A multimodal investigation of dynamic face perception using functional magnetic resonance imaging and magnetoencephalography

Motion is an important aspect of face perception that has been largely neglected to date. Many of the established findings are based on studies that use static facial images, which do not reflect the unique temporal dynamics available from seeing a moving face. In the present thesis a set of naturalistic dynamic facial emotional expressions was purposely created and used to investigate the neural structures involved in the perception of dynamic facial expressions of emotion, with both functional Magnetic Resonance Imaging (fMRI) and Magnetoencephalography (MEG). Through fMRI and connectivity analysis, a dynamic face perception network was identified, which is demonstrated to extend the distributed neural system for face perception (Haxby et al.,2000). Measures of effective connectivity between these regions revealed that dynamic facial stimuli were associated with specific increases in connectivity between early visual regions, such as inferior occipital gyri and superior temporal sulci, along with coupling between superior temporal sulci and amygdalae, as well as with inferior frontal gyri. MEG and Synthetic Aperture Magnetometry (SAM) were used to examine the spatiotemporal profile of neurophysiological activity within this dynamic face perception network. SAM analysis revealed a number of regions showing differential activation to dynamic versus static faces in the distributed face network, characterised by decreases in cortical oscillatory power in the beta band, which were spatially coincident with those regions that were previously identified with fMRI. These findings support the presence of a distributed network of cortical regions that mediate the perception of dynamic facial expressions, with the fMRI data providing information on the spatial co-ordinates paralleled by the MEG data, which indicate the temporal dynamics within this network. This integrated multimodal approach offers both excellent spatial and temporal resolution, thereby providing an opportunity to explore dynamic brain activity and connectivity during face processing.

Are faces special? A case of pure prosopagnosia

The ability to recognize individual faces is of crucial social importance for humans and evolutionarily necessary for survival. Consequently, faces may be “special” stimuli, for which we have developed unique modular perceptual and recognition processes. Some of the strongest evidence for face processing being modular comes from cases of prosopagnosia, where patients are unable to recognize faces whilst retaining the ability to recognize other objects. Here we present the case of an acquired prosopagnosic whose poor recognition was linked to a perceptual impairment in face processing. Despite this, she had intact object recognition, even at a subordinate level. She also showed a normal ability to learn and to generalize learning of nonfacial exemplars differing in the nature and arrangement of their parts, along with impaired learning and generalization of facial exemplars. The case provides evidence for modular perceptual processes for faces.

Changing faces

News & Comment. Many influential models of prefrontal cortex function suggest that activity within this area is often associated with additional activity in posterior regions of the cortex that support perception. The purpose of this cortical ‘coupling’ is to ensure that a perceptual representation is generated and then maintained within the working memory system. Areas in the right ventrolateral prefrontal cortex (vlPFC) and the fusiform gyrus have been implicated as associate areas involved in face processing. In an interesting case study by Vignal, Chauvel and Halgren the functional relationship between these two areas was tested1. In order to confirm the epileptogenic foci prior to resective surgery in a 30-year-old male patient, depth electrodes were implanted into sites around prefrontal, anterior temporal and premotor cortices. While the patient was looking at a blank screen, 50-Hz electrical stimulation of two probes implanted into the right anterior frontal gyrus resulted in the patient’s reporting the perception of a series of colourful faces. These facial hallucinations were described as being ‘…like passing slides, one after the after, linked together’. When asked to look at an actual face during stimulation at the same sites the patient reported transformation of that face (such as appearing without spectacles or with a hat). These findings were related to activity of a cortical network involving the vlPFC and the fusiform gyrus. This paper thus suggests a role in face processing for the vlPFC, evoking working memory processes to maintain facial representations.

The impact of the CACNA1C gene polymorphism on frontolimbic function in bipolar disorder

Genome-wide association studies in bipolar disorder (BD)1 have implicated a single-nucleotide polymorphism (rs1006737, G right arrow A) in the CACNA1C gene, which encodes for the alpha 1c (CAV1.2) subunit of the voltage-gated, L-type calcium channel. Neuroimaging studies of healthy individuals report that this risk allele modulates brain function within limbic (amygdala, anterior cingulate gyrus) and hippocampal regions during tasks of reward processing2, 3 and episodic memory. Moreover, animal studies suggest that the CaV1.2 L-type calcium channels influence emotional behaviour through enhanced neurotransmission via the lateral amygdala pathway. On the basis of this evidence, we tested the hypotheses that the CACNA1C rs1006737 risk allele will modulate neural responses within predefined prefrontal and subcortical regions of interest during emotional face processing and that this effect would be amplified in BD patients.

Face context interferes with local part processing in a prosopagnosic patient

We investigated the role of local and global information on perceptual encoding of faces in patient HJA, who shows prosopagnosia and visual agnosia following occipito-temporal damage. HJA and an age-matched control were tested in a simultaneous matching task which focused on detection of local changes in faces: the inversion of central parts (eyes and mouth) relative to their context (as in the Thatcher illusion). Same-different judgements were made to normal, “thatcherised” and mixed type face pairs. Whole faces (Experiment 1), or face parts (Experiment 2), were presented in upright and inverted orientations. Compared to the control, HJA was severely impaired at matching whole faces, but he improved dramatically when face parts were presented in isolation. This suggests an inhibitory influence of face context on HJAs processing of local parts and a relatively intact ability to process part-based information from a face (when context cannot interfere). Face inversion did not affect HJAs performance. A control experiment (Experiment 3) with non-face stimuli (houses) suggested that the inhibitory influence of context on HJAs performance was restricted to faces. These results indicate that contextual information in a face can have an adverse influence on the processing of local part-based information in prosopagnosia.

Comparing neural correlates of configural processing in faces and objects:An ERP study of the thatcher illusion

In the Thatcher illusion, a face with inverted eyes and mouth looks abnormal when upright but not when inverted. Behavioral studies have shown that thatcherization of an upright face disrupts perceptual processing of the local configuration. We recorded high-density EEG from normal observers to study ERP correlates of the illusion during the perception of faces and nonface objects, to determine whether inversion and thatcherization affect similar neural mechanisms. Observers viewed faces and houses in four conditions (upright vs. inverted, and normal vs. thatcherized) while detecting an oddball category (chairs). Thatcherization delayed the N170 component over occipito-temporal cortex to faces, but not to houses. This modulation matched the illusion as it was larger for upright than inverted faces. The P1 over medial occipital regions was delayed by face inversion but unaffected by thatcherization. Finally, face thatcherization delayed P2 over occipito-temporal but not over parietal regions, while inversion affected P2 across categories. All effects involving thatcherization were face-specific. These results indicate that effects of face inversion and feature inversion (in thatcherized faces) can be distinguished on a functional as well as neural level, and that they affect configural processing of faces in different time windows. © 2006 Elsevier Inc.

Differential patterns of activity and functional connectivity in emotion processing neural circuitry to angry and happy faces in adolescents with and without suicide attempt

Background - Neural substrates of emotion dysregulation in adolescent suicide attempters remain unexamined. Method - We used functional magnetic resonance imaging to measure neural activity to neutral, mild or intense (i.e. 0%, 50% or 100% intensity) emotion face morphs in two separate emotion-processing runs (angry and happy) in three adolescent groups: (1) history of suicide attempt and depression (ATT, n = 14); (2) history of depression alone (NAT, n = 15); and (3) healthy controls (HC, n = 15). Post-hoc analyses were conducted on interactions from 3 group × 3 condition (intensities) whole-brain analyses (p < 0.05, corrected) for each emotion run. Results - To 50% intensity angry faces, ATT showed significantly greater activity than NAT in anterior cingulate gyral–dorsolateral prefrontal cortical attentional control circuitry, primary sensory and temporal cortices; and significantly greater activity than HC in the primary sensory cortex, while NAT had significantly lower activity than HC in the anterior cingulate gyrus and ventromedial prefrontal cortex. To neutral faces during the angry emotion-processing run, ATT had significantly lower activity than NAT in the fusiform gyrus. ATT also showed significantly lower activity than HC to 100% intensity happy faces in the primary sensory cortex, and to neutral faces in the happy run in the anterior cingulate and left medial frontal gyri (all p < 0.006,corrected). Psychophysiological interaction analyses revealed significantly reduced anterior cingulate gyral–insula functional connectivity to 50% intensity angry faces in ATT v. NAT or HC. Conclusions - Elevated activity in attention control circuitry, and reduced anterior cingulate gyral–insula functional connectivity, to 50% intensity angry faces in ATT than other groups suggest that ATT may show inefficient recruitment of attentional control neural circuitry when regulating attention to mild intensity angry faces, which may represent a potential biological marker for suicide risk.

Late development of metric part-relational processing in object recognition

Four experiments with unfamiliar objects examined the remarkably late consolidation of part-relational relative to part-based object recognition (Jüttner, Wakui, Petters, Kaur, & Davidoff, 2013). Our results indicate a particularly protracted developmental trajectory for the processing of metric part relations. Schoolchildren aged 7 to 14 years and adults were tested in 3-Alternative-Forced-Choice tasks to judge the correct appearance of upright and inverted newly learned multipart objects that had been manipulated in terms of individual parts or part relations. Experiment 1 showed that even the youngest tested children were close to adult levels of performance for recognizing categorical changes of individual parts and relative part position. By contrast, Experiment 2 demonstrated that performance for detecting metric changes of relative part position was distinctly reduced in young children compared with recognizing metric changes of individual parts, and did not approach the latter until 11 to 12 years. A similar developmental dissociation was observed in Experiment 3, which contrasted the detection of metric relative-size changes and metric part changes. Experiment 4 showed that manipulations of metric size that were perceived as part (rather than part-relational) changes eliminated this dissociation. Implications for theories of object recognition and similarities to the development of face perception are discussed. © 2014 American Psychological Association.

Developmental commonalities between object and face recognition in adolescence

In the visual perception literature, the recognition of faces has often been contrasted with that of non-face objects, in terms of differences with regard to the role of parts, part relations and holistic processing. However, recent evidence from developmental studies has begun to blur this sharp distinction. We review evidence for a protracted development of object recognition that is reminiscent of the well-documented slow maturation observed for faces. The prolonged development manifests itself in a retarded processing of metric part relations as opposed to that of individual parts and offers surprising parallels to developmental accounts of face recognition, even though the interpretation of the data is less clear with regard to holistic processing. We conclude that such results might indicate functional commonalities between the mechanisms underlying the recognition of faces and non-face objects, which are modulated by different task requirements in the two stimulus domains.

The influence of variations in eating disorder-related symptoms on processing of emotional faces in a non-clinical female sample:an eye-tracking study

This study aimed to: i) determine if the attention bias towards angry faces reported in eating disorders generalises to a non-clinical sample varying in eating disorder-related symptoms; ii) examine if the bias occurs during initial orientation or later strategic processing; and iii) confirm previous findings of impaired facial emotion recognition in non-clinical disordered eating. Fifty-two females viewed a series of face-pairs (happy or angry paired with neutral) whilst their attentional deployment was continuously monitored using an eye-tracker. They subsequently identified the emotion portrayed in a separate series of faces. The highest (n=18) and lowest scorers (n=17) on the Eating Disorders Inventory (EDI) were compared on the attention and facial emotion recognition tasks. Those with relatively high scores exhibited impaired facial emotion recognition, confirming previous findings in similar non-clinical samples. They also displayed biased attention away from emotional faces during later strategic processing, which is consistent with previously observed impairments in clinical samples. These differences were related to drive-for-thinness. Although we found no evidence of a bias towards angry faces, it is plausible that the observed impairments in emotion recognition and avoidance of emotional faces could disrupt social functioning and act as a risk factor for the development of eating disorders.