Brain Advance Access originally published online on June 9, 2005
Brain 2005 128(9):2084-2096; doi:10.1093/brain/awh562
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Functional dissociation of amygdala-modulated arousal and cognitive appraisal, in Turner syndrome
1 Behavioural and Brain Sciences Unit, Institute of Child Health, 30 Guilford Street, London WC1N 1EH, UK and 2 Wellcome Department of Imaging Neuroscience, Institute of Neurology, 12 Queen Square, London WC1N 3BG, UK
Correspondence to: Prof. David Skuse E-mail: dskuse{at}ich.ucl.ac.uk
The amygdala is preferentially activated by facial expressions of fear. Right and left amygdala are hypothesized to play distinct, but complementary, roles that influence somatic and cognitive responses to facial expressions. Right amygdala activation is linked to autonomic arousal, and thus indirectly influences left hemisphere cognitive processing centres. Left amygdala activation is more closely associated with cognitive processing and differentiation of facial emotions. A double-dissociation between the functions of left and right amygdala is implied by lesion studies but supportive evidence is inconsistent, partly because patients with structural anteromedial temporal anomalies have experienced variable surgical procedures. A functional dissociation can be demonstrated between arousal and the cognitive appraisal of fearful faces in the condition of X-monosomy or Turner syndrome. Previous research found Turner syndrome women of normal verbal intelligence are seriously impaired in their ability cognitively to differentiate fearful from other facial expressions but they acquire fear conditioning normally, with enhanced autonomic responses. These findings supported the dissociation hypothesis, which was formally tested in a study of 12 X-monosomic and 12 control females who participated in functional magnetic resonance imaging during which simultaneous skin conductance recordings were acquired. Faces depicting fear or neutral emotions were presented to both case and control subjects in random order. Arousal to (fearful–neutral) faces was associated with transiently increased skin conductance responses and bilateral amygdala activation in both groups, but X-monosomic females had proportionately greater—and more persistent—right amygdala activation than controls. In both groups, cognitive accuracy correlated positively with differential activity of left fusiform gyrus. There was a significant correlation between the left fusiform and left medial amygdala activation only in normal females, and only in them did differential SCRs (to fearful–neutral faces) correlate positively with left fusiform responses. Arousal and cognitive appraisal functions of the amygdala can thus be functionally dissociated. X-monosomy selectively impairs explicit recognition of fearful faces in the presence of normal or enhanced autonomic reactivity, and is associated with a functional dissociation of activity in left amygdala and left fusiform gyrus. These findings imply X-linked genes are essential for binding somatic responses to the cognitive appraisal of emotional stimuli.
Key Words: amygdala; functional neuroimaging; social cognition; Turner syndrome
Abbreviations: BOLD = blood oxygen level depletion; fMRI = functional magnetic resonance imaging; IQ = intelligence quotient; SCR = skin conductance response
Received November 18, 2004. Revised April 19, 2005. Accepted April 26, 2005.
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