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ABSTRACT: Attractiveness is a facial attribute that shapes human affiliative behaviours. In a previous study we reported a linear response to facial attractiveness in orbitofrontal cortex (OFC), a region involved in reward processing. There are strong theoretical grounds for the hypothesis that coding stimulus reward value also involves the amygdala. The aim of the present investigation is to address whether the amygdala is also sensitive to reward value in faces, indexed as facial attractiveness. We hypothesized that contrary to the linear effects reported previously in OFC, the amygdala would show a non-linear effect of attractiveness by responding to both high and low attractive faces relative to middle attractive faces. Such a non-linear response would explain previous failures to report an amygdala response to attractiveness. Human subjects underwent fMRI while they were presented with faces that varied in facial attractiveness where the task was either to rate faces for facial attractiveness or for age. Consistent with our hypothesis, right amygdala showed a predicted non-linear response profile with greater responses to highly attractive and unattractive faces compared to middle-ranked faces, independent of task. Distinct patterns of activity were seen across different regions of OFC, with some sectors showing linear effects of attractiveness, others exhibiting a non-linear response profile and still others demonstrating activation only during age judgments. Significant effects were also seen in medial prefrontal and paracingulate cortices, posterior OFC, insula, and superior temporal sulcus during explicit attractiveness judgments. The non-linear response profile of the amygdala is consistent with a role in sensing the value of social stimuli, a function that may also involve specific sectors of the OFC.
Neuropsychologia 02/2007; 45(1):195-206. · 3.64 Impact Factor
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ABSTRACT: An essential, evolutionarily stable feature of brain function is the detection of animate entities, and one of the main cues to identify them is their movement. We developed a model of a simple interaction between two objects, in which an increase of the correlation between their movements varied the amount of interactivity and animacy observers attributed to them. Functional magnetic resonance imaging revealed that activation in the posterior superior temporal sulcus and gyrus (pSTS/pSTG) increased in relation to the degree of correlated motion between the two objects. This activation increase was not different when subjects performed an explicit or implicit task while observing these interacting objects. These data suggest that the pSTS and pSTG play a role in the automatic identification of animate entities, by responding directly to an objective movement characteristic inducing the percept of animacy, such as the amount of interactivity between two moving objects.
Neuron 03/2005; 45(4):625-35. · 14.74 Impact Factor
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ABSTRACT: The James-Lange theory of emotion proposes that automatically generated bodily reactions not only color subjective emotional experience of stimuli, but also necessitate a mechanism by which these bodily reactions are differentially generated to reflect stimulus quality. To examine this putative mechanism, we simultaneously measured brain activity and heart rate to identify regions where neural activity predicted the magnitude of heart rate responses to emotional facial expressions. Using a forewarned reaction time task, we showed that orienting heart rate acceleration to emotional face stimuli was modulated as a function of the emotion depicted. The magnitude of evoked heart rate increase, both across the stimulus set and within each emotion category, was predicted by level of activity within a matrix of interconnected brain regions, including amygdala, insula, anterior cingulate, and brainstem. We suggest that these regions provide a substrate for translating visual perception of emotional facial expression into differential cardiac responses and thereby represent an interface for selective generation of visceral reactions that contribute to the embodied component of emotional reaction.
NeuroImage 03/2005; 24(3):751-62. · 5.89 Impact Factor
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ABSTRACT: Humans have a unique ability to learn more than one language--a skill that is thought to be mediated by functional (rather than structural) plastic changes in the brain. Here we show that learning a second language increases the density of grey matter in the left inferior parietal cortex and that the degree of structural reorganization in this region is modulated by the proficiency attained and the age at acquisition. This relation between grey-matter density and performance may represent a general principle of brain organization.
Nature 11/2004; 431(7010):757. · 36.28 Impact Factor
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ABSTRACT: Instrumental conditioning studies how animals and humans choose actions appropriate to the affective structure of an environment. According to recent reinforcement learning models, two distinct components are involved: a "critic," which learns to predict future reward, and an "actor," which maintains information about the rewarding outcomes of actions to enable better ones to be chosen more frequently. We scanned human participants with functional magnetic resonance imaging while they engaged in instrumental conditioning. Our results suggest partly dissociable contributions of the ventral and dorsal striatum, with the former corresponding to the critic and the latter corresponding to the actor.
Science 05/2004; 304(5669):452-4. · 31.20 Impact Factor
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ABSTRACT: Our ability to have an experience of another's pain is characteristic of empathy. Using functional imaging, we assessed brain activity while volunteers experienced a painful stimulus and compared it to that elicited when they observed a signal indicating that their loved one--present in the same room--was receiving a similar pain stimulus. Bilateral anterior insula (AI), rostral anterior cingulate cortex (ACC), brainstem, and cerebellum were activated when subjects received pain and also by a signal that a loved one experienced pain. AI and ACC activation correlated with individual empathy scores. Activity in the posterior insula/secondary somatosensory cortex, the sensorimotor cortex (SI/MI), and the caudal ACC was specific to receiving pain. Thus, a neural response in AI and rostral ACC, activated in common for "self" and "other" conditions, suggests that the neural substrate for empathic experience does not involve the entire "pain matrix." We conclude that only that part of the pain network associated with its affective qualities, but not its sensory qualities, mediates empathy.
Science 03/2004; 303(5661):1157-62. · 31.20 Impact Factor
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ABSTRACT: Human anterior cingulate function has been explained primarily within a cognitive framework. We used functional MRI experiments with simultaneous electrocardiography to examine regional brain activity associated with autonomic cardiovascular control during performance of cognitive and motor tasks. Using indices of heart rate variability, and high- and low-frequency power in the cardiac rhythm, we observed activity in the dorsal anterior cingulate cortex (ACC) related to sympathetic modulation of heart rate that was dissociable from cognitive and motor-related activity. The findings predict that during effortful cognitive and motor behaviour the dorsal ACC supports the generation of associated autonomic states of cardiovascular arousal. We subsequently tested this prediction by studying three patients with focal damage involving the ACC while they performed effortful cognitive and motor tests. Each showed abnormalities in autonomic cardiovascular responses with blunted autonomic arousal to mental stress when compared with 147 normal subjects tested in identical fashion. Thus, converging neuroimaging and clinical findings suggest that ACC function mediates context-driven modulation of bodily arousal states.
Brain 11/2003; 126(Pt 10):2139-52. · 9.46 Impact Factor
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John O'Doherty
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ABSTRACT: Basolateral amygdala and orbitofrontal cortex are implicated in cue-outcome learning. In this issue of Neuron, Schoenbaum et al. show that, following basolateral amygdala lesions, cue-selective neurons in orbitofrontal cortex are more sensory driven and less sensitive to the motivational value of an outcome, suggesting that predictive value coding in orbitofrontal cortex is dependent on input from basolateral amygdala.
Neuron 09/2003; 39(5):731-3. · 14.74 Impact Factor
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ABSTRACT: Adaptive behavior is optimized in organisms that maintain flexible representations of the value of sensory-predictive cues. To identify central representations of predictive reward value in humans, we used reinforcer devaluation while measuring neural activity with functional magnetic resonance imaging. We presented two arbitrary visual stimuli, both before and after olfactory devaluation, in a paradigm of appetitive conditioning. In amygdala and orbitofrontal cortex, responses evoked by a predictive target stimulus were decreased after devaluation, whereas responses to the nondevalued stimulus were maintained. Thus, differential activity in amygdala and orbitofrontal cortex encodes the current value of reward representations accessible to predictive cues.
Science 09/2003; 301(5636):1104-7. · 31.20 Impact Factor
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ABSTRACT: The precise role of orbitofrontal cortex (OFC) in affective processing is still debated. One view suggests OFC represents stimulus reward value and supports learning and relearning of stimulus-reward associations. An alternate view implicates OFC in behavioral control after rewarding or punishing feedback. To discriminate between these possibilities, we used event-related functional magnetic resonance imaging in subjects performing a reversal task in which, on each trial, selection of the correct stimulus led to a 70% probability of receiving a monetary reward and a 30% probability of obtaining a monetary punishment. The incorrect stimulus had the reverse contingency. In one condition (choice), subjects had to choose which stimulus to select and switch their response to the other stimulus once contingencies had changed. In another condition (imperative), subjects had simply to track the currently rewarded stimulus. In some regions of OFC and medial prefrontal cortex, activity was related to valence of outcome, whereas in adjacent areas activity was associated with behavioral choice, signaling maintenance of the current response strategy on a subsequent trial. Caudolateral OFC-anterior insula was activated by punishing feedback preceding a switch in stimulus in both the choice and imperative conditions, indicating a possible role for this region in signaling a change in reward contingencies. These results suggest functional heterogeneity within the OFC, with a role for this region in representing stimulus-reward values, signaling changes in reinforcement contingencies and in behavioral control.
Journal of Neuroscience 09/2003; 23(21):7931-9. · 7.11 Impact Factor
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ABSTRACT: We combined event-related functional magnetic resonance imaging (fMRI) with olfactory classical conditioning to differentiate the neural responses evoked during appetitive and aversive olfactory learning. Three neutral faces [the conditioned stimuli (CS+)] were repetitively paired with pleasant, neutral, or unpleasant odors [the unconditioned stimuli (UCS)] in a partial reinforcement schedule. A fourth face was never paired to odor [the nonconditioned stimulus (CS-)]. Learning-related neural activity, comparing unpaired (face only) CS+ stimuli with CS-, showed valence-independent activations in rostral and caudal orbitofrontal cortex (OFC). Medial OFC responded to the appetitive (app) CS+, whereas lateral OFC responded to the aversive (av) CS+. Within nucleus accumbens, neural responses showed divergent activation profiles that increased with time in response to the appCS+ but decreased in response to the avCS+. In posterior amygdala, responses were elicited by the appCS+, which habituated over time. In temporal piriform cortex, neural responses were evoked by the avCS+, which progressively increased with time. These results highlight regional and temporal dissociations during olfactory learning and imply that emotionally salient odors can engender cross-modal associative learning. Moreover, the findings suggest that the role of human primary (piriform) and secondary olfactory cortices transcends their function as mere intermediaries of chemosensory information processing.
Journal of Neuroscience 01/2003; 22(24):10829-37. · 7.11 Impact Factor
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Science (New York, NY). 304:452-454.
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Neuron. 45(4):625-635.