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Biomedical subjects

Ralph Adolphs

Publications and source records attributed to Ralph Adolphs.

At least 19 recordsLinked to original sources

Abnormal use of facial information in high-functioning autism.

Altered visual exploration of faces likely contributes to social cognition deficits seen in autism. To investigate the relationship between face gaze and social cognition in autism, we measured both face gaze and how facial regions were actually used during emotion judgments from faces. Compared to IQ-matched healthy controls, nine high-functioning adults with autism failed to make use of information from the eye region of faces, instead relying primarily on information from the mouth. Face gaze accounted for the increased reliance on the mouth, and partially accounted for the deficit in using information from the eyes. These findings provide a novel quantitative assessment of how people with autism utilize information in faces when making social judgments.

Adult↗

Looking at other people: mechanisms for social perception revealed in subjects with focal amygdala damage.

How does the presence of socially relevant information in the environment influence our perception and judgment of other people? We have investigated how we direct our gaze to other people's faces, how we use specific features from faces to make social judgments about the presumed internal states of others, and how these mechanisms are disrupted following pathology. Studies of patients with damage to the amygdala have demonstrated a specific impairment in the ability to direct gaze towards, and to use information from, the eyes in others' faces. This basic impairment may explain the deficient recognition of basic emotions and deficient social judgment seen in such patients. Ongoing studies in our laboratory examine face-to-face social interactions with real people in an attempt to link the above impairments in the laboratory to the dysfunctional social cognition seen in everyday life.

Amygdala↗

Amygdala damage impairs emotion recognition from music.

The role of the amygdala in recognition of danger is well established for visual stimuli such as faces. A similar role in another class of emotionally potent stimuli -- music -- has been recently suggested by the study of epileptic patients with unilateral resection of the anteromedian part of the temporal lobe [Gosselin, N., Peretz, I., Noulhiane, M., Hasboun, D., Beckett, C., & Baulac, M., et al. (2005). Impaired recognition of scary music following unilateral temporal lobe excision. Brain, 128(Pt 3), 628-640]. The goal of the present study was to assess the specific role of the amygdala in the recognition of fear from music. To this aim, we investigated a rare subject, S.M., who has complete bilateral damage relatively restricted to the amygdala and not encompassing other sectors of the temporal lobe. In Experiment 1, S.M. and four matched controls were asked to rate the intensity of fear, peacefulness, happiness, and sadness from computer-generated instrumental music purposely created to express those emotions. Subjects also rated the arousal and valence of each musical stimulus. An error detection task assessed basic auditory perceptual function. S.M. performed normally in this perceptual task, but was selectively impaired in the recognition of scary and sad music. In contrast, her recognition of happy music was normal. Furthermore, S.M. judged the scary music to be less arousing and the peaceful music less relaxing than did the controls. Overall, the pattern of impairment in S.M. is similar to that previously reported in patients with unilateral anteromedial temporal lobe damage. S.M.'s impaired emotional judgments occur in the face of otherwise intact processing of musical features that are emotionally determinant. The use of tempo and mode cues in distinguishing happy from sad music was also spared in S.M. Thus, the amygdala appears to be necessary for emotional processing of music rather than the perceptual processing itself.

Adult↗

Emotional responses to unpleasant music correlates with damage to the parahippocampal cortex.

Music is typically a pleasurable experience. But under certain circumstances, music can also be unpleasant, for example, when a young child randomly hits piano keys. Such unpleasant musical experiences have been shown to activate a network of brain structures involved in emotion, mostly located in the medial temporal lobe: the parahippocampal gyrus, amygdala, hippocampus and temporal pole. However, the differential roles of these regions remain largely unknown. In this study, pleasant and unpleasant music was presented to 17 patients with variable excisions of the medial temporal lobe, as well as to 19 matched controls. The pleasant music corresponded to happy and sad selections taken from the classical instrumental repertoire; the unpleasant music was the dissonant arrangement of the same selections. Only patients with substantial resections of the left or right parahippocampal cortex (PHC) gave highly abnormal judgements to dissonant music; they rated dissonant music as slightly pleasant while controls found it unpleasant. This indifference to dissonance was correlated with the remaining volume in the PHC, but was unrelated to the volume of the surrounding structures. The impairment was specific: the same patients judged consonant music to be pleasant, and were able to judge music as happy or sad. Furthermore, this lack of responsiveness to unpleasantness was not due to a perceptual disorder, because all patients were able to detect intentional errors in the musical excerpts. Moreover, the impairment differed from that induced by amygdala damage alone. These findings are consistent with a two-dimensional model of defensive responses to aversive stimuli, in which the PHC and the amygdala subserve different roles.

Adult↗

Analysis of face gaze in autism using "Bubbles".

One of the components of abnormal social functioning in autism is an impaired ability to direct eye gaze onto other people's faces in social situations. Here, we investigated the relationship between gaze onto the eye and mouth regions of faces, and the visual information that was present within those regions. We used the "Bubbles" method to vary the facial information available on any given trial by revealing only small parts of the face, and measured the eye movements made as participants viewed these stimuli. Compared to ten IQ- and age-matched healthy controls, eight participants with autism showed less fixation specificity to the eyes and mouth, a greater tendency to saccade away from the eyes when information was present in those regions, and abnormal directionality of saccades. The findings provide novel detail to the abnormal way in which people with autism look at faces, an impairment that likely influences all subsequent face processing.

Adult↗

Emotional arousal in agenesis of the corpus callosum.

While the processing of verbal and psychophysiological indices of emotional arousal have been investigated extensively in relation to the left and right cerebral hemispheres, it remains poorly understood how both hemispheres normally function together to generate emotional responses to stimuli. Drawing on a unique sample of nine high-functioning subjects with complete agenesis of the corpus callosum (AgCC), we investigated this issue using standardized emotional visual stimuli. Compared to healthy controls, subjects with AgCC showed a larger variance in their cognitive ratings of valence and arousal, and an insensitivity to the emotion category of the stimuli, especially for negatively-valenced stimuli, and especially for their arousal. Despite their impaired cognitive ratings of arousal, some subjects with AgCC showed large skin-conductance responses, and in general skin-conductance responses discriminated emotion categories and correlated with stimulus arousal ratings. We suggest that largely intact right hemisphere mechanisms can support psychophysiological emotional responses, but that the lack of interhemispheric communication between the hemispheres, perhaps together with dysfunction of the anterior cingulate cortex, interferes with normal verbal ratings of arousal, a mechanism in line with some models of alexithymia.

Adult↗

How do we know the minds of others? Domain-specificity, simulation, and enactive social cognition.

In what ways, and to what extent, is social cognition distinguished from cognition in general? And how do data from cognitive neuroscience speak to this question? I review recent findings that argue social cognition may indeed be specialized, and at multiple levels. One particularly interesting respect in which social cognition differs from the rest of cognition is in its close interaction with the social environment. We actively probe other people in order to make inferences about what is going on in their minds (e.g., by asking them questions, and directing our gaze onto them), and we use the minds of other people as a collective resource. Experiments from our own laboratory point to the amygdala as one structure that is critically involved in such processes.

Animals↗

Perception of socially relevant stimuli in schizophrenia.

To examine whether patients with schizophrenia have deficits in the appraisal of socially relevant stimuli, we tested 20 patients and 14 healthy volunteers equated for parental socioeconomic status on recognition of gender stimuli, emotional people stimuli, and emotional scenes. Patients with schizophrenia showed deficits in discrimination of subtle gender differences and in the identification of emotion from human shapes and body motion. Patients showed no impairment on measures of hedonic appraisal of emotional scenes and recognition of emotional expression in human face stimuli. Across tasks, subjects with schizophrenia showed poorer identification of happiness, anger, and fear. The findings point towards circumscribed domains of impaired social cognition in schizophrenia and suggest specific further hypotheses about the neural dysfunction that may underlie them.

Adult↗

Cardiovascular and respiratory responses during musical mood induction.

Music is used to induce moods in experimental settings as well as for therapeutic purposes. Prior studies suggest that subjects listening to certain types of music experience strong moods and show physiological responses associated with the induced emotions. We hypothesized that cardiovascular and respiratory patterns could discriminate moods induced via music. 18 healthy subjects listened to 12 music clips, four each to induce happiness, sadness, and fear, while cardiovascular and respiratory responses were recorded using an electrocardiogram and chest strain-gauge belt. After each clip subjects completed a questionnaire. Subjects consistently reported experiencing the targeted mood, suggesting successful mood induction. Cardiovascular activity was measured by calculating time domain measures and heart rate changes during each clip. Respiratory activity was measured by total, inspiration, and expiration lengths as well as changes in mean respiration rate during each clip. Evaluation of individuals' patterns and mixed-model analyses were performed. Contrary to expectations, the time domain measures of subjects' cardiovascular responses did not vary significantly between the induced moods, although a heart rate deceleration was found during the sadness inductions and acceleration during the fear inductions. The time domain respiratory measures varied with clip type: the mean breath length was longest for the sad induction, intermediate during fear, and shortest during the happiness induction. However, analysis using normalized least mean squares adaptive filters to measure time correlation indicated that much of this difference may be attributable to entrainment of respiration to characteristics of the music which varied between the stimuli. Our findings point to the difficulty in detecting psychophysiological correlates of mood induction, and further suggest that part of this difficulty may arise from failure to differentiate it from tempo-related contributions when music is used as the inducer.

Adult↗

The influence of autonomic arousal and semantic relatedness on memory for emotional words.

Increased memory for emotional stimuli is a well-documented phenomenon. Emotional arousal during the encoding of a stimulus is one mediator of this memory enhancement. Other variables such as semantic relatedness also play a role in the enhanced memory for emotional stimuli, especially for verbal stimuli. Research has not addressed the contributions of emotional arousal, indexed by self-report and autonomic measures, and semantic relatedness on memory performance. Twenty young adults (10 women) were presented neutral-unrelated words, school-related words, moderately arousing emotional words, and highly arousing taboo words while heart rate and skin conductance were measured. Memory was tested with free recall and recognition tests. Results showed that taboo words, which were both semantically related and high arousal were remembered best. School-related words, which were high on semantic relatedness but low on arousal, were remembered better than the moderately arousing emotional words and semantically unrelated neutral words. Psychophysiological responses showed that within the moderately arousing emotional and neutral word groups, those words eliciting greater autonomic activity were better remembered than words that did not elicit such activity. These results demonstrate additive effects of semantic relatedness and emotional arousal on memory. Relatedness confers an advantage to memory (as in the school-words), but the combination of relatedness and arousal (as in the taboo words) results in the best memory performance.

Adolescent↗

Role of the amygdala in processing visual social stimuli.

We review the evidence implicating the amygdala as a critical component of a neural network of social cognition, drawing especially on research involving the processing of faces and other visual social stimuli. We argue that, although it is clear that social behavioral representations are not stored in the amygdala, the most parsimonious interpretation of the data is that the amygdala plays a role in guiding social behaviors on the basis of socioenvironmental context. Thus, it appears to be required for normal social cognition. We propose that the amygdala plays this role by attentionally modulating several areas of visual and somatosensory cortex that have been implicated in social cognition, and in helping to direct overt visuospatial attention in face gaze. We also hypothesize that the amygdala exerts attentional modulation of simulation in somatosensory cortices such as supramarginal gyrus and insula. Finally, we argue that the term emotion be broadened to include increased attention to bodily responses and their representation in cortex.

Amygdala↗

Neural systems responding to degrees of uncertainty in human decision-making.

Much is known about how people make decisions under varying levels of probability (risk). Less is known about the neural basis of decision-making when probabilities are uncertain because of missing information (ambiguity). In decision theory, ambiguity about probabilities should not affect choices. Using functional brain imaging, we show that the level of ambiguity in choices correlates positively with activation in the amygdala and orbitofrontal cortex, and negatively with a striatal system. Moreover, striatal activity correlates positively with expected reward. Neurological subjects with orbitofrontal lesions were insensitive to the level of ambiguity and risk in behavioral choices. These data suggest a general neural circuit responding to degrees of uncertainty, contrary to decision theory.

Adult↗

Memories for emotional autobiographical events following unilateral damage to medial temporal lobe.

Abnormalities of both memory and emotion have been reported in patients with unilateral damage to the anteromedial temporal lobe, probably reflecting the functions of the amygdala and hippocampus in these processes. Emotion and memory are also known to interact: emotional experiences often leave remarkably durable autobiographical memories. To explore this interaction, and to extend prior studies to the domain of autobiographical memory, we investigated the recollection of real-life emotional events in patients with unilateral damage to the anteromedial temporal lobe. Twenty-three patients who had undergone unilateral temporal lobectomy for the treatment of epilepsy (12 left, 11 right) and 20 healthy comparison participants completed an emotional autobiographical memory test. Participants were asked to recollect their five most emotional memories from any time in their lives and then they completed a word-cued autobiographical memory task. Participants dated each memory and gave ratings on scales of pleasantness, intensity, significance, novelty, vividness and frequency of rehearsal. Left temporal lobectomy (LTL) and healthy comparison groups generated similar numbers of pleasant and unpleasant memories, whereas the right temporal lobectomy (RTL) group produced significantly fewer memories of unpleasant events (P < 0.01). When memories were further categorized according to pleasantness and intensity, the RTL group produced significantly fewer unpleasant/high intensity memories than the other groups (P < 0.01). All groups reported more memories from between the ages of 10 and 30 (the so-called autobiographical memory 'bump'). The results demonstrate a positive bias in the recollection of autobiographical memory following right-sided anteromedial temporal damage. This finding is consistent with the notion that the right, but not the left, anteromedial temporal lobe is involved in the retrieval of negatively valenced, high-intensity memories.

Adult↗

Electrophysiological correlates of reward prediction error recorded in the human prefrontal cortex.

Lesion and functional imaging studies have shown that the ventromedial prefrontal cortex is critically involved in the avoidance of risky choices. However, detailed descriptions of the mechanisms that underlie the establishment of such behaviors remain elusive, due in part to the spatial and temporal limitations of available research techniques. We investigated this issue by recording directly from prefrontal depth electrodes in a rare neurosurgical patient while he performed the Iowa Gambling Task, and we concurrently measured behavioral, autonomic, and electrophysiological responses. We found a robust alpha-band component of event-related potentials that reflected the mismatch between expected outcomes and actual outcomes in the task, correlating closely with the reward-related error obtained from a reinforcement learning model of the patient's choice behavior. The finding implicates this brain region in the acquisition of choice bias by means of a continuous updating of expectations about reward and punishment.

Choice Behavior↗

Emotional autobiographical memories in amnesic patients with medial temporal lobe damage.

The recollection of emotional autobiographical memories has received little attention in patients with memory disorders. Here, we addressed this topic in amnesic patients with damage to the hippocampus (HC group; n = 8) or the hippocampus, amygdala, and surrounding cortices (HC+ group; n = 2). These patients were asked to recollect emotional events from their lives. HC patients produced recollections that were strikingly similar to those of brain-damaged (n = 10) and healthy (n = 25) comparison participants, in terms of both quantity and quality. In contrast, HC+ patients produced a lower proportion of unpleasant memories compared with the other participants. Specifically, the ratings and words used to describe recollections in the HC+ patients were more affectively positive. All groups produced more memories from between 10 and 30 years of age (the so-called autobiographical memory "bump") compared with other time periods in their lives. These results suggest that structures surrounding the hippocampus, but not the hippocampus itself, may be necessary for the recollection of highly emotional, unpleasant autobiographical memories. The amygdala and surrounding cortices of the medial temporal lobe may be a necessary component in the neural circuitry necessary for vivid recollection of unpleasant emotional events.

Adult↗

Amygdala damage impairs emotional memory for gist but not details of complex stimuli.

Neurobiological studies demonstrate the amygdala's role in emotional memory, and psychological studies suggest a particular pattern: enhanced memory for the gist but not the details of complex stimuli. We hypothesized that these two findings are related. Whereas normal (n = 52) and brain-damaged (n = 22) controls showed the expected enhancement of gist memory when the encoding context was emotional, persons with unilateral damage to the medial temporal lobe including the amygdala (n = 16) did not show this pattern. Furthermore, amygdala volume showed a significant positive correlation with gist memory but not with overall memory. A further study in four subjects with selective medial temporal damage sparing the amygdala, and one with selective damage confined to the amygdala, confirmed the specificity of this effect to the amygdala. The data support a model whereby the amygdala focuses processing resources on gist, possibly accounting for features of traumatic memories and eyewitness testimony in real life.

Adult↗

A mechanism for impaired fear recognition after amygdala damage.

Ten years ago, we reported that SM, a patient with rare bilateral amygdala damage, showed an intriguing impairment in her ability to recognize fear from facial expressions. Since then, the importance of the amygdala in processing information about facial emotions has been borne out by a number of lesion and functional imaging studies. Yet the mechanism by which amygdala damage compromises fear recognition has not been identified. Returning to patient SM, we now show that her impairment stems from an inability to make normal use of information from the eye region of faces when judging emotions, a defect we trace to a lack of spontaneous fixations on the eyes during free viewing of faces. Although SM fails to look normally at the eye region in all facial expressions, her selective impairment in recognizing fear is explained by the fact that the eyes are the most important feature for identifying this emotion. Notably, SM's recognition of fearful faces became entirely normal when she was instructed explicitly to look at the eyes. This finding provides a mechanism to explain the amygdala's role in fear recognition, and points to new approaches for the possible rehabilitation of patients with defective emotion perception.

Adult↗

Preferring one taste over another without recognizing either.

Stimuli can be discriminated without being consciously perceived and can be preferred without being remembered. Here we report a subject with a previously unknown dissociation of abilities: a strong behavioral preference for the taste of sugar over saline, despite a complete failure of recognition. The pattern of brain damage responsible for the dissociation suggests that reliable behavioral choice among tastes can occur in the absence of the gustatory cortex necessary for taste recognition.

Aged↗