Hugo D. Critchley

Beauty in a smile: the role of medial orbitofrontal cortex in facial attractiveness

The attractiveness of a face is a highly salient social signal, influencing mate choice and other social judgements. In this study, we used event-related functional magnetic resonance imaging (fMRI) to investigate brain regions that respond to attractive faces which manifested either a neutral or mildly happy face expression. Attractive faces produced activation of medial orbitofrontal cortex (OFC), a region involved in representing stimulus-reward value. Responses in this region were further enhanced by a smiling facial expression, suggesting that the reward value of an attractive face as indexed by medial OFC activity is modulated by a perceiver directed smile.

Activity in ventromedial prefrontal cortex covaries with sympathetic skin conductance level: a physiological account of a "default mode" of brain function

We examined neural activity related to modulation of skin conductance level (SCL), an index of sympathetic tone, using functional magnetic resonance imaging (fMRI) while subjects performed biofeedback arousal and relaxation tasks. Neural activity within the ventromedial prefrontal cortex (VMPFC) and the orbitofrontal cortex (OFC) covaried with skin conductance level (SCL), irrespective of task. Activity within striate and extrastriate cortices, anterior cingulate and insular cortices, thalamus, hypothalamus and lateral regions of prefrontal cortex reflected the rate of change in electrodermal activity, highlighting areas supporting transient skin conductance responses (SCRs). Successful performance of either biofeedback task (where SCL changed in the intended direction) was associated with enhanced activity in mid-OFC. The findings point to a dissociation between neural systems controlling basal sympathetic tone (SCL) and transient skin conductance responses (SCRs). The level of activity in VMPFC has been related to a default mode of brain function and our findings provide a physiological account of this state, indicating that activity within VMPFC and OFC reflects a dynamic between exteroceptive and interoceptive deployment of attention.

Brain activity relating to the contingent negative variation: an fMRI investigation

The contingent negative variation (CNV) is a long-latency electroencephalography (EEG) surface negative potential with cognitive and motor components, observed during response anticipation. CNV is an index of cortical arousal during orienting and attention, yet its functional neuroanatomical basis is poorly understood. We used functional magnetic resonance imaging (fMRI) with simultaneous EEG and recording of galvanic skin response (GSR) to investigate CNV-related central neural activity and its relationship to peripheral autonomic arousal. In a group analysis, blood oxygenation level dependent (BOLD) activity during the period of CNV generation was enhanced in thalamus, somatomotor cortex, bilateral midcingulate, supplementary motor, and insular cortices. Enhancement of CNV-related activity in anterior and midcingulate, SMA, and insular cortices was associated with decreases in peripheral sympathetic arousal. In a subset of subjects in whom we acquired simultaneous EEG and fMRI data, we observed activity in bilateral thalamus, anterior cingulate, and supplementary motor cortex that was modulated by trial-by-trial amplitude of CNV. These findings provide a likely functional neuroanatomical substrate for the CNV and demonstrate modulation of components of this neural circuitry by peripheral autonomic arousal. Moreover, these data suggest a mechanistic model whereby thalamocortical interactions regulate CNV amplitude.

Neuroanatomical basis for first- and second-order representations of bodily states.

Changes in bodily states, particularly those mediated by the autonomic nervous system, are crucial to ongoing emotional experience. A theoretical model proposes a first-order autoregulatory representation of bodily state at the level of dorsal pons, and a second-order experience-dependent re-mapping of changes in bodily state within structures such as cingulate and medial parietal cortices. We tested these anatomical predictions using positron emission tomography and a human neurological model (pure autonomic failure), in which peripheral autonomic denervation prevents the emergence of autonomic responses. Compared to controls, we observed task-independent differences in activity of dorsal pons and context-induced differences in cingulate and medial parietal activity in PAF patients. An absence of afferent feedback concerning autonomically generated bodily states was associated with subtle impairments of emotional responses in PAF patients. Our findings provide empirical support for a theory proposing a hierarchical representation of bodily states.

Volitional control of autonomic arousal: A functional magnetic resonance study

Electrodermal activity reflects autonomic sympathetic innervation of dermal sweat glands providing an index of emotion-related bodily states of arousal. Relaxation techniques, which are facilitated by external (bio)feedback of electrodermal activity, can be used by trained subjects to actively control bodily and emotional arousal. Biofeedback relaxation provides an experimental model to explore neural mechanisms contributing to emotional representations and intentional autonomic control. We used functional magnetic resonance imaging (fMRI) to explore neural mechanisms contributing to integration of volitional intent, self-representation, and autonomic states of arousal, embodied within performance of a biofeedback relaxation exercise. Data were obtained from 17 subjects to assess brain activity during relaxation in which a visual index of electrodermal arousal was modulated by accuracy (addition of random noise) or sensitivity (by scalar adjustments of feedback). A central matrix of cortical, subcortical and brainstem autonomic centres was activated during biofeedback relaxation, as well as regions that mediate visual and somatesthetic representations and executive control. Anterior cingulate, amygdala, and insula activity was modulated by task manipulations that increased demand on processing interoceptive representations, while variation in anterior insula activity reflected an interaction between accuracy and sensitivity of feedback. These findings identify neural substrates that support integration of perceptual processing, interoception, and intentional modulation of bodily states of arousal.

Brain activity during biofeedback relaxation: a functional neuroimaging investigation

The mechanisms by which cognitive processes influence states of bodily arousal are important for understanding the pathogenesis and maintenance of stress-related morbidity. We used PET to investigate cerebral activity relating to the cognitively driven modulation of sympathetic activity. Subjects were trained to perform a biofeedback relaxation exercise that reflected electrodermal activity and were subsequently scanned performing repetitions of four tasks: biofeedback relaxation, relaxation without biofeedback and two corresponding control conditions in which the subjects were instructed not to relax. Relaxation was associated with significant increases in left anterior cingulate and globus pallidus activity, whereas no significant increases in activity were associated with biofeedback compared with random feedback. The interaction between biofeedback and relaxation, highlighting activity unique to biofeedback relaxation, was associated with enhanced anterior cingulate and cerebellar vermal activity. These data implicate the anterior cingulate cortex in the intentional modulation of bodily arousal and suggest a functional neuroanatomy of how cognitive states are integrated with bodily responses. The findings have potential implications for a mechanistic account of how therapeutic interventions, such as relaxation training in stress-related disorders, mediate their effects.

Social and motivational functioning is not critically dependent on feedback of autonomic responses: neuropsychological evidence from patients with pure autonomic failure

Social, emotional and motivational behaviours are associated with production of automatic bodily responses. Re-representation in the brain through feedback of autonomic and skeletomuscular arousal is proposed to underlie feeling states. These influence emotional judgments and bias motivational decision-making and guide social interactions. Consistent with this hypothesis, dissocial behaviour and deficits on emotional and motivation tasks are associated with blunted bodily responses in patients with orbitofrontal brain lesions or developmental psychopathy. To determine the critical dependence of social and emotional behaviours on bodily responses mediated by the autonomic nervous system, we examined patients with pure autonomic failure (PAF), a peripheral denervation of autonomic neurons with onset in middle age. Compared to healthy subjects, PAF patients were unimpaired on tests of motivational decision-making (Iowa Gambling Task), recognition of emotional facial expressions, Theory of Mind Tasks and tests of social cognition. Only on a test of emotional attribution, which is perhaps more sensitive to subjective feeling states, did PAF patients score worse than the comparison group, though there was no evidence that this deficit was specific to a discrete emotion and requires further validation. These findings suggest that emotional and social functioning is not critically tied to on-going experience of autonomic arousal state, Acquisition of autonomic failure late in life may protect against maladaptive social behaviour through established behavioural responses that may be associated with central as if representations.

Brain mechanisms for mood congruent memory facilitation

Emotional information is better remembered when mood at the time of retrieval matches it in valence (positive mood, positive material). An associative memory model predicts that this mood congruent facilitation is due to the mood-related reactivation at retrieval of emotional responses which were linked to valenced information at encoding. To test this model, we presented subjects with positive and negative words at study and manipulated their mood at test while using functional imaging to monitor brain activity. Subjective mood ratings and heart rate variability both indicated that the manipulation was effective, and memory performance showed a strong trend towards facilitation in congruent conditions. In the functional imaging data, valence-specific conjunctions between encoding activity predicting subsequent memory in a congruent mood and retrieval activity relating to mood congruent recollection revealed shared responses in subgenual cingulate for positive valence and posteriolateral orbitofrontal cortex for negative valence, thus supporting the associative model. To elucidate the mnemonic basis of facilitation, independent of valence, we examined the shared correlates of positive and negative congruence and found that parts of the episodic memory system were activated by congruence in correct rejection trials, but no part of this system was activated by congruence in correctly remembered trials. This pattern suggests that mood congruent facilitation occurs at the level of attempted recall rather than that of successful recollection.

Intuitive interference in quantitative reasoning

It is well known that surface features of a task can queue multiple reasoning strategies. Interference or conflict among the strategies is signaled by increasing reaction times and error rates. To determine the neural basis of this interference, we studied 14 volunteers using event-related fMRI, as they compared the perimeters of geometrical shapes in congruent (where the shapes perimeter changed in the same direction as its area) and incongruent (where the shapes perimeter was conserved but its area changed) conditions. We found evidence for the engagement of bilateral parietal lobe systems during congruent trials and incorrect incongruent trials. Activation of bilateral orbital frontal cortex was evident when subjects inhibited interference associated with processing the salient feature area and correctly completed the perimeters in the incongruent condition. Varying the level of interference exerted by the unattended feature area (filled vs. unfilled shapes) affected the relative level of activation of right parietal regions but not orbital frontal cortex suggesting that the former is responding to the degree of facilitation while the latter is responsive to the presence of conflict (rather than the degree of conflict).