Showing papers by "Raymond J. Dolan published in 2004"
TL;DR: Only that part of the pain network associated with its affective qualities, but not its sensory qualities, mediates empathy, suggesting that the neural substrate for empathic experience does not involve the entire "pain matrix".
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.
3,425 citations
TL;DR: In right anterior insular/opercular cortex, neural activity predicted subjects' accuracy in the heartbeat detection task and local gray matter volume correlated with both interoceptive accuracy and subjective ratings of visceral awareness.
Abstract: Influential theories of human emotion argue that subjective feeling states involve representation of bodily responses elicited by emotional events. Within this framework, individual differences in intensity of emotional experience reflect variation in sensitivity to internal bodily responses. We measured regional brain activity by functional magnetic resonance imaging (fMRI) during an interoceptive task wherein subjects judged the timing of their own heartbeats. We observed enhanced activity in insula, somatomotor and cingulate cortices. In right anterior insular/opercular cortex, neural activity predicted subjects' accuracy in the heartbeat detection task. Furthermore, local gray matter volume in the same region correlated with both interoceptive accuracy and subjective ratings of visceral awareness. Indices of negative emotional experience correlated with interoceptive accuracy across subjects. These findings indicate that right anterior insula supports a representation of visceral responses accessible to awareness, providing a substrate for subjective feeling states.
2,972 citations
TL;DR: This work scanned human participants with functional magnetic resonance imaging while they engaged in instrumental conditioning to suggest partly dissociable contributions of the ventral and dorsal striatum to the critic and the actor.
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.
2,049 citations
TL;DR: The data show that combining the fMRI and lesion approaches can help reveal the source of functional modulatory influences between distant but interconnected brain regions.
Abstract: Emotional visual stimuli evoke enhanced responses in the visual cortex. To test whether this reflects modulatory influences from the amygdala on sensory processing, we used event-related functional magnetic resonance imaging (fMRI) in human patients with medial temporal lobe sclerosis. Twenty-six patients with lesions in the amygdala, the hippocampus or both, plus 13 matched healthy controls, were shown pictures of fearful or neutral faces in task-releant or task-irrelevant positions on the display. All subjects showed increased fusiform cortex activation when the faces were in task-relevant positions. Both healthy individuals and those with hippocampal damage showed increased activation in the fusiform and occipital cortex when they were shown fearful faces, but this was not the case for individuals with damage to the amygdala, even though visual areas were structurally intact. The distant influence of the amygdala was also evidenced by the parametric relationship between amygdala damage and the level of emotional activation in the fusiform cortex. Our data show that combining the fMRI and lesion approaches can help reveal the source of functional modulatory influences between distant but interconnected brain regions.
903 citations
TL;DR: It is shown that neural activity in the ventral striatum and the anterior insula displays a marked correspondence to the signals for sequential learning predicted by temporal difference models, revealing a flexible aversive learning process ideally suited to the changing and uncertain nature of real-world environments.
Abstract: The ability to use environmental stimuli to predict impending harm is critical for survival. Such predictions should be available as early as they are reliable. In pavlovian conditioning, chains of successively earlier predictors are studied in terms of higher-order relationships, and have inspired computational theories such as temporal difference learning. However, there is at present no adequate neurobiological account of how this learning occurs. Here, in a functional magnetic resonance imaging (fMRI) study of higher-order aversive conditioning, we describe a key computational strategy that humans use to learn predictions about pain. We show that neural activity in the ventral striatum and the anterior insula displays a marked correspondence to the signals for sequential learning predicted by temporal difference models. This result reveals a flexible aversive learning process ideally suited to the changing and uncertain nature of real-world environments. Taken with existing data on reward learning, our results suggest a critical role for the ventral striatum in integrating complex appetitive and aversive predictions to coordinate behaviour.
592 citations
TL;DR: Data indicate a reciprocal dependence between amygdala and hippocampus during the encoding of emotional memories in patients with variable degrees of left hippocampal and amygdala pathology who performed a verbal encoding task during functional magnetic resonance imaging.
Abstract: We have studied patients with variable degrees of left hippocampal and amygdala pathology who performed a verbal encoding task during functional magnetic resonance imaging (fMRI) to assess the impact of pathology on emotional-memory performance and encoding-evoked activity. The severity of left hippocampal pathology predicted memory performance for neutral and emotional items alike, whereas the severity of amygdala pathology predicted memory performance for emotional items alone. Encoding-related hippocampal activity for successfully remembered emotional items correlated with the degree of left amygdala pathology. Conversely, amygdala-evoked activity with respect to subsequently remembered emotional items correlated with the degree of left hippocampal pathology. Our data indicate a reciprocal dependence between amygdala and hippocampus during the encoding of emotional memories.
486 citations
TL;DR: Results provide neuroanatomical evidence for the distributed model of face processing and highlight a dissociation within right STS between a caudal segment coding identity and a more rostral region coding emotional expression.
Abstract: The distributed model of face processing proposes an anatomical dissociation between brain regions that encode invariant aspects of faces, such as identity, and those that encode changeable aspects of faces, such as expression. We tested for a neuroanatomical dissociation for identity and expression in face perception using a functional MRI (fMRI) adaptation paradigm. Repeating identity across face pairs led to reduced fMRI signal in fusiform cortex and posterior superior temporal sulcus (STS), whereas repeating emotional expression across pairs led to reduced signal in a more anterior region of STS. These results provide neuroanatomical evidence for the distributed model of face processing and highlight a dissociation within right STS between a caudal segment coding identity and a more rostral region coding emotional expression.
483 citations
TL;DR: The data indicate that rapid learning regarding the moral status of others is expressed in altered neural activity within a system associated with social cognition, and this indicates the saliency of social fairness for human interactions.
416 citations
TL;DR: The findings point to a dissociation between neural systems controlling basal sympathetic tone (SCL) and transient skin conductance responses (SCRs), indicating that activity within VMPFC and OFC reflects a dynamic between exteroceptive and interoceptive deployment of attention.
412 citations
TL;DR: Findings provide a likely functional neuroanatomical substrate for the CNV and demonstrate modulation of components of this neural circuitry by peripheral autonomic arousal, and suggest a mechanistic model whereby thalamocortical interactions regulate CNV amplitude.
347 citations
TL;DR: Functional magnetic resonance imaging was used to measure human brain activity evoked during olfactory aversive conditioning and extinction learning and showed that a CS+ retains access to representations of UCS value in distinct regions of ventral prefrontal cortex, even as extinction proceeds.
Abstract: In extinction, an animal learns that a previously conditioned stimulus (CS+) no longer predicts delivery of a salient reinforcer (unconditioned stimulus, UCS). Rodent studies indicate that extinction relies on amygdala-prefrontal interactions and involves formation of memories that inhibit, without actually erasing, the original conditioning trace. Whether extinction learning in humans follows similar neurobiological principles is unknown. We used functional magnetic resonance imaging to measure human brain activity evoked during olfactory aversive conditioning and extinction learning. Neural responses in orbitofrontal cortex and amygdala were preferentially enhanced during extinction, suggesting potential cross-species preservation of learning mechanisms that oppose conditioning. Moreover, by manipulating UCS aversiveness via reinforcer inflation, we showed that a CS+ retains access to representations of UCS value in distinct regions of ventral prefrontal cortex, even as extinction proceeds.
TL;DR: The results suggest that human emotional memory is associated with a beta-adrenergic-dependent modulation of amygdala-hippocampal interactions, and that administration of the propranolol at encoding abolishes the enhanced amygdala encoding and hippocampal retrieval effects.
Abstract: Human emotional experience is typically associated with enhanced episodic memory. We have used functional magnetic resonance imaging to demonstrate that successful encoding of emotional, compared to neutral, verbal stimuli evokes increased human amygdala responses. Items that evoke amygdala activation at encoding evoke greater hippocampal responses at retrieval compared to neutral items. Administration of the β-adrenergic antagonist propranolol at encoding abolishes the enhanced amygdala encoding and hippocampal retrieval effects, despite propranolol being no longer present at retrieval. Thus, memory-related amygdala responses at encoding and hippocampal responses at recognition for emotional items depend on β-adrenergic engagement at encoding. Our results suggest that human emotional memory is associated with a β-adrenergic-dependent modulation of amygdala-hippocampal interactions.
TL;DR: PET during audiovisual speech processing used to study how temporal and spatial factors might jointly affect brain activations yielded increased activity in multisensory association areas, plus in some unimodal visual areas.
TL;DR: For instance, this paper found that deductive and inductive reasoning are distinct logical and psychological processes, and little is known about their respective neural basis, while inductive and deductive reasoning can be distinguished by activation of left lateral prefrontal and bilateral dorsal frontal, parietal and occipital cortex.
TL;DR: It is suggested that reactivation of memory traces distributed across modality-specific brain areas underpins the sensory qualities of episodic memories.
TL;DR: Encoding of emotionally neutral pictures in association with positively, neutrally or negatively valenced background contexts led to differential modulation of neural activity elicited in a subsequent recognition memory test for these pictures, which discussed the findings in terms of current models of emotional memory retrieval.
TL;DR: A critical role for ventral and medial dysfunction in the pathology of mania is suggested, which might underpin aspects of cognitive and clinical symptomatology.
TL;DR: It is reported here the first demonstration of a clinically valuable role for cognitive fMRI in the investigation of patients with Temporal lobe epilepsy, commonly caused by hippocampal sclerosis who underwent left hippocampal resection.
Abstract: Functional MRI (fMRI) of cognitive tasks depends on technology widely available in the clinical sphere, but has yet to show a role in the investigation of patients. We report here the first demonstration of a clinically valuable role for cognitive fMRI. Temporal lobe epilepsy (TLE) is commonly caused by hippocampal sclerosis and is frequently resistant to drug treatment. Surgical resection of the left hippocampus in this setting can cure seizures, but may produce significant verbal memory decline, which is hard to predict. We report 10 right-handed TLE patients with left hippocampal sclerosis who underwent left hippocampal resection. We compared currently used data for the prediction of post-operative verbal memory decline in such patients with a novel fMRI assessment of verbal memory encoding. Multiple regression analyses showed that fMRI provided the strongest independent predictor of memory outcome after surgery. At the individual subject level, the fMRI data had high positive predictive value for memory decline.
TL;DR: It is suggested that, while cholinergic enhancement facilitates visual attention by increasing activity in extrastriate cortex generally, it accomplishes this in a manner that reduces expectation-driven selective biasing of extrastiate cortex.
TL;DR: While orbitofrontal cortex exhibited rapid reversal of acquired fear responses, ventral amygdala showed a persistent, nonreversing "memory" for previous fear-related stimulus associations.
TL;DR: A critical role for attention is suggested in achieving visual representations of objects that lead to both BOLD signal decreases and behavioral priming on repeated presentation.
Abstract: Functional imaging studies of priming-related repetition phenomena have become widely used to study neural object representation. Although blood oxygenation level–dependent (BOLD) repetition decrea...
TL;DR: The findings indicate that retrieval processing is influenced by the emotional valence of the context in which an item is encoded, regardless of whether contextual information is task relevant.
Abstract: In two experiments, we examined event-related potentials (ERPs) elicited in an old/new recognition memory test by emotionally neutral visual objects that, at encoding, had been associated with neutrally, negatively, or positively valenced background contexts. In Experiment 2, subjects also judged the context in which the item had been studied. In Experiment 1, ''left parietal'' old/new ERP effects were elicited by correctly recognized items. Items encoded in emotional contexts, but not those studied in neutral contexts, elicited additional effects early in the recording epoch over lateral temporal scalp and, later, over left temporo-frontal scalp. In Experiment 2, ''left parietal'' and ''right frontal'' ERP effects were elicited by recognized items that attracted correct source judgments. Additional effects, an early lateral temporal positivity and a late-onset, left-sided positivity, were elicited by items studied in emotionally valenced contexts and attracting correct source judgments. Together, the findings indicate that retrieval processing is influenced by the emotional valence of the context in which an item is encoded, regardless of whether contextual information is task relevant.
TL;DR: A robust positive relationship is observed between right-lateralized asymmetry in midbrain activity and proarrhythmic abnormalities of cardiac repolarization (apparent in two independent ECG measures) during stress, which provides empirical support for a putative mechanism for stress-induced sudden death.
Abstract: Patients with specific neurological, psychiatric or cardiovascular conditions are at enhanced risk of cardiac arrhythmia and sudden death. The neurogenic mechanisms are poorly understood. However, in many cases, stress may precipitate cardiac arrhythmia and sudden death in vulnerable patients, presumably via centrally driven autonomic nervous system responses. From a cardiological perspective, the likelihood of arrhythmia is strongly associated with abnormalities in electrical repolarization (recovery) of the heart muscle after each contraction. Inhomogeneous and asymmetric repolarization, reflected in ECG T-wave abnormalities, is associated with a greatly increased risk of arrhythmia, i.e. a proarrhythmic state. We therefore undertook a study to identify the brain mechanisms by which stress can induce cardiac arrhythmia through efferent autonomic drive. We recruited a typical group of 10 out-patients attending a cardiological clinic. We simultaneously measured brain activity, using H2(15)O PET, and the proarrhythmic state of the heart, using ECG, during mental and physical stress challenges and corresponding control conditions. Proarrhythmic changes in the heart were quantified from two ECG-derived measures of repolarization inhomogeneity and were related to changes in magnitude and lateralization of regional brain activity reflected in regional cerebral blood flow. Across the patient group, we observed a robust positive relationship between right-lateralized asymmetry in midbrain activity and proarrhythmic abnormalities of cardiac repolarization (apparent in two independent ECG measures) during stress. This association between stress-induced lateralization of midbrain activity and enhanced arrhythmic vulnerability provides empirical support for a putative mechanism for stress-induced sudden death, wherein lateralization of central autonomic drive during stress results in imbalanced activity in right and left cardiac sympathetic nerves. A right-left asymmetry in sympathetic drive across the surface of the heart disrupts the electrophysiological homogeneity of ventricular repolarization, predisposing to arrhythmia. Our findings highlight a proximal brain basis for stress-induced cardiac arrhythmic vulnerability.
TL;DR: The findings of the present study are consistent with the hypothesis of decreased frontal-striatal control of limbic structures, specifically the amygdala, resulting in an inadequate fear response in OCD patients with contamination fear.
Abstract: Previous imaging studies of obsessive-compulsive symptom states have implicated frontal-striatal and limbic regions in the pathophysiology of obsessive-compulsive disorder (OCD). Functional imaging studies, however, have yielded inconsistent results, presumably due to methodological differences (patient inclusion criteria, stimulus paradigm, imaging technique, and absence of control groups). In the present study, randomized presentation of contamination-related and neutral visual stimuli was used to investigate the neurophysiological correlates of contamination fear in a group of medication-free OCD patients with washing behaviors and healthy controls. A total of 21 subjects (11 OCD patients and 10 healthy controls) were scanned using H(2)(15)O positron emission tomography (PET). Subjects were presented with pictures of clean and dirty surroundings and were requested to make indoor/outdoor decisions to control for attention differences. State anxiety and obsessionality were rated after each scan using visual analogue scales. Main effects of stimulus type (contamination vs. neutral) were found in bilateral occipital cortex in both groups. A significant group interaction effect was observed in the left amygdala reflecting enhanced activity in response to contamination stimuli in OCD patients. Sensitization effects were observed in the right amygdala in the OCD group; these paralleled an increase in levels of distress and obsessionality as well as a decrease in dorsolateral prefrontal activity. The findings of the present study are consistent with the hypothesis of decreased frontal-striatal control of limbic structures, specifically the amygdala, resulting in an inadequate fear response in OCD patients with contamination fear.
TL;DR: The findings suggest that emotional and social functioning is not critically tied to on-going experience of autonomic arousal state, and acquisition of autonomics failure late in life may protect against maladaptive social behaviour through established behavioural responses that may be associated with central "as if" representations.
TL;DR: It is concluded that prolonged exposure to phobic stimuli is associated with a significant decrease in bilateral anterior MTL regional cerebral blood flow, which implicates this region in phobic fear.
Abstract: Imaging studies using symptom-provocation paradigms in specific phobia have yielded contradictory results, possibly reflecting a failure to account for habituation processes. Given that a single session of exposure in vivo can result in significant improvement in specific phobia, we used prolonged exposure to phobic stimuli to identify CNS regions showing habituation. Eighteen subjects (12 with spider phobia, 6 healthy controls) underwent H(2)(15)O-positron emission tomography while being continuously presented with pictures of spiders or butterflies. Results showed main effects (spiders>butterflies) in the phobia group in the left fusiform gyrus (FG) and the right parahippocampal gyrus (PHG), with bilateral perirhinal cortex and right limbic areas approaching significance. Group x condition effects were found in the right amygdala and PHG. During spider scans, large habituation effects were observed in the anterior medial temporal lobe (MTL) bilaterally. Regression analyses demonstrated that state anxiety was correlated with activity in left amygdala, bilateral perirhinal cortex, right FG, and periaquaductal grey; by contrast, phobic fear was only associated with right-sided hippocampal activity. We conclude that prolonged exposure to phobic stimuli is associated with a significant decrease in bilateral anterior MTL regional cerebral blood flow. Right anterior MTL, identified when comparing phobic vs. neutral stimuli and habituation to phobic vs. neutral stimuli in the phobia group, implicates this region in phobic fear. Analyses of covariance suggest a further functional segregation with state anxiety being linked to enhanced activity in amygdala, perirhinal cortex, and tegmentum, and phobic fear with enhanced right hippocampal activity, suggesting a neuroanatomical differentiation between emotional-vegetative and cognitive aspects of (phobic) fear.
TL;DR: A complementary perspective is provided to show how a focus on response pattern differences can elucidate the functional roles of regions subserving olfactory‐visual integration, and the first of these response patterns was identified in the formal interaction between odors and pictures.
01 Apr 2004
TL;DR: In this article, a distinction is drawn between brain systems that mediate relatively automatic responses to emotional stimuli and systems that are involved in what can be termed conscious feeling states, and these distinctions are illustrated by observations from functional neuroimaging and patients with focal brain lesions and pathology of the autonomic nervous system.
Abstract: ABSTRACT An essential feature of emotional states is their association with change in autonomic function. The importance of these changes lies in the fact that in many theoretical accounts of emotion the realization of autonomic states is a primary means through which feeling states are realized. The issue addressed in this chapter is how the brain generates and represents autonomic states of the organism and their importance in feeling states. A distinction will be drawn between brain systems that mediate relatively automatic responses to emotional stimuli and systems that are involved in what can be termed conscious feeling states. These distinctions will be illustrated by observations from functional neuroimaging and patients with focal brain lesions and pathology of the autonomic nervous system. Despite the impact of William James at the end of the nineteenth century, for the best part of several decades in the middle of the twentieth century, neuroscientists treated “emotion” and “feeling” as interchangeable terms. This approach to the language of emotion, coupled with the behaviorist movement prevalent in twentieth century psychology, meant that the neuroscientific study of emotion was grossly neglected, often seen as conceptually ragged and its practitioners as pursuing “soft science” (Damasio, 1999; Damasio, 1994; Damasio, 1998; LeDoux, 1996; LeDoux, 2000). Recent efforts, however, have put the study of emotion center stage in understanding the workings of the brain, proposing roles in cognition (Zajonc, 1980), decision making (Damasio, 1994), perception (Anderson & Phelps, 2001), and even consciousness (Panksepp, 1998; Damasio, 1999).