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Processing facial emotions in adults with velo-cardio-facial syndrome: functional magnetic resonance imaging

Department of Psychological Medicine, Institute of Psychiatry, London, UK and Department of Psychiatry, Academic Medical Centre, Amsterdam, The Netherlands

NICOLE SCHMITZ, PhD

Department of Psychological Medicine, Institute of Psychiatry, London, and Department of Radiology, Leiden University Medical Centre, The Netherlands

EILEEN DALY, BSc and QUINTON DEELEY, MRCPsych

Department of Psychological Medicine, Institute of Psychiatry, London

HUGO CRITCHLEY, MRCPsych, DPhil

Functional Imaging Laboratory, Institute of Neurology, London

JAYNE HENRY, DPsych and DENE ROBERTSON, MRCPsych

Department of Psychological Medicine, Institute of Psychiatry, London

MICHAEL OWEN, FRCPsych, PhD

Department of Psychological Medicine,University of Cardiff, UK

KIERAN C. MURPHY, MRCPsych, PhD

Department of Psychiatry, Royal College of Surgeons, Dublin, Ireland

DECLAN G. MURPHY, MRCPsych, MD

Department of Psychological Medicine, Institute of Psychiatry, London.

Correspondence: Therese van Amelsvoort, Department of Psychiatry, Academic Medical Centre, Amsterdam, The Netherlands. Email: t.a.vanamelsvoort{at}amc.uva.nl

Declaration of interest None. The study was part funded by the Stanley Foundation and the Medical Research Council.

	ABSTRACT

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We studied the functional neuroanatomy of social behaviour in velo-cardio-facial syndrome (VCFS) using a facial emotional processing task and functional magnetic resonance imaging in adults with this syndrome and controls matched for age and IQ. The VCFS group had less activation in the right insula and frontal brain regions and more activation in occipital regions. Genetically determined abnormalities in pathways including those involved in emotional processing may underlie deficitsin social cognition in people with VCFS.

	INTRODUCTION

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Velo-cardio-facial syndrome (VCFS) is associated with intellectual impairments and with IQ-independent deficits in visuoperceptual function and social and abstract reasoning (Henry et al, 2002). These deficits may underlie the social impairments of VCFS (Swillen et al, 1997). Facial expressions are important social cues. As explicit processing of facial emotions is positively correlated with IQ and involves higher cognitive processes (Kroeger et al, 2001), we used functional magnetic resonance imaging (fMRI) to investigate implicit processing, which involves (para)limbic areas in an automatic, attention-independent manner (Critchley et al, 2000). We predicted that compared with controls, people with VCFS have less activation of brain regions normally activated during implicit emotional processing (the amygdala, insula and frontal cortex).

	METHOD

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Our sample included eight right-handed adults – seven women and one man (mean age 34 years, s.d.=9; mean IQ 72, s.d.=10), three of whom had schizophrenia and five had no mental illness – with clinical features of VCFS and a 22q11 deletion confirmed by fluorescence in situ hybridisation (Oncor Inc., Gaithersburg, Maryland, USA). Our control group comprised nine healthy individuals (five women and four men; mean age 37 years, s.d.=11, mean IQ 73, s.d.=16). Details of inclusion criteria, recruitment methods and psychiatric and neuropsychological assessments are described elsewhere (Murphy et al, 1999; van Amelsvoort et al, 2004). The control group did not differ significantly in age, IQ and gender from the VCFS group. The study was approved by the local research ethics committee. Written informed consent was obtained from all participants (or their guardians).

All participants were familiarised with the scanner and the task. Ten blocks of eight facial stimuli from the Ekman series (Ekman & Friesen, 1975) were used, as described previously by Critchley et al (2000). The participants viewed a pseudo-randomised mixture of happy or angry (‘on’ phase) and neutral (‘off’ phase) facial expressions, with instructions to attend to and judge the gender of each face. During this task 100 T₂*-weighted echoplanar images, depicting blood oxygenation level-dependent contrast (14 non-continuous slices, thickness 7 mm (gap 0.7 mm), inplane resolution 3.1 mm, echo time (TE) 40 ms, repetition time (TR) 3000 ms), and one T₁-weighted whole-brain anatomical image (43 continuous slices, thickness 3 mm, in-plane resolution 1.5 mm, TE=73 ms, TR=1600 ms) were acquired using a 1.5 T GE Signa System 7(General Electric, Milwaukee, Wisconsin, USA). Data were analysed using Statistical Parametric Mapping 99 (http://www.fil.ion.ucl.ac.uk/spm). Functional images were movement corrected, normalised into standard space and smoothed with 12 mm full width at half maximum gaussian kernel prior to statistical comparisons. Condition-specific task effects were assessed by comparing the ‘on’ phases of each task with their respective ‘off’ condition. Changes in regional blood flow were determined by applying the general linear model. Between-group comparisons of brain activation patterns were performed using t statistics. The resulting statistical parametric (SPM (t)) maps were transformed to SPM {Z} values.

	RESULTS

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Participants were task-compliant, and debriefed after scanning. Responses were made in the required time window, and there was no group difference in task performance. Between-group analysis revealed an anterior–posterior dichotomy in activation patterns during emotional processing (on>off). Compared with the control group, the VCFS group showed less activity in the right insula and frontal regions. In contrast, people with VCFS had more activity in bilateral occipital regions (Table 1).

	DISCUSSION

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To our knowledge this is the first fMRI study investigating facial emotional processing in VCFS. Compared with controls, people with VCFS had more activation of the bilateral occipital brain regions involved in early visual processing (including face perception) (Haxby et al, 2002). In contrast, people with VCFS showed less activation in the right insula and premotor cortex – areas implicated in emotional processing (Critchley et al, 2000; Haxby et al, 2002).

The neural network mediating face perception includes a ‘core system’ for visual face analysis, in which occipital gyri provide input into fusiform and superior temporal regions. These then interact with an extended system (e.g. amygdala, insula, limbic system) to process the meaning of information (including emotions) from faces (Haxby et al, 2002). Ventral stream disruption could be one explanation for social impairments in VCFS (Lajiness-O’Neill et al, 2005). Moreover, adults with VCFS perform poorly on object perception tasks (relying on the ventral ‘what’ pathway), whereas they perform better on space perception tasks (relying on the dorsal ‘where’ pathway) (Henry et al, 2002). Our results suggest that in VCFS the pathways between ‘face perception’ areas and the extended ventral ‘what’ pathway for processing emotional expressions may be dysfunctional.

A consistent finding in face expression neuroimaging research is increased extrastriate activation in association with facial emotional expressions. Hence, our results may also reflect greater modulation of visual cortices by emotional faces in VCFS compared with controls, with downstream areas involved in attributing the social significance of faces being hypoactive. Hence, people with VCFS may show normal or enhanced affective responses to facial expressions (intact affective empathy), but an impaired ability to identify the social and contextual significance of socioemotional cues (impaired cognitive empathy). This could partially explain why people with VCFS have high levels of anxiety and affective symptoms.

In our between-group analysis, we observed an anterior–posterior dichotomy in brain activation patterns. This dichotomy has been reported previously in anatomical studies of VCFS (Kates et al, 2001) and might be partially explained by dysmaturation of white-matter tracts in this syndrome (van Amelsvoort et al, 2004). White-matter integrity is associated with better performance on cognitive tasks; for example, improvement in working memory is associated with increased frontal fractional anisotropy (Nagy et al, 2004). Thus, people with VCFS may need to activate occipital brain regions more in order to process visual stimuli, owing to reduced white-matter integrity or connectivity. This ‘compensation’ hypothesis is supported by the findings of Eliez et al (2001), who reported increased activation in parietal regions of children with VCFS compared with controls during mathematical reasoning.

Limitations of our study include the use of a block design including both ‘happy’ and ‘angry’ faces; we are therefore unable to comment on brain activations to separate emotions or neutral faces. Event-related fMRI is needed to evaluate this. Our results did not survive correction for multiple comparisons and should be interpreted as preliminary. Men and women were included in the study, but there was no difference in gender distribution. Inclusion in the VCFS group of three people receiving medication for psychosis could have confounded our results. Given the high prevalence of psychiatric disorders in VCFS, however, a population without any psychiatric problem is rare.

In summary, the results of our preliminary study of emotional processing in VCFS suggest that social impairments in this syndrome may be associated with abnormal connectivity between early visual processing areas and limbic brain regions.

	REFERENCES

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Critchley, H., Daly, E., Phillips, M., et al (2000) Explicit and implicit neural mechanisms for processing of social information from facial expressions: a functional magnetic resonance imaging study. Human Brain Mapping, 9, 93 –105.[CrossRef][Medline]

Ekman, P. & Friesen, W. (1975) Pictures of Facial Affect. Palo Alto, CA: Consulting Psychologists Press.

Eliez, S., Blasey, C. M., Menon, V., et al (2001) Functional brain imaging study of mathematical reasoning abilities in velocardiofacial syndrome. Genetics in Medicine, 3, 49 –55.[Medline]

Haxby, J. V., Hoffman, E. A. & Gobbini, M. I. (2002) Human neural systems for face recognition and social communication. Biological Psychiatry, 51, 59 –67.[CrossRef][Medline]

Henry, J., van Amelsvoort, T., Morris, R., et al (2002) An investigation of the neuropsychological profile in adults with velo-cardio-facial syndrome (VCFS). Neuropsychologia, 40, 471 –478.[CrossRef][Medline]

Kates, W., Burnette, C., Jabs, E., et al (2001) Regional cortical white matter reductions in velocardiofacial syndrome: a volumetric MRI analysis. Biological Psychiatry, 49, 677 –684.[CrossRef][Medline]

Kroeger, T. L., Rojahn, J. & Naglieri, J. A. (2001) Role of planning, attention, and simultaneous and successive cognitive processing in facial recognition in adults with mental retardation. American Journal of Mental Retardation, 106, 151 –161.

Lajiness-O’Neill, R. R., Beaulieu, I., Titus, J. B., et al (2005) Memory and learning in children with 22q11.2 deletion syndrome: evidence for ventral and dorsal stream disruption? Child Neuropsychology, 11, 55 –71.[Medline]

Murphy, K. C., Jones, L. A. & Owen, M. J. (1999) High rates of schizophrenia in adults with velo-cardio-facial syndrome. Archives of General Psychiatry, 56, 940 –945.[Abstract/Free Full Text]

Nagy, Z., Westerberg, H. & Klingberg, T. (2004) Maturation of white matter is associated with the development of cognitive functions during childhood. Journal of Cognitive Neuroscience, 16, 1227 –1233.[Abstract/Free Full Text]

Swillen, A., Devriendt, K., Legius, E., et al (1997) Intelligence and psychosocial adjustment in velocardiofacial syndrome: a study of 37 children and adolescents with VCFS. Journal of Medical Genetics, 34, 453 –458.[Abstract]

Van Amelsvoort, T., Daly, E., Henry, J., et al (2004) Brain anatomy in adults with velo-cardio-facial syndrome with and without schizophrenia: preliminary results of a structural magnetic resonance imaging study. Archives of General Psychiatry, 61, 1085 –1096.[Abstract/Free Full Text]

Received for publication November 23, 2005. Revision received June 19, 2006. Accepted for publication July 4, 2006.

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