Meike Ramon

Fixation patterns during recognition of personally familiar and unfamiliar faces

Previous studies recording eye gaze during face perception have rendered somewhat inconclusive findings with respect to fixation differences between familiar and unfamiliar faces. This can be attributed to a number of factors that differ across studies: the type and extent of familiarity with the faces presented, the definition of areas of interest subject to analyses, as well as a lack of consideration for the time course of scan patterns. Here we sought to address these issues by recording fixations in a recognition task with personally familiar and unfamiliar faces. After a first common fixation on a central superior location of the face in between features, suggesting initial holistic encoding, and a subsequent left eye bias, local features were focused and explored more for familiar than unfamiliar faces. Although the number of fixations did not differ for un-/familiar faces, the locations of fixations began to differ before familiarity decisions were provided. This suggests that in the context of familiarity decisions without time constraints, differences in processing familiar and unfamiliar faces arise relatively early – immediately upon initiation of the first fixation to identity-specific information – and that the local features of familiar faces are processed more than those of unfamiliar faces.

Early adaptation to repeated unfamiliar faces across viewpoint changes in the right hemisphere : evidence from the N170 ERP component

Event-related potential (ERP) studies have shown that sensitivity to individual faces emerges as early as approximately 160ms in the human occipitotemporal cortex (N170). Here we tested whether this effect generalizes across changes in viewpoint. We recorded ERPs during an unfamiliar individual face adaptation paradigm. Participants were presented first with an adapting face ( approximately 3000ms) rotated 30 degrees in depth, followed by a second face (200ms) in a frontal view of either the same or a different identity. The N170 amplitude at right occipitotemporal sites to the second stimulus was reduced for repeated as compared to different faces. A bilateral adaptation effect emerged after 250ms following stimulus onset. These observations indicate that individual face representations activated as early as 160ms after stimulus onset in the right hemisphere show a substantial degree of generalization across viewpoints.

Impaired holistic processing of unfamiliar individual faces in acquired prosopagnosia.

Prosopagnosia is an impairment at individualizing faces that classically follows brain damage. Several studies have reported observations supporting an impairment of holistic/configural face processing in acquired prosopagnosia. However, this issue may require more compelling evidence as the cases reported were generally patients suffering from integrative visual agnosia, and the sensitivity of the paradigms used to measure holistic/configural face processing in normal individuals remains unclear. Here we tested a well-characterized case of acquired prosopagnosia (PS) with no object recognition impairment, in five behavioral experiments (whole/part and composite face paradigms with unfamiliar faces). In all experiments, for normal observers we found that processing of a given facial feature was affected by the location and identity of the other features in a whole face configuration. In contrast, the patients results over these experiments indicate that she encodes local facial information independently of the other features embedded in the whole facial context. These observations and a survey of the literature indicate that abnormal holistic processing of the individual face may be a characteristic hallmark of prosopagnosia following brain damage, perhaps with various degrees of severity.

Reduced fixation on the upper area of personally familiar faces following acquired prosopagnosia

Selective impairment of face recognition following brain damage, as in acquired prosopagnosia, may cause a dramatic loss of diagnosticity of the eye area of the face and an increased reliance on the mouth for identification (Caldara et al., 2005). To clarify the nature of this phenomenon, we measured eye fixation patterns in a case of pure prosopagnosia (PS, Rossion et al., 2003) during her identification of photographs of personally familiar faces (27 children of her kindergarten). Her age-matched colleague served as a control. Consistent with previous evidence, the normal control identified the faces within two fixations located just below the eyes (central upper nose). This pattern (location and duration) of fixations remained unchanged even by increasing difficulty by presenting anti-caricatures of the faces. In contrast, the great majority of the patients fixations, irrespective of her accuracy, were located on the mouth. Overall, these observations confirm the abnormally reduced processing of the upper area of the face in acquired prosopagnosia. Most importantly, the prosopagnosic patient also fixated the area of the eyes spontaneously in between the first and last fixation, ruling out alternative accounts of her behaviour such as, for example, avoidance or failure to orient attention to the eyes, as observed in autistic or bilateral amygdala patients. Rather, they reinforce our proposal of a high-level perceptual account (Caldara et al., 2005), according to which acquired prosopagnosic patients have lost the ability to represent multiple elements of an individual face as a perceptual unit (holistic face perception). To identify a given face, they focus very precisely on local features rather than seeing the whole of a face from its diagnostic centre (i.e., just below the eyes). The upper area of the face is particularly less attended to and less relevant for the prosopagnosic patient because it contains multiple features that require normal holistic perception in order to be the most diagnostic region. Consequently, prosopagnosic patients develop a more robust representation of the mouth, a relatively isolated feature in the face that may contain more information than any single element of the upper face area, and is thus sampled repeatedly for resolving ambiguity in the process of identification.

Event‐related potentials reflect heterogeneity of developmental prosopagnosia

Event‐related potential (ERP) studies of developmental prosopagnosia (DP) are rare. Previous ERP investigations have reported smaller N170 amplitude differences between faces and objects in at least three prosopagnosics. The present study is based on a combination of behavioural and electrophysiological assessment of face processing. The aim was to investigate the face‐specifity of the N170 in both healthy subjects and a group of DP individuals (N = 4), using famous and nonfamous faces, caricatures and houses as stimuli. All prosopagnosic subjects showed impairments in recognition of famous faces, memory for faces and learning new faces in behavioural assessment. In healthy subjects the largest effects were found at parieto‐occipital electrode positions (PO7 and PO8), along with a familiarity effect at these electrode positions. Thus, parieto‐occipital areas appear to play an important role in face processing. Three prosopagnosics showed reliable N170 amplitude differences between faces and nonface stimuli, whereas one DP individual showed significantly reduced amplitude differences between faces and nonface objects. The behavioural and electrophysiological data support the idea that DP reflects a heterogeneous impairment and that face processing deficits are not necessarily correlated with a lack of face‐specific N170.

The speed of recognition of personally familiar faces

Despite the generally accepted notion that humans are very good and fast at recognising familiar individuals from their faces, the actual speed with which this fundamental brain function can be achieved remains largely unknown. Here, two groups of participants were required to respond by finger-lift when presented with either a photograph of a personally familiar face (classmate), or an unfamiliar one. This speeded manual go/no-go categorisation task revealed that personally familiar faces could be categorised as early as 380 ms after presentation, about 80 ms faster than unfamiliar faces. When response times were averaged across all 8 stimulus presentations, we found that minimum RTs for both familiar and unfamiliar face decisions were substantially lower (310 ms and 370 ms). Analyses confirmed that stimulus repetition enhanced the speed with which faces were categorised, irrespective of familiarity, and that repetition did not affect the observed benefit in RTS for familiar over unfamiliar faces. These data, representing the elapsed time from stimulus onset to motor output, put constraints on the time course of familiar face recognition in the human brain, which can be tracked more precisely by high temporal resolution electrophysiological measures.

Hemisphere-dependent holistic processing of familiar faces

In two behavioral experiments involving lateralized stimulus presentation, we tested whether one of the most commonly used measures of holistic face processing-the composite face effect-would be more pronounced for stimuli presented to the right as compared to the left hemisphere. In experiment 1, we investigated the composite face effect in a verbal identification task, similar to its original report (Young, Hellawell, & Hay, 1987). Aligning top and bottom halves of composite face stimuli led to performance decreases irrespective of hemifield, indicating holistic processing of comparable magnitude for inputs provided separately to either hemisphere. However, when matching of the same top parts was required in experiment 2, an alignment-dependent performance decrease was found for stimuli presented in the left, but not right visual field. These observations suggest that the right hemisphere dominates in early stages of holistic processing, as indexed by the composite face effect, but that later processes such as face identification and naming are based on unified representations that are independent of input lateralization. Moreover, the composite face effect may not rely on the exact same representation(s) when measured in matching and identification tasks.

Early electrophysiological correlates of adaptation to personally familiar and unfamiliar faces across viewpoint changes

Behavioral studies have shown that matching individual faces across depth rotation is easier and faster for familiar than unfamiliar faces. Here we used event-related potentials (ERPs) to clarify the locus of this behavioral facilitation, that is whether it reflects changes at the level of perceptual face encoding, or rather at later stages of processing. We used an identity adaptation paradigm in ERPs, during which a first (adapting) face (~3000 ms) rotated 30° in depth was followed by a second full front face (200 ms) which was either the same or a different identity as the first face. For unfamiliar faces, the early face-sensitive N170 component was reduced for immediately repeated as compared to different unfamiliar faces in the right hemisphere only. However, for personally familiar faces, the effect was absent at right hemisphere electrode sites and appeared instead over the left hemisphere at the same latency. Later effects of face identity adaptation were also present on the scalp, but from about 300 to 400 ms over fronto-central regions, and slightly later on occipito-temporal regions, there was a strong adaptation effect only for familiar faces. These observations suggest that the perceptual encoding of familiar and unfamiliar faces may be of different nature, as indicated by early (N170) hemispheric differences for identity adaptation effects depending on long-term familiarity. However, the behavioral advantage provided by familiarity to match faces across viewpoints might rather be related to processes that are closer in time to the behavioral response, such as semantic associations between the faces to match.

Face familiarity decisions take 200 msec in the human brain: Electrophysiological evidence from a go/no-go speeded task

Recognizing a familiar face rapidly is a fundamental human brain function. Here we used scalp EEG to determine the minimal time needed to classify a face as personally familiar or unfamiliar. Go (familiar) and no-go (unfamiliar) responses elicited clear differential waveforms from 210 msec onward, this difference being first observed at right occipito-temporal electrode sites. Similar but delayed (by about 40 msec) responses were observed when go response were required to the unfamiliar rather than familiar faces, in a second group of participants. In both groups, a small increase of amplitude was also observed on the right hemisphere N170 face-sensitive component for familiar faces. However, unlike the post-200 msec differential go/no-go effect, this effect was unrelated to behavior and disappeared with repetition of unfamiliar faces. These observations indicate that accumulation of evidence within the first 200 msec poststimulus onset is sufficient for the human brain to decide whether a person is familiar based on his or her face, a time frame that puts strong constraints on the time course of face processing.

Personally familiar faces are perceived categorically in face-selective regions other than the fusiform face area.

Neuroimaging studies of humans have provided inconsistent evidence with respect to the response properties of the fusiform face area (FFA). It has been claimed that neural populations within this region are sensitive to subtle differences between individual faces only when they are perceived as distinct identities [P. Rotshtein et al. (2005)Nature Neuroscience, 8, 107–113]. However, sensitivity to subtle changes of identity was found in previous studies using unfamiliar faces, for which categorical perception is less pronounced. Using functional magnetic resonance adaptation and morph continua of personally familiar faces, we investigated sensitivity to subtle changes between faces that were located either on the same or opposite sides of a categorical perceptual boundary. We found no evidence for categorical perception within the FFA, which exhibited reliable sensitivity to subtle changes of face identity whether these were perceived as distinct identities, or not. On the contrary, both the posterior superior temporal sulcus and prefrontal cortex exhibited categorical perception, as subtle changes between faces perceived as different identities yielded larger release from adaptation than those perceived as the same identity. These observations suggest that, whereas the FFA discriminates subtle physical changes of personally familiar faces, other regions encode faces in a categorical fashion.