Non-face Stimuli Research Articles

Endogenous context for visual processing of human faces and other objects

The human ability to quickly recognise faces and objects is an important skill. This skill may be facilitated by the prior existence of context-setting functional brain states. MEG was used to test the hypothesis that such states may be defined neurophysiologically. One type of state was identified by evaluating deterministic features in the dynamics of pre-stimulus brain activity in 10 individuals engaging in an object categorisation task. These states followed a statistical gamma-distribution similar to that seen in models of percept duration of competing stimuli. Both an early (42 ms) and a late (440 ms) response were only seen for face stimuli that were presented during states in which the MEG data displayed low determinism. A second type of state was identified by evaluating amplitudes of pre-stimulus brain activity. Between 140 and 150 ms, activity was highest for face as well as non-face stimuli presented during a low amplitude state. These findings suggest that detectable states may provide an endogenous context for object processing, independently of experimental parameters.

Neocortical modulation of the amygdala response to fearful stimuli

Background The cortical circuitry involved in conscious cognitive processes and the subcortical circuitry involved in fear responses have been extensively studied with neuroimaging, but their interactions remain largely unexplored. A recent functional magnetic resonance imaging (fMRI) study demonstrated that the engagement of the right prefrontal cortex during the cognitive evaluation of angry and fearful facial expressions is associated with an attenuation of the response of the amygdala to these same stimuli, providing evidence for a functional neural network for emotional regulation. Methods In the current study, we have explored the generalizability of this functional network by using threatening and fearful non-face stimuli derived from the International Affective Picture System (IAPS), as well as the influence of this network on peripheral autonomic responses. Results Similar to the earlier findings with facial expressions, blood oxygen level dependent fMRI revealed that whereas perceptual processing of IAPS stimuli was associated with a bilateral amygdala response, cognitive evaluation of these same stimuli was associated with attenuation of this amygdala response and a correlated increase in response of the right prefrontal cortex and the anterior cingulate cortex. Moreover, this pattern was reflected in changes in skin conductance. Conclusions The current results further implicate the importance of neocortical regions, including the prefrontal and anterior cingulate cortices, in regulating emotional responses mediated by the amygdala through conscious evaluation and appraisal.

Recognition of emotion from inverted schematic drawings of faces.

The present study investigated whether facial expressions of emotion are recognized holistically, i.e., all at once as an entire unit, as faces are or featurally as other nonface stimuli. Evidence for holistic processing of faces comes from a reliable decrement in recognition performance when faces are presented inverted rather than upright. If emotion is recognized holistically, then recognition of facial expressions of emotion should be impaired by inversion. To test this, participants were shown schematic drawings of faces showing one of six emotions (surprise, sadness, anger, happiness, disgust, and fear) in either an upright or inverted orientation and were asked to indicate the emotion depicted. Participants were more accurate in the upright than in the inverted orientation, providing evidence in support of holistic recognition of facial emotion. Because recognition of facial expressions of emotion is important in social relationships, this research may have implications for treatment of some social disorders.

RECOGNITION OF EMOTION FROM INVERTED SCHEMATIC DRAWINGS OF FACES

The present study investigated whether facial expressions of emotion are recognized holistically, i.e., all at once as an entire unit, as faces are or featurally as other nonface stimuli. Evidence for holistic processing of faces comes from a reliable decrement in recognition performance when faces are presented inverted rather than upright. If emotion is recognized holistically, then recognition of facial expressions of emotion should be impaired by inversion. To test this, participants were shown schematic drawings of faces showing one of six emotions (surprise, sadness, anger, happiness, disgust, and fear) in either an upright or inverted orientation and were asked to indicate the emotion depicted. Participants were more accurate in the upright than in the inverted orientation, providing evidence in support of holistic recognition of facial emotion. Because recognition of facial expressions of emotion is important in social relationships, this research may have implications for treatment of some social disorders.

The processing of emotional facial expression is gated by spatial attention: evidence from event-related brain potentials

To investigate whether the processing of faces and emotional facial expression can be modulated by spatial attention, ERPs were recorded in response to stimulus arrays containing two faces and two non-face stimuli (houses). In separate trials, attention was focused on the face pair or on the house pair, and facial expression was either fearful or neutral. When faces were attended, a greater frontal positivity in response to arrays containing fearful faces was obtained, starting about 100 ms after stimulus onset. In contrast, with faces located outside the attentional focus, this emotional expression effect was completely eliminated. This differential result demonstrates for the first time a strong attentional gating of brain processes involved in the analysis of emotional facial expression. It is argued that while an initial detection of emotionally relevant events mediated by the amygdala may occur pre-attentively, subsequent stages of emotional processing require focal spatial attention. The face-sensitive N170 component was unaffected by emotional facial expression, but N170 amplitudes were enhanced when faces were attended, suggesting that spatial attention can modulate the structural encoding of faces.

Non-spatial attentional effects on P1.

It has been suggested that P1, the earliest endogenous visual potential, is influenced primarily by spatial location. However, we have found that attention to non-spatial visual features can affect both the latency and amplitude of this component. A series of studies are reviewed, starting with 4 using simple geometric forms, and either serial presentation of single stimuli or presentation of stimulus arrays followed by two studies using natural complex images. With simple stimuli, latency and amplitude effects are seen on the P1, but differ among the paradigms, depending on the demands of the task. The data further showed a facilitation effect and that binding occurs in parallel with single feature processing. For complex stimuli we found P1 shorter to faces than inverted faces, eyes or non-face stimuli, and larger to animal than non-animal pictures. The above effects were present in children as well as in adults. These findings demonstrate that very early stages of processing can be modified by top-down attentional influences across a range of ages and experimental paradigms, concordant with visual processing models showing very rapid and dispersed activation with feedback at early cortical levels.

Analysis of the Neuronal Selectivity Underlying Low fMRI Signals

Background: A prevailing assumption in neuroimaging studies is that relatively low fMRI signals are due to weak neuronal activation, and, therefore, they are commonly ignored. However, lower fMRI signals may also result from intense activation by highly selective, albeit small, subsets of neurons in the imaged voxel. We report on an approach that could form a basis for resolving this ambiguity imposed by the low (mm range) spatial resolution of fMRI. Our approach employs fMR-adaptation as an indicator for highly active neuronal populations even when the measured fMRI signal is low.Results: In this study, we first showed that fMRI-adaptation is diminished when overall neuronal activity is lowered substantially by reducing image contrast. We then applied the same adaptation paradigm, but this time we lowered the fMRI signal by changing object shape. While the overall fMRI signal in category-related regions such as the face-related pFs was drastically reduced for non-face stimuli, the adaptation level obtained for these stimuli remained high. We hypothesize that the relatively greater adaptation level following exposure to “nonoptimal” object shapes is indicative of small subsets of neurons responding vigorously to these “nonoptimal” objects even when the overall fMRI activity is low.Conclusions: Our results show that fMR-adaptation can be used to differentiate between neuronal activation patterns that appear similar in the overall fMRI signal. The results suggest that it may be possible to employ fMR-adaptation to reveal functionally heterogeneous islands of activity, which are too small to image using conventional imaging methods.

Processing of facial and non‐facial visual stimuli in 2–5‐year‐old children

AbstractThe present experiments examined the degree to which analytic and holistic modes of processing play a role in the way 2–5‐year‐old children process facial and non‐facial visual stimuli. Children between 2 and 5 years of age were instructed to categorize faces (in Experiment 1) and non‐facial visual stimuli, such as birds and planes (in Experiment 2), into two categories. The categories were so constructed as to allow the children to categorize the facial and non‐facial stimuli either analytically (by focusing on a single attribute) or holistically (in terms of overall similarity). The results demonstrated that the previous conclusions concerning older children's (from 6 years onwards) holistic mode of facial processing could not be generalized to younger children because most of the 2–5‐year olds processed the faces by taking single facial attributes into account. A similar pattern of results emerged for the processing of objects, showing that the majority of the children focused on single attributes. Thus, for both visual domains, holistic processing was the exception rather than the rule. Copyright © 2002 John Wiley & Sons, Ltd.

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.

Attention to emotion modulates fMRI activity in human right superior temporal sulcus

A parallel neural network has been proposed for processing various types of information conveyed by faces including emotion. Using functional magnetic resonance imaging (fMRI), we tested the effect of the explicit attention to the emotional expression of the faces on the neuronal activity of the face-responsive regions. Delayed match to sample procedure was adopted. Subjects were required to match the visually presented pictures with regard to the contour of the face pictures, facial identity, and emotional expressions by valence (happy and fearful expressions) and arousal (fearful and sad expressions). Contour matching of the non-face scrambled pictures was used as a control condition. The face-responsive regions that responded more to faces than to non-face stimuli were the bilateral lateral fusiform gyrus (LFG), the right superior temporal sulcus (STS), and the bilateral intraparietal sulcus (IPS). In these regions, general attention to the face enhanced the activities of the bilateral LFG, the right STS, and the left IPS compared with attention to the contour of the facial image. Selective attention to facial emotion specifically enhanced the activity of the right STS compared with attention to the face per se. The results suggest that the right STS region plays a special role in facial emotion recognition within distributed face-processing systems. This finding may support the notion that the STS is involved in social perception.

Functional delineation of the human occipito-temporal areas related to face and scene processing. A PET study.

By measuring regional cerebral blood flow using PET, we delineated the roles of the occipito-temporal regions activated by faces and scenes. We asked right-handed normal subjects to perform three tasks using facial images as visual stimuli: in the face familiar/unfamiliar discrimination (FF) task, they discriminated the faces of their friends and associates from unfamiliar ones; in the face direction discrimination (FD) task, they discriminated the direction of each unfamiliar face; in the dot location discrimination (DL) task, they discriminated the location of a red dot on a scrambled face. The activity in each task was compared with that in the control fixation (CF) task, in which they fixated on the centre of a display without visual stimuli. The DL task activated the occipital cortices and posterior fusiform gyri bilaterally. During the FD task, the activation extended anteriorly in the right fusiform gyrus and laterally to the right inferior temporal cortex. The FF task further activated the right temporal pole. To examine whether the activation due to faces was face-specific, we used a scene familiar/unfamiliar discrimination (SF) task, in which the subjects discriminated familiar scenes from unfamiliar ones. Our results suggest that (i) the occipital cortices and posterior fusiform gyri non-selectively respond to faces, scrambled faces and scenes, and are involved mainly in the extraction of physical features of complex visual images; (ii) the right inferior temporal/fusiform gyrus responds selectively to faces but not to non-face stimuli and is involved in the visual processing related to face perception, whereas the bilateral parahippocampal gyri and parieto-occipital junctions respond selectively to scenes and are involved in processing related to scene perception; and (iii) the right temporal pole is activated during the discrimination of familiar faces and scenes from unfamiliar ones, and is probably involved in the recognition of familiar objects.

Domain specificity in face perception.

Is face perception carried out by modules specialized only for processing faces? Or are faces perceived by domain-general mechanisms that can also operate on non-face stimuli? Considerable evidence supports the domain-specific view.

The face-specific N170 component reflects late stages in the structural encoding of faces.

To investigate which stages in the structural encoding of faces are reflected by the face-specific N170 component, ERPs (event-related brain potentials) were recorded in response to different types of face and non-face stimuli. The N170 was strongly attenuated for cheek and back views of faces relative to front and profile views, demonstrating that it is not merely triggered by head detection. Attenuated and delayed N170 components were elicited for faces lacking internal features as well as for faces without external features, suggesting that it is not exclusively sensitive to salient internal features. It is suggested that the N170 is linked to late stages of structural encoding, where representations of global face configurations are generated in order to be utilised by subsequent face recognition processes.

The selectivity of the occipitotemporal M170 for faces.

Evidence from fMRI, ERPs and intracranial recordings suggests the existence of face-specific mechanisms in the primate occipitotemporal cortex. The present study used a 64-channel MEG system to monitor neural activity while normal subjects viewed a sequence of grayscale photographs of a variety of unfamiliar faces and non-face stimuli. In 14 of 15 subjects, face stimuli evoked a larger response than non-face stimuli at a latency of 160 ms after stimulus onset at bilateral occipitotemporal sensors. Inverted face stimuli elicited responses that were no different in amplitude but 13 ms later in latency than upright faces. The profile of this M170 response across stimulus conditions is largely consistent with prior results using scalp and subdural ERPs.

ATTENTIONAL MODULATIONS OF EVENT-RELATED BRAIN POTENTIALS SENSITIVE TO FACES

Event-related brain potentials (ERPs) were recorded in response to centrally and peripherally presented faces and chairs under conditions where one stimulus category was attended and the other unattended. It was studied whether selective attention affects ERP components sensitive to the presence of faces. When compared with chairs, faces elicited larger N1 amplitudes at lateral temporal electrodes and a midline positivity in the same latency range. The latter effect was only found for central faces. Attention to centrally presented faces was reflected in enhanced posterior N1 amplitudes. This effect may be related to an attentional modulation of processing within face-specific brain areas. It was not elicited by chairs or peripheral faces. Beyond 200msec post-stimulus, a category-unspecific attentional negativity was found at all recording sites for centrally and peripherally presented face and nonface stimuli.

THE COGNITIVE NEUROSCIENCE OF FACE PROCESSING: AN INTRODUCTION

Faces are extraordinarily rich sources of information. From one glance, you can determine the person’s age and sex. You know where he or she is looking. You can read mood. If the person is familiar, you know who it is. For most of us, faces are a unique class of visual stimulus: What else do we look at more often or care about more deeply? The very fact that faces have been so special to us and to our primate ancestors makes them a fascinating test case for many of the central questions in cognitive neuroscience. To what extent does visual cognition rely on domain-specific processing mechanisms? How do these specialised cognitive mechanisms arise? How autonomous are they, and how do they interact with other cognitive systems? The centrality of faces in our lives, however, poses a thorny problem for researchers. What visual stimuli can serve as adequate controls, matched for interest, biological relevance, and visual expertise? Few investigators would disagree that faces are visually special, but it’s not easy to discover exactly how and why they are unique. Not easy, but worth the effort. Exploiting the gamut of techniques from cognitive neuroscience, research on face processing is now making substantial progress. The articles in the present issue use single-unit recording, event-related potentials (ERPS), fMRI, cortical microstimulation, and behavioural testing of patients with brain damage. These studies, together with recent related studies published elsewhere, have helped us gain traction on the long-standing questions of how faces are perceived, how their processing differs from that of nonface stimuli, and how the interaction of evolutionary and experiential forces has produced a neural mechanism that still outperforms the best computer vision algorithms. Here we synopsise the main advances that have been made by the research reported in this volume.

Face up to the fusiform gyrus

The fundamental question of whether the visual processes underlying the recognition of human faces are unique, in contrast to other complex visual stimuli, has been intensely studied. To examine this issue, neuroimaging, physiological and behavioral studies often focus on the ventral occipitotemporal pathway; in particular, a region in the fusiform gyrus known as the fusiform face area (FFA). Significant results from such studies suggest that this region is specialized for the perception of human faces. In a recent neuroimaging study Kanwisher et al. report data supporting the existence of a human FFA that is selective for face processing 1 Kanwisher N. et al. The fusiform face area is selective for faces not animals. NeuroReport. 1999; 10: 183-187 Crossref PubMed Scopus (200) Google Scholar . The authors used eight different stimuli and recorded the strongest FFA response when subjects viewed human faces rather than control stimuli of human heads, whole humans or animal heads. Although the FFA responded to stimuli other than human faces, the responses were dominated by face stimuli rather than non-face stimuli. These results suggest a specialized face-processing region, whilst not ruling out the discovery of other face-responsive areas. While significant progress has been made in understanding specific aspects of face-recognition, a comprehensive understanding of just how ‘special’ this process is still eludes us.

Face Perception During Early Infancy

Previous studies of face perception during early infancy are difficult to interpret because of discrepant results and procedural differences. We used a standardized method based on the Teller acuity card procedure to test newborns, 6-week-olds, and 12-week-olds with three pairs of face and nonface stimuli modified from previous studies. Newborns' preferences were influenced both by the visibility of the stimuli and by their resemblance to a human face. There appears to be a mechanism, likely subcortical, predisposing newborns to look toward faces. Changes in preferences at 6 and 12 weeks of age suggest increasing cortical influence over infants' preferences for faces.

Electrophysiological studies of human face perception. I: Potentials generated in occipitotemporal cortex by face and non-face stimuli.

This and the following two papers describe event-related potentials (ERPs) evoked by visual stimuli in 98 patients in whom electrodes were placed directly upon the cortical surface to monitor medically intractable seizures. Patients viewed pictures of faces, scrambled faces, letter-strings, number-strings, and animate and inanimate objects. This paper describes ERPs generated in striate and peristriate cortex, evoked by faces, and evoked by sinusoidal gratings, objects and letter-strings. Short-latency ERPs generated in striate and peristriate cortex were sensitive to elementary stimulus features such as luminance. Three types of face-specific ERPs were found: (i) a surface-negative potential with a peak latency of approximately 200 ms (N200) recorded from ventral occipitotemporal cortex, (ii) a lateral surface N200 recorded primarily from the middle temporal gyrus, and (iii) a late positive potential (P350) recorded from posterior ventral occipitotemporal, posterior lateral temporal and anterior ventral temporal cortex. Face-specific N200s were preceded by P150 and followed by P290 and N700 ERPs. N200 reflects initial face-specific processing, while P290, N700 and P350 reflect later face processing at or near N200 sites and in anterior ventral temporal cortex. Face-specific N200 amplitude was not significantly different in males and females, in the normal and abnormal hemisphere, or in the right and left hemisphere. However, cortical patches generating ventral face-specific N200s were larger in the right hemisphere. Other cortical patches in the same region of extrastriate cortex generated grating-sensitive N180s and object-specific or letter-string-specific N200s, suggesting that the human ventral object recognition system is segregated into functionally discrete regions.

Face-selective neurons during passive viewing and working memory performance of rhesus monkeys: evidence for intrinsic specialization of neuronal coding.

The functional organization of prefrontal cortex (PFC) is a central issue in cognitive neuroscience. Previous physiological investigations have often failed to reveal specialization within the PFC. However, these studies have generally not been designed to examine this issue. Methodological issues such as statistical criteria for specificity, the number of neurons sampled, the extent of cortex sampled, and the number, location and nature of the stimuli used are among the variables that need to be considered in evaluating the results of studies on functional localization. In the present study, we have examined neurons in macaque monkeys trained to fixate while viewing visual stimuli, including faces, or to use them as memoranda on a working memory task. Visual responses of over 1500 neurons were recorded throughout a wide expanse of the PFC (areas 12, 9, 46, 8 and 45). Neurons were considered selective for faces if the best response to a face was over twice as strong as that to any of a wide variety of non-face stimuli. Full electrode track reconstructions in three monkeys revealed in each that neurons which met this criterion were concentrated almost exclusively in three distinct subregions within the projection region of the temporal lobe visual areas. We further show that for all neurons, the most visually selective neurons (for faces, objects or color patterns) were also the most concentrated in the temporal lobe recipient PFC. Similar face selectivity, regional specialization, and delay or delay-like activity were observed in monkeys whether trained on memory tasks or not, which suggests that these are naturally occurring properties of prefrontal neurons. These results confirm neuronal and regional specialization for information processing in PFC and elucidate how heretofore unexamined experimental variables have a strong influence on the detection of regional specialization.