here may provide an alternative approach to study mechanisms of neuronal representation based on aspects of the fMRI response independent of those assessed in adaptation paradigms.
Abstract: The lateral occipital complex (LOC) is a set of areas in the human occipito-temporal cortex responding to objects as opposed to low-level control stimuli. Conventional functional magnetic resonance imaging (fMRI) analysis methods based on regional averages could not detect signals discriminative of different types of objects in this region. Here, we examined fMRI signals using multivariate pattern recognition (support vector classification) to systematically explore the nature of object-related information available in fine-grained activity patterns in the LOC. Distributed fMRI signals from the LOC allowed for above-chance discrimination not only of the category but also of within-category exemplars of everyday man-made objects, and such exemplar-specific information generalized across changes in stimulus size and viewpoint, particularly in posterior subregions. Object identity could also be predicted from responses of the early visual cortex, even significantly across the changes in size and viewpoint used here. However, a dissociation was observed between these two regions of interest in the degree of discrimination for objects relative to size: In the early visual cortex, two different sizes of the same object were even better discriminated than two different objects (in accordance with measures of pixelwise stimulus similarity), whereas the opposite was true in the LOC. These findings provide the first evidence that direct evoked fMRI activity patterns in the LOC can be different for individual object exemplars (within a single category). We propose that pattern recognition methods as used here may provide an alternative approach to study mechanisms of neuronal representation based on aspects of the fMRI response independent of those assessed in adaptation paradigms.
170 citations
TL;DR: It is found that dopamine storage capacity in human amygdala was positively correlated with functional magnetic resonance imaging blood oxygen level–dependent signal changes in amygdala and dorsal anterior cingulate cortex that were evoked by aversive stimuli, and functional connectivity between these two regions was inversely related to trait anxiety.
Abstract: Dopamine is known to contribute to the amygdala-mediated aversive response, where increased dopamine release can augment amygdala function. Combining fMRI and PET imaging techniques, Kienast et al. present findings that suggest a functional link between anxiety temperament, dopamine storage capacity and emotional processing in the amygdala. Dopamine is released under stress and modulates processing of aversive stimuli. We found that dopamine storage capacity in human amygdala, measured with 6-[18F]fluoro-L-DOPA positron emission tomography, was positively correlated with functional magnetic resonance imaging blood oxygen level–dependent signal changes in amygdala and dorsal anterior cingulate cortex that were evoked by aversive stimuli. Furthermore, functional connectivity between these two regions was inversely related to trait anxiety. Our results suggest that individual dopamine storage capacity in amygdala subserves modulation of emotional processing in amygdala and dorsal cingulate, thereby contributing to individual differences in anxious temperament.
163 citations
TL;DR: Individual differences in empathy and emotion regulatory tendency predicted the magnitude of EEI-evoked regional activity with BA 47 and STS, and findings point to these regions as providing a putative neural substrate underpinning a crucial adaptive aspect of social/emotional behavior.
Abstract: Emotional facial expressions can engender similar expressions in others. However, adaptive social and motivational behavior can require individuals to suppress, conceal, or override prepotent imitative responses. We predicted, in line with a theory of "emotion contagion," that when viewing a facial expression, expressing a different emotion would manifest as behavioral conflict and interference. We employed facial electromyography (EMG) and functional magnetic resonance imaging (fMRI) to investigate brain activity related to this emotion expression interference (EEI) effect, where the expressed response was either concordant or discordant with the observed emotion. The Simon task was included as a nonemotional comparison for the fMRI study. Facilitation and interference effects were observed in the latency of facial EMG responses. Neuroimaging revealed activation of distributed brain regions including anterior right inferior frontal gyrus (brain area [BA] 47), supplementary motor area (facial area), posterior superior temporal sulcus (STS), and right anterior insula during emotion expression-associated interference. In contrast, nonemotional response conflict (Simon task) engaged a distinct frontostriatal network. Individual differences in empathy and emotion regulatory tendency predicted the magnitude of EEI-evoked regional activity with BA 47 and STS. Our findings point to these regions as providing a putative neural substrate underpinning a crucial adaptive aspect of social/emotional behavior.
TL;DR: The data indicate that a central opioid system contributes to both reward and loss processing in humans and directly modulates the hedonic experience of outcomes.
Abstract: Reward processing is linked to specific neuromodulatory systems with a dopaminergic contribution to reward learning and motivational drive being well established. Neuromodulatory influences on hedonic responses to actual receipt of reward, or punishment, referred to as experienced utility are less well characterized, although a link to the endogenous opioid system is suggested. Here, in a combined functional magnetic resonance imaging–psychopharmacological investigation, we used naloxone to block central opioid function while subjects performed a gambling task associated with rewards and losses of different magnitudes, in which the mean expected value was always zero. A graded influence of naloxone on reward outcome was evident in an attenuation of pleasure ratings for larger reward outcomes, an effect mirrored in attenuation of brain activity to increasing reward magnitude in rostral anterior cingulate cortex. A more striking effect was seen for losses such that under naloxone all levels of negative outcome were rated as more unpleasant. This hedonic effect was associated with enhanced activity in anterior insula and caudal anterior cingulate cortex, areas implicated in aversive processing. Our data indicate that a central opioid system contributes to both reward and loss processing in humans and directly modulates the hedonic experience of outcomes.
TL;DR: Functional magnetic resonance imaging results indicate that rewards can influence not only classical reward-related regions, but also early somatosensory cortex when a decision is required for that modality.
Abstract: Reinforcing effects of reward on action are well established, but possible effects on sensory function are less well explored. Here, using functional magnetic resonance imaging, we assessed whether reward can influence somatosensory judgments and modulate activity in human somatosensory cortex. Participants discriminated electrical somatosensory stimuli on an index finger with correct performance rewarded financially at trial end, at one of four different anticipated levels. Higher rewards improved tactile performance and led to increased hemodynamic signals from ventral striatum on rewarded trials. Remarkably, primary somatosensory cortex contralateral to the judged hand was reactivated at the point of reward delivery, despite the absence of concurrent somatosensory input at that time point. This side-specific reactivation of primary somatosensory cortex increased monotonically with level of reward. Moreover, the level of reward received on a particular trial influenced somatosensory performance and neural activity on the subsequent trial, with better discrimination and enhanced hemodynamic response in contralateral primary somatosensory cortex for trials that followed higher rewards. These results indicate that rewards can influence not only classical reward-related regions, but also early somatosensory cortex when a decision is required for that modality.
TL;DR: It is demonstrated that physostigmine can improve both stimulus- and attention-dependent responses in functionally affected extrastriate and frontoparietal regions in AD, while perturbing the normal pattern of responses in many of the same regions in healthy controls.
Abstract: Visuo-attentional deficits occur early in Alzheimer's disease (AD) and are considered more responsive to pro-cholinergic therapy than characteristic memory disturbances. We hypothesised that neural responses in AD during visuo-attentional processing would be impaired relative to controls, yet partially susceptible to improvement with the cholinesterase inhibitor physostigmine. We studied 16 mild AD patients and 17 age-matched healthy controls, using fMRI-scanning to enable within-subject placebo-controlled comparisons of effects of physostigmine on stimulus- and attention- related brain activations, plus between-group comparisons for these. Subjects viewed face or building stimuli while performing a shallow judgement (colour of image) or a deep judgement (young/old age of depicted face or building). Behaviourally, AD subjects performed slower than controls in both tasks, while physostigmine benefited the patients for the more demanding age-judgement task. Stimulus-selective (face minus building, and vice versa) BOLD signals in precuneus and posterior parahippocampal cortex were attenuated in patients relative to controls, but increased following physostigmine. By contrast, face-selective responses in fusiform cortex were not impaired in AD and showed decreases following physostigmine for both groups. Task-dependent responses in right parietal and prefrontal cortices were diminished in AD but improved following physostigmine. A similar pattern of group and treatment effects was observed in two extrastriate cortical regions that showed physostigmine-induced enhancement of stimulus-selectivity for the deep versus shallow task. Finally, for the healthy group, physostigmine decreased stimulus and task-dependent effects, partly due to an exaggeration of selectivity during the shallow relative to deep task. The differences in brain activations between groups and treatments were not attributable merely to performance (reaction time) differences. Our results demonstrate that physostigmine can improve both stimulus- and attention-dependent responses in functionally affected extrastriate and frontoparietal regions in AD, while perturbing the normal pattern of responses in many of the same regions in healthy controls.
TL;DR: Behavioural evidence is reported that β-adrenergic blockade with propranolol impairs attention independent of target valence, and increasing NE tone, using the selective NE reuptake inhibitor reboxetine, improves detection of emotional stimuli.
Abstract: Introduction Norepinephrine (NE) has a regulatory role in human attention. Objective To examine its role in emotional modulation of attention, we used an attentional blink (AB) paradigm, in the context of psychopharmacological manipulation, where targets were either emotional or neutral items. Results and discussion We report behavioural evidence that β-adrenergic blockade with propranolol impairs attention independent of target valence. Furthermore, this effect is centrally mediated as administration of the peripheral βadrenergic antagonist nadolol did not impair attention. By contrast, increasing NE tone, using the selective NE reuptake inhibitor reboxetine, improves detection of emotional stimuli. Conclusion In line with theoretical and animal models, these findings provide human behavioural evidence that the adrenergic system has a modulatory influence on selective attention that in some instances depends on item valence.
TL;DR: These results demonstrate distorted neuronal coding of reward probabilities in the absence of choice, stress the importance of experience with probabilistic outcomes and contrast with linear probability coding in the striatum.
Abstract: Reward probability crucially determines the value of outcomes. A basic phenomenon, defying explanation by traditional decision theories, is that people often overweigh small and underweigh large probabilities in choices under uncertainty. However, the neuronal basis of such reward probability distortions and their position in the decision process are largely unknown. We assessed individual probability distortions with behavioral pleasantness ratings and brain imaging in the absence of choice. Dorsolateral frontal cortex regions showed experience dependent overweighting of small, and underweighting of large, probabilities whereas ventral frontal regions showed the opposite pattern. These results demonstrate distorted neuronal coding of reward probabilities in the absence of choice, stress the importance of experience with probabilistic outcomes and contrast with linear probability coding in the striatum. Input of the distorted probability estimations to decision-making mechanisms are likely to contribute to well known inconsistencies in preferences formalized in theories of behavioral economics.
TL;DR: This review provides a personal and selective perspective on fMRI's past, present, and future through the detailed analysis of microcircuitry.
TL;DR: Only the familiarity component of recognition memory was impaired in frontal patients compared to healthy controls whilst the recollection-type (or variance ratio) processes remained intact.
TL;DR: It is concluded that amygdala and fusiform encode affective value in a manner that closely approximates a standard computational solution to learning.
Abstract: To monitor the environment for social threat humans must build affective evaluations of others. These evaluations are malleable and to a high degree shaped by responses engendered by specific social encounters. The precise neuronal mechanism by which these evaluations are constructed is poorly understood. We tested a hypothesis that conjoint activity in amygdala and fusiform gyrus would correlate with acquisition of social stimulus value. We tested this using a reinforcement learning algorithm, Q-learning, that assigned values to faces as a function of a history of pairing, or not pairing, with aversive shocks. Behaviourally, we observed a correlation between conditioning induced changes in skin conductance response (SCR) and subjective ratings for likeability of faces. Activity in both amygdala and fusiform gyrus (FG) correlated with the output of the reinforcement learning algorithm parameterized by these ratings. In amygdala, this effect was greater for averted than direct gaze faces. Furthermore, learning-related activity change in these regions correlated with SCR and subjective ratings. We conclude that amygdala and fusiform encode affective value in a manner that closely approximates a standard computational solution to learning.
TL;DR: In this paper, the authors used functional magnetic resonance imaging (FEMI) to assess whether reward can influence sensory judgments and modulate activity in human somatosensory cortex.
Abstract: Reinforcing effects of reward on action are well established, but possible effects on sensory function are less well explored. Here, using functional magnetic resonance imaging, we assessed whether reward can influence somatosensory judgments and modulate activity in human somatosensory cortex. Participants discriminated electrical somatosensory stimuli on an index finger with correct performance rewarded financially at trial end, at one of four different anticipated levels. Higher rewards improved tactile performance and led to increased hemodynamic signals from ventral striatum on rewarded trials. Remarkably, primary somatosensory cortex contralateral to the judged hand was reactivated at the point of reward delivery, despite the absence of concurrent somatosensory input at that time point. This side-specific reactivation of primary somatosensory cortex increased monotonically with level of reward. Moreover, the level of reward received on a particular trial influenced somatosensory performance and neural activity on the subsequent trial, with better discrimination and enhanced hemodynamic response in contralateral primary somatosensory cortex for trials that followed higher rewards. These results indicate that rewards can influence not only classical reward-related regions, but also early somatosensory cortex when a decision is required for that modality.
TL;DR: It is demonstrated that whereas emotional memory for aversive events per se is not influenced by 5-HTT polymorphism, an emotion-induced retrograde amnesia is expressed solely in the presence of the short allele, indicating a critical role for the serotonin system in emotion-mediated memory disruption.
Abstract: A polymorphism in the human serotonin transporter (5-HTT) gene is implicated in susceptibility to anxiety and depression and in enhanced emotion-induced activation in the amygdala A role for 5-HTT polymorphism in the emotional modulation of human episodic memory has yet to be demonstrated Here, we demonstrate that whereas emotional memory for aversive events per se is not influenced by 5-HTT polymorphism, an emotion-induced retrograde amnesia is expressed solely in the presence of the short allele The findings indicate a critical role for the serotonin system in emotion-mediated memory disruption
TL;DR: It is observed that memory for a target stimulus can be corrupted by distracters in the delay period, in contrast to theoretical predictions, and there is a trend towards a reduced distractibility under conditions of high reward.
Abstract: This work reports an empirical examination of two key issues in theoretical neuroscience: distractibility in the context of working memory (WM) and its reward dependence. While these issues have been examined fruitfully in isolation (e.g. Macoveanu et al. in Biol Cybern 96(4): 407–19, 2007), we address them here in tandem, with a focus on how distractibility and reward interact. In particular, we parameterise an observation model that embodies the nonlinear form of such interactions, as described in a recent neuronal network model (Gruber et al. in J Comput Neurosci 20:153–166, 2006). We observe that memory for a target stimulus can be corrupted by distracters in the delay period. Interestingly, in contrast to our theoretical predictions, this corruption was only partial. Distracters do not simply overwrite target; rather, a compromise is reached between target and distracter. Finally, we observed a trend towards a reduced distractibility under conditions of high reward. We discuss the implications of these findings for theoretical formulations of basal and dopamine (DA)-modulated neural bump- attractor networks of working memory.