Activation reduction in anterior temporal cortices during repeated recognition of faces of personal acquaintances

Repeated recognition of the face of a familiar individual is known to show semantic repetition priming effect. In this study, normal subjects were repeatedly presented faces of their colleagues, and the effect of repetition on the regional cerebral blood flow change was measured using positron emission tomography. They repeated a set of three tasks: the familiar-face detection (F) task, the facial direction discrimination (D) task, and the perceptual control (C) task. During five repetitions of the F task, familiar faces were presented six times from different views in a pseudorandom order. Activation reduction through the repetition of the F tasks was observed in the bilateral anterior (anterolateral to the polar region) temporal cortices which are suggested to be involved in the access to the long-term memory concerning people. The bilateral amygdala, the hypothalamus, and the medial frontal cortices, were constantly activated during the F tasks, and considered to be associated with the behavioral significance of the presented familiar faces. Constant activation was also observed in the bilateral occipitotemporal regions and fusiform gyri and the right medial temporal regions during perception of the faces, and in the left medial temporal regions during the facial familiarity detection task, which are consistent with the results of previous functional brain imaging studies. The results have provided further information about the functional segregation of the anterior temporal regions in face recognition and long-term memory.     

Passive and active recognition of one's own face

Facial identity recognition has been studied mainly with explicit discrimination requirement and faces of social figures in previous human brain imaging studies. We performed a PET activation study with normal volunteers in facial identity recognition tasks using the subject's own face as visual stimulus. Three tasks were designed so that the activation of the visual representation of the face and the effect of sustained attention to the representation could be separately examined: a control-face recognition task (C), a passive own-face recognition task (no explicit discrimination was required) (P), and an active own-face recognition task (explicit discrimination was required) (A). Increased skin conductance responses during recognition of own face were seen in both task P and task A, suggesting the occurrence of psychophysiological changes during recognition of one's own face. The left fusiform gyrus, the right supramarginal gyrus, the left putamen, and the right hypothalamus were activated in tasks P and A compared with task C. The left fusiform gyrus and the right supramarginal gyrus are considered to be involved in the representation of one's own face. The activation in the right supramarginal gyrus may be associated with the representation of one's own face as a part of one's own body. The prefrontal cortices, the right anterior cingulate, the right presupplementary motor area, and the left insula were specifically activated during task A compared with tasks C and P, indicating that these regions may be involved in the sustained attention to the representation of one's own face.     

Anatomy and time course of discrimination and categorization processes in vision: an fMRI study

Studies investigating the cerebral areas involved in visual processes generally oppose either different tasks or different stimulus types. This work addresses, by fMRI, the interaction between the type of task (discrimination vs. categorization) and the type of stimulus (Latin letters, well-known geometrical figures, and Korean letters). Behavioral data revealed that the two tasks did not differ in term of percentage of errors or correct responses, but a delay of 185 ms was observed for the categorization task in comparison with the discrimination task. All conditions activated a common neural network that includes both striate and extrastriate areas, especially the fusiform gyri, the precunei, the insulae, and the dorsolateral frontal cortex. In addition, interaction analysis revealed that the right insula was sensitive to both tasks and stimuli, and that stimulus type induced several significant signal variations for the categorization task in right frontal cortex, the right middle occipital gyrus, the right cuneus, and the left and right fusiform gyri, whereas for the discrimination task, significant signal variations were observed in the right occipito-parietal junction only. Finally, analyzing the latency of the BOLD signal also revealed a differential neural dynamics according to tasks but not to stimulus type. These temporal differences suggest a parallel hemisphere processing in the discrimination task vs. a cooperative interhemisphere processing in the categorization task that may reflect the observed differences in reaction time.     

The Role of the Fusiform Gyrus in Successful Encoding of Face Stimuli

PET was used to measure regional cerebral blood flow (rCBF) while memorizing pictures of unfamiliar human faces presented one at a time (FaceMemory). Other conditions included: (1) FaceRepeat—memorization of four individual faces presented repeatedly; (2) FaceWatching—viewing passively single faces without overt memory demands; and (3) Scrambled—counting dots superimposed on pictures of scrambled faces. After each FaceMemory condition and after the final FaceWatching condition scan, recall was tested by measuring face recognition. Contrasting FaceMemory and Scrambled conditions revealed several temporal activations: right midfusiform and bilateral anterior fusiform gyri. Contrasting FaceWatching and Scrambled conditions showed bilateral activation in the temporal poles and in the anterior fusiform gyri. No hippocampal activation arose from any contrast. Region of interest analyses on the above areas showed correlations with performance: (1) only rCBF in the right midfusiform correlated positively with encoding during the FaceMemory and FaceWatching conditions; (2) in the right temporal polar cortex rCBF decreased during FaceMemory and correlated positively with performance, whereas rCBF increased during FaceWatching and correlated negatively with incidental performance; and (3) activity in the anterior fusiform gyri remained constant across the conditions of FaceMemory, FaceRepeat, FaceWatching, and Scrambled and was uncorrelated with performance. These data suggest an expanded mnemonic role for the right midfusiform in depth of processing/encoding of face information, temporal polar cortex in face perception and recognition, and anterior fusiform activity in featural visual feature processing.     

Cortical mechanisms of visual self-recognition

Several lines of evidence have suggested that visual self-recognition is supported by a special brain mechanism; however, its functional anatomy is of great controversy. We performed an event-related functional magnetic resonance imaging (fMRI) study to identify brain regions selectively involved in recognition of one's own face. We presented pictures of each subject's own face (SELF) and a prelearned face of an unfamiliar person (CONT), as well as two personally familiar faces with high and low familiarity (HIGH and LOW, respectively) to test selectivity of activation to the SELF face. Compared with the CONT face, activation selective to the SELF face was observed in the right occipito-temporo-parietal junction and frontal operculum, as well as in the left fusiform gyrus. On the contrary, the temporoparietal junction in both the hemispheres and the left anterior temporal cortex, which were activated during recognition of HIGH and/or LOW faces, were not activated during recognition of the SELF face. The results confirmed the partial distinction of the brain mechanism involved in recognition of personally familiar faces and that in recognition of one's own face. The right occipito-temporo-parietal junction and frontal operculum appear to compose a network processing motion-action contingency, a role of which in visual self-recognition has been suggested in previous behavioral studies. Activation of the left fusiform gyrus selective to one's own face was consistent with the results of two previous functional imaging studies and a neuropsychological report, possibly suggesting its relationship with lexical processing.     

Early Category-Specific Cortical Activation Revealed by Visual Stimulus Inversion

Visual categorization may already start within the first 100-ms after stimulus onset, in contrast with the long-held view that during this early stage all complex stimuli are processed equally and that category-specific cortical activation occurs only at later stages. The neural basis of this proposed early stage of high-level analysis is however poorly understood. To address this question we used magnetoencephalography and anatomically-constrained distributed source modeling to monitor brain activity with millisecond-resolution while subjects performed an orientation task on the upright and upside-down presented images of three different stimulus categories: faces, houses and bodies. Significant inversion effects were found for all three stimulus categories between 70–100-ms after picture onset with a highly category-specific cortical distribution. Differential responses between upright and inverted faces were found in well-established face-selective areas of the inferior occipital cortex and right fusiform gyrus. In addition, early category-specific inversion effects were found well beyond visual areas. Our results provide the first direct evidence that category-specific processing in high-level category-sensitive cortical areas already takes place within the first 100-ms of visual processing, significantly earlier than previously thought, and suggests the existence of fast category-specific neocortical routes in the human brain.     

The role of action knowledge in the comprehension of artefacts--a PET study.

Activation of the left ventral premotor cortex (PMv) has in previous imaging studies been associated with the processing of visually presented artefacts. It has been suggested that this activation reflects processing of action knowledge and that action knowledge contributes to the comprehension of artefacts. The purpose of the present study was to test whether activation of the left PMv is common for all tasks involving the comprehension of artefacts or whether it is task specific. This was done by comparing performance and regional cerebral blood flow (rCBF) associated with two categorization tasks and two naming tasks divided by category (natural objects vs artefacts). The left PMv (BA 6/44) was more activated by the categorization task for artefacts than by the categorization task for natural objects and the naming task for artefacts. However, the left PMv was not associated with the contrast between the naming task for artefacts and the naming task for natural objects nor with the processing of artefacts in general. If the PMv does mediate action knowledge, these results suggest that action knowledge does not contribute directly to the comprehension of artefacts but may support the categorization of artefacts. The significance of these findings is discussed in relation to category-specific recognition impairments for artefacts.     

The functionally defined right occipital and fusiform "face areas" discriminate novel from visually familiar faces

Neuroimaging (PET and fMRI) studies have identified a set of brain areas responding more to faces than to other object categories in the visual extrastriate cortex of humans. This network includes the middle lateral fusiform gyrus (the fusiform face area, or FFA) as well as the inferior occipital gyrus (occipital face area, OFA). The exact functions of these areas in face processing remain unclear although it has been argued that their primary function is to distinguish faces from nonface object categories-"face detection"-or also to discriminate among faces, irrespective of their visual familiarity to the observer. Here, we combined the data from two previous positron emission tomography (PET) studies to show that the functionally defined face areas are involved in the automatic discrimination between unfamiliar faces and familiar faces. Consistent with previous studies, a face localizer contrast (faces-objects) revealed bilateral activation in the middle lateral fusiform gyrus (FFA, BA37) and in the right inferior occipital cortex (OFA, BA19). Within all the regions of the right hemisphere, larger levels of activation were found for unfamiliar as compared to familiar faces. These results suggest that the very same areas involved in categorizing faces at the basic or individual level, play a role in differentiating familiar faces from new faces, showing an overlap between visual and presemantic mnesic representations of faces in the right hemisphere.     

Position-specific and position-invariant face aftereffects reflect the adaptation of different cortical areas

Adaptation to faces leads to face aftereffects and currently this topic attracts a lot of attention because it clearly shows that adaptation occurs even at the higher stages of visual cortical processing. Recently it has been found that long-term exposure to a face stimulus results in adaptation of a position-specific population of face sensitive neurons in addition to a position-invariant neural population, the later being also adapted in the case of short-term adaptation. Here we used the fMRI adaptation technique to investigate the neural locus of position-specific and position-invariant face adaptation. We show that in the right fusiform face area adaptation effects are position invariant and can be evoked by short (500 ms) as well as long (4500 ms) adaptation durations. On the other hand adaptation effects in the right occipital face area are position-specific and require long-term adaptation to develop. These findings imply that the behaviourally observed face aftereffects reflect time-dependent adaptation processes of both position-specific and invariant face sensitive neurons at different stages of visual processing.     

When meaningless symbols become letters: neural activity change in learning new phonograms

Left fusiform gyrus and left angular gyrus are considered to be respectively involved with visual form processing and associating visual and auditory (phonological) information in reading. However, there are a number of studies that fail to show the contribution of these regions in carrying out these aspects of reading. Considerable differences in the type of stimuli and tasks used in the various studies may account for the discrepancy in results. This functional magnetic resonance imaging (fMRI) study attempts to control aspects of experimental stimuli and tasks to specifically investigate brain regions involved with visual form processing and character-to-phonological (i.e., simple grapheme-to-phonological) conversion processing for single letters. Subjects performed a two-back identification task using known Japanese, and previously unknown Korean, and Thai phonograms before and after training on one of the unknown language orthographies. Japanese subjects learned either five Korean or five Thai phonograms. Brain regions related to visual form processing were assessed by comparing activity related to native (Japanese) phonograms with that of non-native (Korean and Thai) phonograms. There was no significant differential brain activity for visual form processing. Brain regions related to character-to-phonological conversion processing were assessed by comparing pre- and post-tests of trained non-native phonograms with that of native phonograms and non-trained non-native phonograms. Significant differential activation post-relative to pre-training exclusively for the trained non-native phonograms was found in left angular gyrus. In addition, psychophysiologic interaction (PPI) analysis revealed greater integration of left angular gyrus with primary visual cortex as well as with superior temporal gyrus for the trained phonograms post-relative to pre-training. The results suggest that left angular gyrus is involved with character-to-phonological conversion in letter perception.     

View-independent coding of face identity in frontal and temporal cortices is modulated by familiarity: an event-related fMRI study

Face recognition is a unique visual skill enabling us to recognize a large number of person identities, despite many differences in the visual image from one exposure to another due to changes in viewpoint, illumination, or simply passage of time. Previous familiarity with a face may facilitate recognition when visual changes are important. Using event-related fMRI in 13 healthy observers, we studied the brain systems involved in extracting face identity independent of modifications in visual appearance during a repetition priming paradigm in which two different photographs of the same face (either famous or unfamiliar) were repeated at varying delays. We found that functionally defined face-selective areas in the lateral fusiform cortex showed no repetition effects for faces across changes in image views, irrespective of pre-existing familiarity, suggesting that face representations formed in this region do not generalize across different visual images, even for well-known faces. Repetition of different but easily recognizable views of an unfamiliar face produced selective repetition decreases in a medial portion of the right fusiform gyrus, whereas distinct views of a famous face produced repetition decreases in left middle temporal and left inferior frontal cortex selectively, but no decreases in fusiform cortex. These findings reveal that different views of the same familiar face may not be integrated within a single representation at initial perceptual stages subserved by the fusiform face areas, but rather involve later processing stages where more abstract identity information is accessed.     

Neural Activation during Covert Processing of Positive Emotional Facial Expressions

Lesion studies indicate distinct neural systems for recognition of facial identity and emotion. Split-brain experiments also suggest that emotional evaluation of a stimulus can occur without conscious identification. The present study tested a hypothesis of a differential neural response, independent of explicit conscious mediation, to emotional compared to nonemotional faces. The experimental paradigm involved holding in mind an image of a face across a 45-s delay while regional cerebral blood flow was measured using positron emission tomography. Prior to the delay, a single face was presented with an explicit instruction to match it to one of two faces, photographed at different angles from the target face, presented at the end of the delay. Repeated blood flow measures were obtained while subjects held happy or neutral faces in mind or during a neutral control fixation condition without initial face presentation. The representation of emotional faces over a delay period, compared to either the nonemotional or the fixation condition, was associated with significant activation in the left ventral prefrontal cortex, the left anterior cingulate cortex, and the right fusiform gyrus. The findings support our hypothesis of a differential neural response to facial emotion, independent of conscious mediation, in regions implicated in the processing of faces and of emotions.     

Human brain regions involved in visual categorization

Categorization of dot patterns is a frequently used paradigm in the behavioral study of natural categorization. To determine the human brain regions involved in categorization, we used Positron Emission Tomography to compare regional Cerebral Blood Flow patterns in two tasks employing patterns that consisted of nine dots. In the categorization task, subjects categorized novel exemplars of two categories, generated by distorting two prototypes, and other random dot patterns. In the control task, subjects judged the position of similarly distorted patterns. Each task was presented at two matched levels of difficulty. Fixation of the fixation target served as baseline condition. The categorization task differentially activated the orbitofrontal cortex and two dorsolateral prefrontal regions. These three prefrontal regions were equally weakly active in the position discrimination task and the baseline condition. The intraparietal sulcus was activated in both tasks, albeit significantly less in the position discrimination than in the categorization task. A similar activation pattern was present in the neostriatum. Task difficulty had no effect. These functional imaging results show that the dot-pattern categorization task strongly engages prefrontal and parietal cortical areas. The activation of prefrontal cortex during visual categorization in humans agrees with the recent finding of category-related responses in macaque prefrontal neurons.     

The roles of "face" and "non-face" areas during individual face perception: evidence by fMRI adaptation in a brain-damaged prosopagnosic patient

Two regions in the human occipito-temporal cortex respond preferentially to faces: 'the fusiform face area' ('FFA') and the 'occipital face area' ('OFA'). Whether these areas have a dominant or exclusive role in face perception, or if sub-maximal responses in other visual areas such as the lateral occipital complex (LOC) are also involved, is currently debated. To shed light on this issue, we tested normal participants and PS, a well-known brain-damaged patient presenting a face-selective perception deficit (prosopagnosia) [Rossion, B., Caldara, R., Seghier, M., Schuller, A. M., Lazeyras, F., Mayer, E. (2003). A network of occipito-temporal face-sensitive areas besides the right middle fusiform gyrus is necessary for normal face processing. Brain 126 2381-2395.], with functional magnetic resonance imaging (fMRI). Of particular interest, the right hemisphere lesion of the patient PS encompasses the 'OFA' but preserves the 'FFA' and LOC [Sorger, B., Goebel, R., Schiltz, C., Rossion, B. (2007). Understanding the functional neuroanatomy of acquired prosopagnosia. NeuroImage 35, 836-852.]. Using fMRI-adaptation, we found a dissociation between the coding of individual exemplars in the structurally intact 'FFA', which was impaired for faces but preserved for objects in the patient PS's brain. Most importantly, a larger response to different faces than repeated faces was found in the ventral part of the LOC both for normals and the patient, next to the right hemisphere lesion. Thus, following prosopagnosia, areas that do not respond preferentially to faces such as the ventral part of the LOC (vLOC) may still be recruited for compensatory or residual individual face perception. Overall, these observations indicate that several high-level visual areas in the human brain contribute to individual face perception. However, a subset of these areas in the right hemisphere, those responding preferentially to faces ('FFA' and 'OFA'), appear to be critical for this function.     

Faces are represented holistically in the human occipito-temporal cortex

Two identical top parts of a face photograph look different if their bottom parts differ. This perceptual illusion, the "face composite effect", is taken as strong evidence that faces are processed as a whole rather than as a collection of independent features. To test the hypothesis that areas responding preferentially to faces in the human brain represent faces holistically, we recorded functional magnetic resonance imaging (fMRI) during an adaptation paradigm with the composite face illusion. In both the middle fusiform gyrus (MFG) and the inferior occipital gyrus (IOG), we observed a significantly larger response to the same top face when it was aligned with different bottom parts than with the same bottom part, with a most robust effect in the right middle fusiform gyrus. This difference was not found when the top and the bottom face parts were spatially misaligned or when the faces were presented upside-down. These findings indicate that facial features are integrated into holistic face representations in areas of the human visual cortex responding preferentially to faces.     

fMRI correlates of cortical specialization and generalization for letter processing

The present study used functional magnetic resonance imaging to examine cortical specialization for letter processing. We assessed whether brain regions that were involved in letter processing exhibited domain-specific and/or mandatory responses, following Fodor's definition of properties of modular systems (Fodor, J.A., 1983. The Modularity of Mind. The MIT Press, Cambridge, MA.). Domain-specificity was operationalized as selective, or exclusive, activation for letters relative to object and visual noise processing and a baseline fixation task. Mandatory processing was operationalized as selective activation for letters during both a silent naming and a perceptual matching task. In addition to these operational definitions, other operational definitions of selectivity for letter processing discussed by [Pernet, C., Celsis, P., Demonet, J., 2005. Selective response to letter categorization within the left fusiform gyrus. NeuroImage 28, 738-744] were applied to the data. Although the left fusiform gyrus showed a specialized response to letters using the definition of selectivity put forth by [Pernet, C., Celsis, P., Demonet, J., 2005. Selective response to letter categorization within the left fusiform gyrus. NeuroImage 28, 738-744], this region did not exhibit specialization for letters according to our more conservative definition of selectivity. Instead, this region showed equivalent activation by letters and objects in both the naming and matching tasks. Hence, the left fusiform gyrus does not exhibit domain-specific or mandatory processing but may reflect a shared input system for both stimulus types. The left insula and some portions of the left inferior parietal lobule, however, did show a domain-specific response for letter naming but not for letter matching. These regions likely subserve some linguistically oriented cognitive process that is unique to letters, such as grapheme-to-phoneme translation or retrieval of phonological codes for letter names. Hence, cortical specialization for letters emerged in the naming task in some peri-sylvian language related cortices, but not in occipito-temporal cortex. Given that the domain-specific response for letters in left peri-sylvian regions was only present in the naming task, these regions do not process letters in a mandatory fashion, but are instead modulated by the linguistic nature of the task.     

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.     

Emotion modulates the effects of endogenous attention on retinotopic visual processing

A fundamental challenge for organisms is how to focus on perceptual information relevant to current goals while remaining able to respond to goal-irrelevant stimuli that signal potential threat. Here, we studied how visual threat signals influence the effects of goal-directed spatial attention on the retinotopic distribution of processing resources in early visual cortex. We used a combined blocked and event-related functional magnetic resonance imaging paradigm with target displays comprising diagonal pairs of intact and scrambled faces presented simultaneously in the four visual field quadrants. Faces were male or female and had fearful or neutral emotional expressions. Participants attended covertly to a pair of two diagonally opposite stimuli and performed a gender-discrimination task on the attended intact face. In contrast to the fusiform face area, where attention and fearful emotional expression had additive effects, neural responses to attended and unattended fearful faces were indistinguishable in early retinotopic visual areas: When attended, fearful face expression did not further enhance responses, whereas when unattended, fearful expression increased responses to the level of attended face stimuli. Remarkably, the presence of fearful stimuli augmented the enhancing effect of attention on retinotopic responses to neutral faces in remote visual field locations. We conclude that this redistribution of neural activity in retinotopic visual cortex may serve the purpose of allocating processing resources to task-irrelevant threat-signaling stimuli while at the same time increasing resources for task-relevant stimuli as required for the maintenance of goal-directed behavior.     

Developmental changes in category-specific brain responses to numbers and letters in a working memory task

Neuroimaging studies have identified a common network of brain regions involving the prefrontal and parietal cortices across a variety of working memory (WM) tasks. However, previous studies have also reported category-specific dissociations of activation within this network. In this study, we investigated the development of category-specific activation in a WM task with digits, letters, and faces. Eight-year-old children and adults performed a 2-back WM task while their brain activity was measured using functional magnetic resonance imaging (fMRI). Overall, children were significantly slower and less accurate than adults on all three WM conditions (digits, letters, and faces); however, within each age group, behavioral performance across the three conditions was very similar. FMRI results revealed category-specific activation in adults but not children in the intraparietal sulcus for the digit condition. Likewise, during the letter condition, category-specific activation was observed in adults but not children in the left occipital–temporal cortex. In contrast, children and adults showed highly similar brain-activity patterns in the lateral fusiform gyri when solving the 2-back WM task with face stimuli. Our results suggest that 8-year-old children do not yet engage the typical brain regions that have been associated with abstract or semantic processing of numerical symbols and letters when these processes are task-irrelevant and the primary task is demanding. Nevertheless, brain activity in letter-responsive areas predicted children's spelling performance underscoring the relationship between abstract processing of letters and linguistic abilities. Lastly, behavioral performance on the WM task was predictive of math and language abilities highlighting the connection between WM and other cognitive abilities in development.     

Reactivation of visual cortex during memory retrieval: content specificity and emotional modulation

Studies on memory retrieval suggest a reactivation of cortical regions engaged during encoding, such that visual or auditory areas reactivate for visual or auditory memories. The content specificity and any emotion dependency of such reactivations are still unclear. Because distinct visual areas are specialized in processing distinct stimulus categories, we tested for face and word specific reactivations during a memory task using functional magnetic resonance imaging (fMRI). Furthermore, because visual processing and memory are both modulated by emotion, we compared reactivation for stimuli encoded in a neutral or emotionally significant context. In the learning phase, participants studied pairs of stimuli that consisted of either a scene and a face, or a scene and a word. Scenes were either neutral or negative, but did not contain faces or words. In the test phase scenes were presented alone (one in turn), and participants indicated whether it was previously paired with a face, a word, or was new. Results from the test phase showed activation in a functionally defined face-responsive region in the right fusiform gyrus, as well as in a word-responsive region in the left inferior temporal gyrus, for scenes previously paired with faces and words, respectively. Reactivation tended to be larger in both the face- and word-responsive regions when the associated scene was negative as compared to neutral. However, relative to neutral context, the recall of faces and words paired with a negative context produced smaller activations in brain regions associated with social and semantic processing, respectively, as well as poorer memory performance overall. Taken together, these results support the idea of cortical memory reactivations, even at a content-specific level, and further suggest that emotional context may produce opposite effects on reactivations in early sensory areas and more elaborate processing in higher-level cortical areas.