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Enhanced Salience and Emotion Recognition in Autism: A PET Study
Geoffrey B.C. Hall, Ph.D.; Henry Szechtman, Ph.D.; Claude Nahmias, Ph.D.
Am J Psychiatry 2003;160:1439-1441. doi:10.1176/appi.ajp.160.8.1439

Abstract

OBJECTIVE: This study examined neural activation of facial stimuli in autism when the salience of emotional cues was increased by prosodic information. METHOD: Regional cerebral blood flow (rCBF) was measured while eight high-functioning men with autism and eight men without autism performed an emotion-recognition task in which facial emotion stimuli were matched with prosodic voices and a baseline gender-recognition task. RESULTS: Emotion processing in autistic subjects, compared to that in comparison subjects, resulted in lower rCBF in the inferior frontal and fusiform areas and higher rCBF in the right anterior temporal pole, the anterior cingulate, and the thalamus. CONCLUSIONS: Even with the enhanced emotional salience of facial stimuli, adults with autism showed lower activity in the fusiform cortex and differed from the comparison subjects in activation of other brain regions. The authors suggested that the recognition of emotion by adults with autism is achieved through recruitment of brain regions concerned with allocation of attention, sensory gating, the referencing of perceptual knowledge, and categorization.

Abstract Teaser
Figures in this Article

Individuals with autism are notably deficient in both the recognition of emotional prosody (1) and the perception of facial emotion (2). Seemingly to compensate for these deficits, individuals with autism use effortful cognitive strategies based on learned associations and prototypical references to label emotional expressions (3). Preferentially, they tend to categorize facial stimuli with reference to some nonsocial dimension rather than according to emotional content (2). Thus, the social relevance and communicative value of emotional faces seem to be less salient stimuli for individuals with autism than for individuals without autism.

Investigations of facial emotion processing in autism with functional imaging techniques have revealed that in addition to lower activation of the fusiform gyrus, an area of the brain associated with the processing of faces, there are further absences or reductions in activation noted in limbic and paralimbic regions of the brain in individuals with autism (4, 5). The latter regions function not only in the attachment of emotional significance to sensory experiences but also in the reception of emotionally arousing sensory stimuli through extensive reciprocal connections with sensory association cortices (6). Thus, lessened fusiform activation identified during emotion processing (4) may reflect a failure of emotional facial stimuli to acquire motivational or emotional significance. Therefore, the present study examined whether attenuation in neural activation to facial stimuli is present in subjects with autism when the salience of emotional cues is increased and additional prosodic information is provided.

Eight men with autism (ages 20–33 years) and eight male comparison subjects of similar ages gave informed written consent to participate in this study, as approved by the ethics committee of McMaster University. Participants with autism had a DSM-IV diagnosis of autism (N=6) or Asperger’s syndrome (N=2), and neither they nor their parents or guardians reported any comorbid neurological or psychiatric disorders, drug or alcohol abuse, or history of head injury or seizures. The comparison subjects did not endorse drug or alcohol abuse or report neurological or psychiatric disorders, a history of head injury, or a familial history of autism. All subjects were assessed as right-handed (7); nonverbal IQs (8) were similar for participants with autism (mean=105, SD=18, range=80–130) and comparison subjects (mean=109, SD=16, range=90–135) (t=0.46, df=14, p>0.70).

Regional cerebral blood flow (rCBF) was measured during the performance of two task conditions: an emotion-recognition task and a gender-recognition baseline task, with each condition repeated four times (ABABABAB or BABABABA), with one-half of the subjects receiving each letter order. During both conditions, the subjects were administered a series of 36 trials in which the sound of a prosodic voice was presented concurrently with an image of a pair of facial stimuli. Facial images were displayed for 3.4 seconds and preceded by a 0.2-second fixation point. In the emotion-recognition condition, the subjects matched the emotional quality of the voice with the corresponding facial emotion by pressing the appropriate left- or right-hand response button. The emotions were never labeled for the subjects by the experimenter. The gender-recognition condition required that the subjects match the gender of a neutrally prosodic voice to the face of the appropriate gender. Visual and auditory stimuli were presented automatically by a computer, which also recorded response choices and latencies. Between scans, the subjects viewed 7–10 minutes of a videotaped program from a preselected menu of public television documentaries; the available choice of films did not include subject matter that was of strong interest for the participants with autism. The computer screen remained blank for 1 minute before each test condition began. Before the study, the subjects received up to 12 practice trials, and all demonstrated six successive correct responses on each task.

Facial stimuli were constructed by using standardized pictures conveying the emotions happy, sad, surprised, or angry (9, 10). Each image was bound by a frame and masked by an oval so that just the face was visible. Pairs of facial stimuli were generated from a set of 44 distinct male and female faces and were presented on a video monitor at a viewing distance of 40–50 cm. As in the study by Anderson and Phelps (11), auditory stimuli were constructed from recordings made by professional actors (three of each sex), who repeated a series of proper names in voices that conveyed the emotions happy, sad, surprised, and angry or that were neutral in tone. Forty-eight neutral and 48 prosodic distinct voice recordings were edited for consistent quality and equal volume.

rCBF was measured by using an ECAT 953/31 tomograph (CTI PET Systems, Knoxville, Tenn.). Before each scan, 466 MBq of H2[15O] was injected into an intravenous line and flushed with normal saline solution. Scan frames 3 to 5 were summed and reconstructed with filtered back-projection (Hann filter: cutoff frequency=0.3) to yield one image per scan, corrected for attenuation and analyzed in SPM 99 (12). To identify brain regions activated by each group during emotion processing, a multisubject repeated-measures design was used in which rCBF during emotion recognition was contrasted with rCBF during gender recognition (threshold=p<0.001, uncorrected). To identify brain regions that distinguished participants with autism from comparison subjects during emotion processing, a between-group random-effects analysis (threshold=p<0.001, uncorrected) was performed, as described by Woods (13).

Response latency and error measures showed that the participants with autism performed as well as the comparison subjects on the gender-recognition task; they responded as quickly but made significantly more errors than the comparison subjects during the emotion-recognition task (data not shown).

Between-group comparisons (t1) revealed that the recognition of emotion by the participants with autism produced significantly more activation than that of the comparison subjects in the right anterior temporal pole, the left anterior cingulate, and the right thalamus. The recognition of emotions produced significantly greater activation in the comparison subjects than in the participants with autism in the right fusiform gyrus, the left lingual gyrus, and the left inferior frontal cortex.

Regions of activation that relate to the processing of emotion, relative to baseline gender recognition, are shown in the within-group results (t1) and include regions not identified by the between-group analysis, such as the bilateral anterior temporal pole activation in the participants with autism.

The present paradigm is relatively novel in its use of a cross-modal (visual and auditory) task to amplify the cortical response to facial emotional stimuli (14). We found that when the emotional salience of facial stimuli was enhanced by the availability of prosodic information, adults with autism showed not only diminished activity in the right fusiform region, as observed previously (4, 15), but also reduced inferior frontal activation. These results suggest that when recognizing emotion, high-functioning adults with autism place less processing emphasis on the extraction of facial information and the assembly and evaluation of an integrated emotional experience than do subjects without autism.

Instead, with emotion processing, our adults with autism showed greater activation than the comparison subjects in the thalamus, the anterior cingulate gyrus, and the right anterior temporal pole. Greater thalamic activation appears consistent with the suggestion that individuals with autism process facial stimuli through a selective analysis of features rather than holistically (16). Conceivably, within the present context, the processing of faces along multiple select channels necessitates greater sensory modulation by the thalamus. The greater anterior cingulate activation observed for our participants with autism was localized to a region functionally associated with both allocation of attention to features of the sensory environment (17) and direction of attention to a single modality under competing conditions of cross-modal stimuli (18). Thus, in addition to placing greater demands for attention on our participants with autism than on our comparison subjects, the cross-modal emotional stimuli may have been processed as competing rather than complementary sensory experiences. Finally, in light of functional imaging research regarding categorization (19), greater activation of the right anterior temporal pole in the adults with autism than in the comparison subjects may suggest that they accessed categorical perceptual knowledge to guide their decisions about emotional stimuli. Thus, the difficulties that individuals with autism experience in recognizing and understanding emotions may in part be due to their reliance on prototypical representations of emotions and use of categorical knowledge to solve novel problems of emotional experiences.

Although preliminary, these results suggest that emotion processing in autism fails to engage the limbic emotion system and instead is achieved in a feature-selective manner that places large demands on attention processes and draws on categorical knowledge to interpret emotional signals.

 

Received June 24, 2002; revision received Feb. 10, 2003; accepted Feb. 26, 2003. From the Brain-Body Institute, St. Joseph’s Healthcare Hamilton; and the Department of Psychiatry and Behavioural Neurosciences, McMaster University, Hamilton, Ontario, Canada. Address reprint requests to Dr. Hall, Brain-Body Institute, 314 Martha Wing, St. Joseph’s Healthcare Hamilton, 50 Charlton Ave. East, Hamilton, Ontario, Canada L8N 4A6; hallg@mcmaster.ca (e-mail). Dr. Szechtman is a Senior Research Fellow at the Ontario Mental Health Foundation. The authors thank Dr. Raman Chikaral for the radioisotopes, Ms. Margo Thompson for assistance in conducting the PET sessions, Dr. Bob Sainsbury for the visual facial stimuli, Dr. Geoff Coates and the Department of Nuclear Medicine at Hamilton Health Sciences Center for use of its facilities, and the study participants for their help.

VanLancker D, Cornelius C, Kreiman J: Recognition of emotion-prosodic meanings in speech by autistic, schizophrenic, and normal children. Dev Neuropsychol  1989; 5:207–226
[CrossRef]
 
Weeks SJ, Hobson RP: The salience of facial expression for autistic children. J Child Psychol Psychiatry  1987; 28:137–151
[PubMed]
[CrossRef]
 
Capps L, Yirmiya N, Sigman M: Understanding of simple and complex emotions in non-retarded children with autism. J Child Psychol Psychiatry  1992; 33:1169–1182
[PubMed]
[CrossRef]
 
Critchley HD, Daly EM, Bullmore ET, Williams SC, Van Amelsvoort T, Robertson DM, Rowe A, Phillips M, McAlonan G, Howlin P, Murphy DG: The functional neuroanatomy of social behaviour: changes in cerebral blood flow when people with autistic disorder process facial expressions. Brain 2000; 123(part 11):2203–  2212
 
Baron-Cohen S, Ring HA, Wheelwright S, Bullmore ET, Brammer MJ, Simmons A, Williams SC: Social intelligence in the normal and autistic brain: an fMRI study. Eur J Neurosci  1999; 11:1891–1898
[PubMed]
[CrossRef]
 
Dubois S, Rossion B, Schiltz C, Bodart JM, Michel C, Bruyer R, Crommelinck M: Effect of familiarity on the processing of human faces. Neuroimage  1999; 9:278–289
[PubMed]
[CrossRef]
 
Oldfield RC: The assessment and analysis of handedness: the Edinburgh Inventory. Neuropsychologia  1971; 9:97–113
[PubMed]
[CrossRef]
 
Brown L, Sherbenou RJ, Johnsen SK: Test of Nonverbal Intelligence, 2nd ed. Austin, Tex, Pro-Ed, 1990
 
Ekman P, Friesen WV: Pictures of Facial Affect. Palo Alto, Calif, Consulting Psychologists Press, 1976
 
Sainsbury-Butler Facial Recognition Test. Calgary, Alberta, Canada, University of Calgary, Department of Psychology, 1992
 
Anderson AK, Phelps EA: Intact recognition of vocal expressions of fear following bilateral lesions of the human amygdala. Neuroreport  1998; 9:3607–3613
[PubMed]
 
SPM 99. London, University College, Institute of Neurology, Wellcome Department of Cognitive Neurology, 1999
 
Woods RP: Modeling for intergroup comparisons of imaging data. Neuroimage 1996; 4:S84-S94
 
Calvert GA, Brammer MJ, Bullmore ET, Campbell R, Iversen SD, David AS: Response amplification in sensory-specific cortices during crossmodal binding. Neuroreport  1999; 10:2619–2623
[PubMed]
[CrossRef]
 
Schultz RT, Gauthier I, Klin A, Fulbright RK, Anderson AW, Volkmar F, Skudlarski P, Lacadie C, Cohen DJ, Gore JC: Abnormal ventral temporal cortical activity during face discrimination among individuals with autism and Asperger syndrome. Arch Gen Psychiatry  2000; 57:331–340
[PubMed]
[CrossRef]
 
Hobson RP, Ouston J, Lee A: What’s in a face? the case of autism. Br J Psychol 1988; 79(part 4):441–453
 
Devinsky O, Morrell MJ, Vogt BA: Contributions of anterior cingulate cortex to behaviour. Brain 1995; 118(part 1):279–306
 
Calvert GA, Campbell R, Brammer MJ: Evidence from magnetic resonance imaging of crossmodal binding in human heteromodal cortex. Curr Biol  2000; 10:649–657
[PubMed]
[CrossRef]
 
Moore CJ, Price CJ: A functional neuroimaging study of the variables that generate category-specific object processing differences. Brain 1999; 122(part 5):943–962
 
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References

VanLancker D, Cornelius C, Kreiman J: Recognition of emotion-prosodic meanings in speech by autistic, schizophrenic, and normal children. Dev Neuropsychol  1989; 5:207–226
[CrossRef]
 
Weeks SJ, Hobson RP: The salience of facial expression for autistic children. J Child Psychol Psychiatry  1987; 28:137–151
[PubMed]
[CrossRef]
 
Capps L, Yirmiya N, Sigman M: Understanding of simple and complex emotions in non-retarded children with autism. J Child Psychol Psychiatry  1992; 33:1169–1182
[PubMed]
[CrossRef]
 
Critchley HD, Daly EM, Bullmore ET, Williams SC, Van Amelsvoort T, Robertson DM, Rowe A, Phillips M, McAlonan G, Howlin P, Murphy DG: The functional neuroanatomy of social behaviour: changes in cerebral blood flow when people with autistic disorder process facial expressions. Brain 2000; 123(part 11):2203–  2212
 
Baron-Cohen S, Ring HA, Wheelwright S, Bullmore ET, Brammer MJ, Simmons A, Williams SC: Social intelligence in the normal and autistic brain: an fMRI study. Eur J Neurosci  1999; 11:1891–1898
[PubMed]
[CrossRef]
 
Dubois S, Rossion B, Schiltz C, Bodart JM, Michel C, Bruyer R, Crommelinck M: Effect of familiarity on the processing of human faces. Neuroimage  1999; 9:278–289
[PubMed]
[CrossRef]
 
Oldfield RC: The assessment and analysis of handedness: the Edinburgh Inventory. Neuropsychologia  1971; 9:97–113
[PubMed]
[CrossRef]
 
Brown L, Sherbenou RJ, Johnsen SK: Test of Nonverbal Intelligence, 2nd ed. Austin, Tex, Pro-Ed, 1990
 
Ekman P, Friesen WV: Pictures of Facial Affect. Palo Alto, Calif, Consulting Psychologists Press, 1976
 
Sainsbury-Butler Facial Recognition Test. Calgary, Alberta, Canada, University of Calgary, Department of Psychology, 1992
 
Anderson AK, Phelps EA: Intact recognition of vocal expressions of fear following bilateral lesions of the human amygdala. Neuroreport  1998; 9:3607–3613
[PubMed]
 
SPM 99. London, University College, Institute of Neurology, Wellcome Department of Cognitive Neurology, 1999
 
Woods RP: Modeling for intergroup comparisons of imaging data. Neuroimage 1996; 4:S84-S94
 
Calvert GA, Brammer MJ, Bullmore ET, Campbell R, Iversen SD, David AS: Response amplification in sensory-specific cortices during crossmodal binding. Neuroreport  1999; 10:2619–2623
[PubMed]
[CrossRef]
 
Schultz RT, Gauthier I, Klin A, Fulbright RK, Anderson AW, Volkmar F, Skudlarski P, Lacadie C, Cohen DJ, Gore JC: Abnormal ventral temporal cortical activity during face discrimination among individuals with autism and Asperger syndrome. Arch Gen Psychiatry  2000; 57:331–340
[PubMed]
[CrossRef]
 
Hobson RP, Ouston J, Lee A: What’s in a face? the case of autism. Br J Psychol 1988; 79(part 4):441–453
 
Devinsky O, Morrell MJ, Vogt BA: Contributions of anterior cingulate cortex to behaviour. Brain 1995; 118(part 1):279–306
 
Calvert GA, Campbell R, Brammer MJ: Evidence from magnetic resonance imaging of crossmodal binding in human heteromodal cortex. Curr Biol  2000; 10:649–657
[PubMed]
[CrossRef]
 
Moore CJ, Price CJ: A functional neuroimaging study of the variables that generate category-specific object processing differences. Brain 1999; 122(part 5):943–962
 
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