Facial Expressions Evoke Differential Neural Coupling in Macaques.

In humans and monkeys, face perception activates a distributed cortical network that includes extrastriate, limbic, and prefrontal regions. Within face-responsive regions, emotional faces evoke stronger responses than neutral faces ("valence effect"). We used fMRI and Dynamic Causal Modeling (DCM) to test the hypothesis that emotional faces differentially alter the functional coupling among face-responsive regions. Three monkeys viewed conspecific faces with neutral, threatening, fearful, and appeasing expressions. Using Bayesian model selection, various models of neural interactions between the posterior (TEO) and anterior (TE) portions of inferior temporal (IT) cortex, the amygdala, the orbitofrontal (OFC), and ventrolateral prefrontal cortex (VLPFC) were tested. The valence effect was mediated by feedback connections from the amygdala to TE and TEO, and feedback connections from VLPFC to the amygdala and TE. Emotional faces were associated with differential effective connectivity: Fearful faces evoked stronger modulations in the connections from the amygdala to TE and TEO; threatening faces evoked weaker modulations in the connections from the amygdala and VLPFC to TE; and appeasing faces evoked weaker modulations in the connection from VLPFC to the amygdala. Our results suggest dynamic alterations in neural coupling during the perception of behaviorally relevant facial expressions that are vital for social communication.

Expertise reduces neural cost but does not modulate repetition suppression.

The extent to which repetition suppression is modulated by expertise is currently unknown. We used event-related fMRI to test whether architecture students would respond faster to buildings and would exhibit stronger repetition suppression in the fusiform gyrus (FG) and parahippocampa cortex (PHC) than students from other disciplines. Behaviorally, we found shorter response latencies with target repetition in all subjects. Moreover, the repetition of targets and distracters was associated with decreased neural responses in the FG and PHC in all subjects. In control, but not in architecture students, reaction times during the first repetition of the target were correlated with activation in the cuneus, lingual gyrus, inferior parietal lobule, insula, and anterior cingulate cortex, indicating that the non-experts had to recruit additional regions in order to perform the task. Our findings suggest that due to their expertise, architects were able to encode and detect building stimuli at a lower neural cost.

The Gender of Face Stimuli is Represented in Multiple Regions in the Human Brain.

Face perception in humans is mediated by activation in a network of brain areas. Conventional univariate fMRI data analysis has not localized differential responses to viewing male as compared with viewing female faces within this network. We tested whether we could detect neural response patterns specific to viewing male vs. female faces in 40 participants. Replicating earlier work, face stimuli evoked activation in the core (inferior occipital gyrus, IOG; fusiform gyrus, FG; and superior temporal sulcus, STS), as well as extended (amygdala, inferior frontal gyrus, IFG; insula, INS; and orbitofrontal cortex, OFC) regions of the face network. Multivariate pattern classification of activity within these regions revealed successful decoding of gender information, significantly above chance, in the IOG, FG, STS, IFG, INS, and OFC, but not in the amygdala. Multiple control regions indicated that this result might be restricted to face-responsive regions. Our findings suggest that gender information is distributed across the face network and is represented in the core regions that process invariant facial features, as well as the extended regions that process changeable aspects of faces.

Seeing with the mind's eye: top-down, bottom-up, and conscious awareness.

With the advent of functional brain imaging techniques and recent developments in the analysis of cortical connectivity, the focus of mental imagery studies has shifted from a semi-modular approach to an integrated cortical network perspective. Functional magnetic resonance imaging studies of visual imagery of faces and objects show that activation of content-specific representations stored in the ventral visual stream is top-down-modulated by parietal and frontal regions. Recent findings in patients with conscious awareness disorders reveal that mental imagery can be used to map patterns of residual cognitive function in their brain and to provide diagnostic and prognostic indicators.

Seeing faces and objects with the "mind's eye".

With the advent of functional brain imaging techniques and recent developments in the analysis of cortical connectivity, the focus of mental imagery studies has shifted from a semi-modular approach to a more realistic, integrated, cortical networks perspective. Recent studies of visual imagery of faces and objects suggest that activation of content-specific representations stored in the ventral visual stream is top-down modulated by parietal and frontal regions. The relation of these findings to other cognitive functions is discussed, as well as their clinical implications for patients with impaired states of conscious awareness.

Training facilitates object recognition in cubist paintings.

To the naïve observer, cubist paintings contain geometrical forms in which familiar objects are hardly recognizable, even in the presence of a meaningful title. We used fMRI to test whether a short training session about Cubism would facilitate object recognition in paintings by Picasso, Braque and Gris. Subjects, who had no formal art education, were presented with titled or untitled cubist paintings and scrambled images, and performed object recognition tasks. Relative to the control group, trained subjects recognized more objects in the paintings, their response latencies were significantly shorter, and they showed enhanced activation in the parahippocampal cortex, with a parametric increase in the amplitude of the fMRI signal as a function of the number of recognized objects. Moreover, trained subjects were slower to report not recognizing any familiar objects in the paintings and these longer response latencies were correlated with activation in a fronto-parietal network. These findings suggest that trained subjects adopted a visual search strategy and used contextual associations to perform the tasks. Our study supports the proactive brain framework, according to which the brain uses associations to generate predictions.

Recollection- and familiarity-based decisions reflect memory strength.

We used event-related fMRI to investigate whether recollection- and familiarity-based memory judgments are modulated by the degree of visual similarity between old and new art paintings. Subjects performed a flower detection task, followed by a Remember/Know/New surprise memory test. The old paintings were randomly presented with new paintings, which were either visually similar or visually different. Consistent with our prediction, subjects were significantly faster and more accurate to reject new, visually different paintings than new, visually similar ones. The proportion of false alarms, namely remember and know responses to new paintings, was significantly reduced with decreased visual similarity. The retrieval task evoked activation in multiple visual, parietal and prefrontal regions, within which remember judgments elicited stronger activation than know judgments. New, visually different paintings evoked weaker activation than new, visually similar items in the intraparietal sulcus. Contrasting recollection with familiarity revealed activation predominantly within the precuneus, where the BOLD response elicited by recollection peaked significantly earlier than the BOLD response evoked by familiarity judgments. These findings suggest that successful memory retrieval of pictures is mediated by activation in a distributed cortical network, where memory strength is manifested by differential hemodynamic profiles. Recollection- and familiarity-based memory decisions may therefore reflect strong memories and weak memories, respectively.

Neural correlates of object indeterminacy in art compositions.

Indeterminate art invokes a perceptual dilemma in which apparently detailed and vivid images resist identification. We used event-related fMRI to study visual perception of representational, indeterminate and abstract paintings. We hypothesized increased activation along a gradient of posterior-to-anterior ventral visual areas with increased object resolution, and postulated that object resolution would be associated with visual imagery. Behaviorally, subjects were faster to recognize familiar objects in representational than in both indeterminate and abstract paintings. We found activation within a distributed cortical network that includes visual, parietal, limbic and prefrontal regions. Representational paintings, which depict scenes cluttered with familiar objects, evoked stronger activation than indeterminate and abstract paintings in higher-tier visual areas. Perception of scrambled paintings was associated with imagery-related activation in the precuneus and prefrontal cortex. Finally, representational paintings evoked stronger activation than indeterminate paintings in the temporoparietal junction. Our results suggest that perception of familiar content in art works is mediated by object recognition, memory recall and mental imagery, cognitive processes that evoke activation within a distributed cortical network.

Famous faces activate contextual associations in the parahippocampal cortex.

The parahippocampal cortex (PHC) has been traditionally implicated both in place processing and in episodic memory. How could the same cortical region mediate these cognitive functions that seem quite different? We have recently proposed that the PHC should be seen as more generally mediating contextual associative processing, which is required for both navigation and memory. We therefore predicted that any associative objects should activate the PHC. To test this generalization, we investigated the extent to which common stimuli that are nonspatial by nature, namely faces, activate the PHC, although their perception is typically associated with other cortical structures. Specifically, we compared the activation elicited by famous faces, which are highly associated with rich pictorial and contextual information (e.g., Tom Cruise) and are not associated with a specific place, with activation elicited by unfamiliar faces. Consistent with our prediction, contrasting famous with unfamiliar faces revealed significant activation within the PHC. Taken collectively, these findings indicate that the PHC should be regarded as mediating contextual associations in general and not necessarily spatial or episodic information.

Let's face it: it's a cortical network.

Face perception elicits activation within a distributed cortical network in the human brain. The network includes visual ("core") regions, which process invariant facial features, as well as limbic and prefrontal ("extended") regions that process changeable aspects of faces. Analysis of effective connectivity reveals that the major entry node in the "face network" is the lateral fusiform gyrus and that the functional coupling between the core and the extended systems is content-dependent. A model for face perception is proposed, in which the flow of information through the network is shaped by cognitive demands.

Mapping the human brain: new insights from FMRI data sharing.

The sharing of primary data in the field of neuroscience has received considerable scrutiny from scientific societies and from science journals. Many see this as value added for science publishing that can enhance and inform secondary examination of data and results. Still others worry that data sharing is an undue burden for researchers with little long term value to science. But examples of how data sharing can be done successfully do exist. The fMRI Data Center, established at Dartmouth College in 2000 and now based at the University of California Santa Barbara, has worked to facilitate the open sharing of neuroimaging data from peer-reviewed papers to foster progress in cognitive science. The fMRI study on the representation of objects in the human occipital and temporal cortex, published in 2000 in the Journal of Cognitive Neuroscience (JOCN), marked the first deposition in the new database. Despite initial concerns about fMRI data sharing, this data set was frequently downloaded. We describe the original results of distributed brain activation patterns elicited by faces and objects in the human visual system, and overview several secondary analyses by independent investigators. A philosopher tested Husserl's temporal components of consciousness, whereas other brain imagers deployed new analytic tools, from Dynamic Causal Modeling, which estimates the neural interactions between cortical regions, to a novel method for constructing reproducibility maps. These re-analyses revealed new findings not reported in the original study, provided new perspectives on visual perception, generated new predictions, and resulted in new collaborations and publications in high profile journals.

Perception, memory and aesthetics of indeterminate art.

Indeterminate art, in which familiar objects are only suggestive, invokes a perceptual conundrum as apparently detailed and vivid images resist identification. We hypothesized that compared with paintings that depict meaningful content, object recognition in indeterminate images would be delayed, and tested whether aesthetic affect depends on meaningful content. Subjects performed object recognition and judgment of aesthetic affect tasks. Response latencies were significantly longer for indeterminate images and subjects perceived recognizable objects in 24% of these paintings. Although the aesthetic affect rating of all paintings was similar, judgement latencies for the indeterminate paintings were significantly longer. A surprise memory test revealed that more representational than indeterminate paintings were remembered and that affective strength increased the probability of subsequent recall. Our results suggest that perception and memory of art depend on semantic aspects, whereas, aesthetic affect depends on formal visual features. The longer latencies associated with indeterminate paintings reflect the underlying cognitive processes that mediate object resolution. Indeterminate art works therefore comprise a rich set of stimuli with which the neural correlates of visual perception can be investigated.

Effective connectivity within the distributed cortical network for face perception.

Face perception elicits activation within a distributed cortical network in the human brain. The network includes visual ("core") regions, as well as limbic and prefrontal ("extended") regions, which process invariant facial features and changeable aspects of faces, respectively. We used functional Magnetic Resonance Imaging and Dynamic Causal Modeling to investigate effective connectivity and functional organization between and within the core and the extended systems. We predicted a ventral rather than dorsal connection between the core and the extended systems during face viewing and tested whether valence and fame would alter functional coupling within the network. We found that the core system is hierarchically organized in a predominantly feed-forward fashion, and that the fusiform gyrus (FG) exerts the dominant influence on the extended system. Moreover, emotional faces increased the coupling between the FG and the amygdala, whereas famous faces increased the coupling between the FG and the orbitofrontal cortex. Our results demonstrate content-specific dynamic alterations in the functional coupling between visual-limbic and visual-prefrontal face-responsive pathways.

Sex, beauty and the orbitofrontal cortex.

Face perception is mediated by a distributed neural system in the human brain. Attention, memory and emotion modulate the neural activation evoked by faces, however the effects of gender and sexual orientation are currently unknown. To test whether subjects would respond more to their sexually-preferred faces, we scanned 40 hetero- and homosexual men and women whilst they assessed facial attractiveness. Behaviorally, regardless of their gender and sexual orientation, all subjects similarly rated the attractiveness of both male and female faces. Consistent with our hypothesis, a three-way interaction between stimulus gender, beauty and the sexual preference of the subject was found in the medial orbitofrontal cortex (OFC). In heterosexual women and homosexual men, attractive male faces elicited stronger activation than attractive female faces, whereas in heterosexual men and homosexual women, attractive female faces evoked stronger activation than attractive male faces. These findings suggest that the OFC represents the value of salient sexually-relevant faces, irrespective of their reproductive fitness.

Recognition memory of newly learned faces.

We used event-related fMRI to study recognition memory of newly learned faces. Caucasian subjects memorized unfamiliar, neutral and happy South Korean faces and 4 days later performed a memory retrieval task in the MR scanner. We predicted that previously seen faces would be recognized faster and more accurately and would elicit stronger neural activation than novel faces. Consistent with our hypothesis, novel faces were recognized more slowly and less accurately than previously seen faces. We found activation in a distributed cortical network that included face-responsive regions in the visual cortex, parietal and prefrontal regions, and the hippocampus. Within all regions, correctly recognized, previously seen faces evoked stronger activation than novel faces. Additionally, in parietal and prefrontal cortices, stronger activation was observed during correct than incorrect trials. Finally, in the hippocampus, false alarms to happy faces elicited stronger responses than false alarms to neutral faces. Our findings suggest that face recognition memory is mediated by stimulus-specific representations stored in extrastriate regions; parietal and prefrontal regions where old and new items are classified; and the hippocampus where veridical memory traces are recovered.

Temporal dynamics of face repetition suppression.

Single-unit recordings and functional brain imaging studies have shown reduced neural responses to repeated stimuli in the visual cortex. Using MEG, we compared responses evoked by repetitions of neutral faces to those evoked by fearful faces, which were either task relevant (targets) or irrelevant (distracters). Faces evoked a bi-phasic response in extrastriate cortex, peaking at 160-185 ms and at 220-250 ms, with stronger responses to neutral faces at the earlier interval and stronger responses to fearful faces at the later interval. At both latencies, repetitions of neutral and fearful targets resulted in reduced amplitude of the MEG signal. Additionally, we found that the context in which targets were presented affected their processing: fearful distracters increased the responses evoked by both neutral and fearful targets. Our data indicate that valence enhancement and context effects can be detected in extrastriate visual cortex within 250 ms and that these processes likely reflect feedback from other regions.

Recognition memory is modulated by visual similarity.

We used event-related fMRI to test whether recognition memory depends on visual similarity between familiar prototypes and novel exemplars. Subjects memorized portraits, landscapes, and abstract compositions by six painters with a unique style, and later performed a memory recognition task. The prototypes were presented with new exemplars that were either visually similar or dissimilar. Behaviorally, novel, dissimilar items were detected faster and more accurately. We found activation in a distributed cortical network that included face- and object-selective regions in the visual cortex, where familiar prototypes evoked stronger responses than new exemplars; attention-related regions in parietal cortex, where responses elicited by new exemplars were reduced with decreased similarity to the prototypes; and the hippocampus and memory-related regions in parietal and prefrontal cortices, where stronger responses were evoked by the dissimilar exemplars. Our findings suggest that recognition memory is mediated by classification of novel exemplars as a match or a mismatch, based on their visual similarity to familiar prototypes.

Face perception is modulated by sexual preference.

Face perception is mediated by a distributed neural system in the human brain . The response to faces is modulated by cognitive factors such as attention, visual imagery, and emotion ; however, the effects of gender and sexual orientation are currently unknown. We used fMRI to test whether subjects would respond more to their sexually preferred faces and predicted such modulation in the reward circuitry. Forty heterosexual and homosexual men and women viewed photographs of male and female faces and assessed facial attractiveness. Regardless of their gender and sexual orientation, all subjects similarly rated the attractiveness of both male and female faces. Within multiple, bilateral face-selective regions in the visual cortex, limbic system, and prefrontal cortex, similar patterns of activation were found in all subjects in response to both male and female faces. Consistent with our hypothesis, we found a significant interaction between stimulus gender and the sexual preference of the subject in the thalamus and medial orbitofrontal cortex, where heterosexual men and homosexual women responded more to female faces and heterosexual women and homosexual men responded more to male faces. Our findings suggest that sexual preference modulates face-evoked activation in the reward circuitry.

Face perception is mediated by a distributed cortical network.

The neural system associated with face perception in the human brain was investigated using functional magnetic resonance imaging (fMRI). In contrast to many studies that focused on discreet face-responsive regions, the objective of the current study was to demonstrate that regardless of stimulus format, emotional valence, or task demands, face perception evokes activation in a distributed cortical network. Subjects viewed various stimuli (line drawings of unfamiliar faces and photographs of unfamiliar, famous, and emotional faces) and their phase scrambled versions. A network of face-responsive regions was identified that included the inferior occipital gyrus, fusiform gyrus, superior temporal sulcus, hippocampus, amygdala, inferior frontal gyrus, and orbitofrontal cortex. Although bilateral activation was found in all regions, the response in the right hemisphere was stronger. This hemispheric asymmetry was manifested by larger and more significant clusters of activation and larger number of subjects who showed the effect. A region of interest analysis revealed that while all face stimuli evoked activation within all regions, viewing famous and emotional faces resulted in larger spatial extents of activation and higher amplitudes of the fMRI signal. These results indicate that a mere percept of a face is sufficient to localize activation within the distributed cortical network that mediates the visual analysis of facial identity and expression.

Comparison of fMRI activation as measured with gradient- and spin-echo EPI during visual perception.

In this study, we compared fMRI activation measured with gradient- and spin-echo-based fMRI during visual perception of faces, which is mediated by neural activation within a distributed cortical network. With both fMRI techniques, bilateral activation was observed in multiple regions including the inferior occipital gyrus, fusiform gyrus, superior temporal sulcus, amygdala, inferior frontal gyrus, and orbitofrontal cortex. When compared with the gradient-echo sequence, activation measured with the spin-echo sequence was significantly reduced. This decrease was manifested by smaller cluster size, lower statistical significance, smaller amplitude of the fMRI signal, and smaller number of subjects who showed activation in all face-responsive regions. In orbitofrontal cortex, a region prone to susceptibility-related signal dephasing, the spin-echo acquisition considerably restored the signal, but did not reveal stronger activation when compared with the gradient-echo acquisition. Our data indicate that optimized GE sequences that reduce susceptibility artefacts are sufficient to detect activation in regions such as the orbitofrontal cortex.