Showing papers by "Raymond J. Dolan published in 2003"

Encoding predictive reward value in human amygdala and orbitofrontal cortex

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.

Human cingulate cortex and autonomic control: converging neuroimaging and clinical evidence

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.

Distinct spatial frequency sensitivities for processing faces and emotional expressions.

Abstract: High and low spatial frequency information in visual images is processed by distinct neural channels. Using event-related functional magnetic resonance imaging (fMRI) in humans, we show dissociable roles of such visual channels for processing faces and emotional fearful expressions. Neural responses in fusiform cortex, and effects of repeating the same face identity upon fusiform activity, were greater with intact or high-spatial-frequency face stimuli than with low-frequency faces, regardless of emotional expression. In contrast, amygdala responses to fearful expressions were greater for intact or low-frequency faces than for high-frequency faces. An activation of pulvinar and superior colliculus by fearful expressions occurred specifically with low-frequency faces, suggesting that these subcortical pathways may provide coarse fear-related inputs to the amygdala.

Dissociating valence of outcome from behavioral control in human orbital and ventral prefrontal cortices.

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.

An emotion-induced retrograde amnesia in humans is amygdala- and beta-adrenergic-dependent.

Abstract: The influence of emotion on human memory is associated with two contradictory effects in the form of either emotion-induced enhancements or decrements in memory. In a series of experiments involving single word presentation, we show that enhanced memory for emotional words is strongly coupled to decrements in memory for items preceding the emotional stimulus, an effect that is more pronounced in women. These memory effects would appear to depend on a common neurobiological substrate, in that enhancements and decrements are reversed by propranolol, a β-adrenergic antagonist, and abolished by selective bilateral amygdala damage. Thus, our findings suggest that amygdala-dependent β-adrenergic modulation of episodic encoding has costs as well as benefits.

Effects of Attention and Emotion on Repetition Priming and Their Modulation by Cholinergic Enhancement

Abstract: We examined whether behavioral and neural effects of repeating faces are modulated by independent factors of selective attention, emotion, and cholinergic enhancement, during functional MRI. Face repetition occurred either between task-relevant (spatially attended) or task-irrelevant (unattended) stimuli; faces could be fearful or neutral; subjects received either placebo or physostigmine. Under placebo, a reaction time advantage occurred with repetition (i.e., priming) that did not differ between levels of attention, but was attenuated with emotion. Inferior temporo-occipital cortex demonstrated repetition decreases to both attended and unattended faces, and showed either equivalent or greater repetition decreases with emotional compared with neutral faces. By contrast, repetition decreases were attenuated for emotional relative to neutral faces in lateral orbitofrontal cortex. These results distinguish automatic repetition effects in sensory cortical regions from repetition effects modulated by emotion in orbitofrontal cortex, which parallel behavioral effects. Under physostigmine, unlike placebo, behavioral repetition effects were seen selectively for attended faces only, whereas emotional faces no longer impaired priming. Physostigmine enhanced repetition decreases in inferior occipital cortex selectively for attended faces, and reversed the emotional interaction with repetition in lateral orbitofrontal cortex. Thus we show that cholinergic enhancement both augments a neural signature of priming and modulates the effects of attention and emotion on behavioral and neural consequences of repetition.

Reciprocal links between emotion and attention

Abstract: Attention and emotion share many reciprocal links. Both attention and emotion involve distributed neural networks of highly interactive cortical and subcortical brain regions that are in a position to regulate processes related to perception, action, and memory. This chapter reviews evidence from human functional neuroimaging investigation indicating that dedicated brain systems are specifically tuned to process emotional information. In particular, it discusses how emotional processing can interact with attentional systems, focusing on the neural mechanisms by which emotion can affect the allocation of attention, as well as the degree to which selective attention in turn influences emotional processing. Moreover, reciprocal interactions between emotion, attention, and cognition have potentially important implications for understanding a number of psychiatric diseases. An abnormal modulation of attention by emotion, mood, or past affective experiences has now been observed by both behavioral and imaging studies in a variety of conditions, including anxiety, phobia, posttraumatic stress disorder, obsessive-compulsive disorder, depression, or schizophrenia. This constitutes a new challenge for cognitive neuroscience, which can now be powerfully addressed by neuroimaging research. © 2004 Elsevier Inc. All rights reserved.

Neuronal correlates of familiarity-driven decisions in artificial grammar learning.

Abstract: It has been proposed on the basis of behavioural data that grammaticality judgments in implicit artificial grammar learning paradigms are largely driven by priming based on fragment familiarity. A prediction that follows from this account is that neural deactivation, a common correlate of repetition priming, should be observed for grammatical compared to ungrammatical stimuli. We conducted an event-related fMRI study to investigate neuronal correlates of such fragment-based priming. In a study phase, participants performed a short-term memory task on a series of strings of pseudofont characters. Scanning was performed in a subsequent test phase in which participants classified new strings as either grammatical or ungrammatical. Test strings differed systematically from training strings in terms of exemplar and fragment similarity. Behaviourally, participants classified strings as grammatical based on fragment familiarity. Differential activity was evident during string classification as reduced activity in left lateral occipital complex and bilateral lingual gyri for strings with high fragment familiarity compared to strings with low fragment familiarity. Thus, consistent with the hypothesis, neuronal facilitation in extrastriate occipital regions may constitute one basis of implicit grammaticality decisions based on fragment priming.

Functional neuroanatomy of human emotion

Abstract: This chapter reviews recent findings in the neuroscientific study of emotion focusing on data from human functional neuroimaging experiments. It begins with a brief historical overview of theories of emotion. Neuroimaging experiments have demonstrated the importance of functional integration of emotional and non-emotional processes in the brain, as well as functional specialization of distinct brain regions. The neuroscientific investigation of emotion has been hindered in the past by a philosophical dualism that tended to emphasize the separation of affective and cognitive processes. The revival of evolutionary, comparative approaches has enabled emotion and cognition to be viewed from a common neurobiological perspective rather than from the separate domains of metapsychology and cognitive psychology. Furthermore, the concept of value- dependent neural selection has proved valuable in modeling emotional processes in the brain, as it combines an evolutionary perspective with an explicit account of both functional integration and functional segregation. The combination of molecular genetics and functional neuroimaging can be a powerful tool in the investigation of the neural basis of human emotion. © 2004 Elsevier Inc. All rights reserved.