Edited by: Stefania D'Ascenzo, University of Modena and Reggio Emilia, Italy
Reviewed by: David Melcher, The Center for Mind/Brain Sciences (CIMeC), Italy; Maximilian Bruchmann, University of Münster, Germany
*Correspondence: Márta Zimmer
Gyula Kovács
This article was submitted to Perception Science, a section of the journal Frontiers in Psychology
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Several studies demonstrated that face perception is biased by the prior presentation of another face, a phenomenon termed as face-related after-effect (FAE). FAE is linked to a neural signal-reduction at occipito-temporal areas and it can be observed in the amplitude modulation of the early event-related potential (ERP) components. Recently, macaque single-cell recording studies suggested that manipulating the duration of the adaptor makes the selective adaptation of different visual motion processing steps possible. To date, however, only a few studies tested the effects of adaptor duration on the electrophysiological correlates of human face processing directly. The goal of the current study was to test the effect of adaptor duration on the image-, identity-, and generic category-specific face processing steps. To this end, in a two-alternative forced choice familiarity decision task we used five adaptor durations (ranging from 200–5000 ms) and four adaptor categories: adaptor and test were identical images—Repetition Suppression (RS); adaptor and test were different images of the Same Identity (SameID); adaptor and test images depicted Different Identities (DiffID); the adaptor was a Fourier phase-randomized image (No). Behaviorally, a strong priming effect was observed in both accuracy and response times for RS compared with both DiffID and No. The electrophysiological results suggest that rapid adaptation leads to a category-specific modulation of P100, N170, and N250. In addition, both identity and image-specific processes affected the N250 component during rapid adaptation. On the other hand, prolonged (5000 ms) adaptation enhanced, and extended category-specific adaptation processes over all tested ERP components. Additionally, prolonged adaptation led to the emergence of image-, and identity-specific modulations on the N170 and P2 components as well. In other words, there was a clear dissociation among category, identity-, and image-specific processing steps in the case of longer (3500 and 5000 ms) but not for shorter durations (< 3500 ms), reflected in the gradual reduction of N170 and enhancement of P2 in the No, DiffID, SameID, and RS conditions. Our findings imply that by manipulating adaptation duration one can dissociate the various steps of human face processing, reflected in the ERP response.
The ability of the visual system to rapidly adjust to changing environmental conditions is one of its key characteristics (Mesik et al.,
Regarding human face perception, electrophysiological studies have described a large, early positive (P1 or P100) and a negative (N170) wave over the occipito-temporal areas (Bentin et al.,
The electrophysiological correlates of facial after-effects have been reported as early as 140–200 ms post-stimulus onset (in the time window of the N170 component). Following the initial study of Kovács et al. (
To the best of our knowledge, so far the only study testing priming and adaptation simultaneously within a single paradigm is a study by Walther et al. (
One of the important parameters affecting the mechanisms of adaptation is its timescale and this can be tested by either the manipulation of the exposition time of the adaptor or by using different adaptor-test image inter-stimulus intervals (ISIs). Determining how adaptation duration influences changes in neuronal response properties is central to the understanding whether the sensory system employs different strategies for adjusting its sensitivity on the different timescales (Patterson et al.,
In the present study, we systematically manipulated the duration of adaptation in the commonly applied range of 200–5000 ms with different facial adaptation conditions. In a 2AFC familiarity decision task we used three different face adaptors: different identity (DiffID), different image of the same identity (SameID), and identical image of the same person (repetition suppression, RS). A Fourier phase-randomized noise image served as control (No). By using these conditions we intended to separate three major steps of face processing. The GENERIC, face category specific processes were isolated by the comparison of noise adaptation (No) with the adaptation to a face that is unrelated to the test stimulus identity (DiffID). IDENTITY-SPECIFIC effects were tested by the DiffID vs. SameID comparison while IMAGE-SPECIFIC effects were measured by the SameID vs. RS comparison. We hypothesized that by varying the duration of adaptation time, we might dissociate generic-, identity-, and image-based information processing, reflected on the face-evoked ERP components.
Sixteen naïve healthy-volunteers (15 right-handed and one ambidextrous, six females, mean age = 22.69 years, ± 4.83 years SD) participated in the study. They received partial course credits for their participation and gave signed, informed consent in accordance with the Ethical Committee of the Budapest University of Technology and Economics prior to testing. All participants had normal or corrected-to-normal visual acuity, no previous history of any neurological or ophthalmological diseases and were not under any medication. One additional participant was excluded from the behavioral and electrophysiological analysis (right-handed 22 years old male) due to an insufficient number of recognized familiar faces and a high number of recognized unfamiliar faces, which was evident in the post-testing questionnaire.
Grayscale images of familiar and unfamiliar faces were used, with sixteen different identities (eight female) for each category. Familiar faces were digital images of famous persons, ranging from Hollywood celebrities to politicians that Hungarian students were likely to recognize, whereas unfamiliar faces were digital images of less-known persons that were unlikely to be recognized by the participants (such as Finnish politicians or actresses from Iceland). Two different images portraying the same person were used for each identity, corresponding to a number of 32 images in total. All images were downloaded from freely available websites and converted into grayscale (8 bit) using Adobe Photoshop CS3 Extended 10.0 (Adobe Systems Inc.). Images were then cropped to reveal only the contour of the face, including hair. Stimuli subtended 3.6 × 5° of visual angle. Since previous studies have shown that early ERP components, such as P100, are sensitive to luminance (Johannes et al.,
Three different images were used as adaptors: an image that was identical to the test stimulus [repetition suppression (RS) condition], a different image depicting the same identity as the test stimulus [same identity (SameID) condition], and an image depicting a same gender different identity than the test stimulus [different identity (DiffID) condition]. For the control condition, sixteen Fourier phase-randomized images were created from the face images and used as adaptors [non-adapted (No) condition].
Stimuli were presented centrally on a uniform gray background. An LG Flatron W2600 HP monitor (resolution: 1920 × 1200 pixels, refresh rate: 60 Hz) was used for stimulus presentation, while viewing distance (57 cm) was maintained constant using a chinrest. Stimulus presentation was controlled using MATLAB 2008a Psychtoolbox 3.0.9 (Brainard,
Subjects were instructed to perform a two-alternative forced-choice (2AFC) familiarity task for faces by pressing the key labeled “7” on a keyboard when the second, target face was perceived as familiar and the key labeled “8” when it was perceived as unfamiliar. A yellow fixation cross presented in the center of the screen indicated the presence of the target stimulus to the subject. Prior to the presentation of the target, a gray screen was presented for a random period of time between 500 and 700 ms, followed by the adaptor image. The duration of the adaptor image varied randomly between one of five values: 200, 1200, 2000, 3500, and 5000 ms. The adaptor was followed by a 500 ms gray screen after which the target stimulus appeared for 200 ms (Figure
At the end of the session participants had to answer a questionnaire that verified their familiarity with the identities used in the experiment. The questionnaire consisted of presenting each previously presented person and asking the participants to identify the familiar ones by naming them (or at least giving some correct information about them, such as occupation and nationality). In case the subject did not recognize one or more of the faces belonging to the familiar category or recognized faces belonging to the unfamiliar category, the trials containing those identities were removed from the statistical analysis for both behavioral and electrophysiological data. From the 32 faces on average 2.56 ± 2.25 faces were excluded from further analyses across participants.
Accuracy and response times (RTs) were recorded during the experiment. In the case of accuracy, we calculated d′-values that were analyzed with a 4 × 5 repeated measures ANOVA with adaptor category (4; No, RS, SameID, DiffID) and adaptor duration (5; 200, 1200, 2000, 3500, 5000) as within-subject factors. RTs were analyzed with a 2 × 4 × 5 repeated measures ANOVA with familiarity (2; familiarity: F vs. UF), adaptor category (4; No, RS, SameID, DiffID) and adaptor duration (5; 200, 1200, 2000, 3500, 5000 ms) as within-subject factors. All analyses involved Greenhouse—Geisser adjusted degrees of freedom for correction for non-sphericity.
Electroencephalography (EEG) data was recorded using a Brain-Amp (BrainProducts GmbH, Munich, Germany) amplifier from 60 Ag/AgCl scalp electrodes placed according to the international 10/10 electrode system (Chatrian et al.,
EEG data were analyzed using Brain Vision Analyzer 1.05.0002 (BrainProducts GmbH., Munich, Germany). After correcting ocular movement artifacts and digitally re-referencing to a common average, the EEG was segmented offline into 700 ms long epochs starting 100 ms prior to target stimulus onset and ending 600 ms after target stimulus onset. DC trend correction was applied, and a semi-automatic artifact rejection was implemented. Segments containing blinks, movement artifacts, and baseline drifts were rejected on the basis of visual inspection. After cleaning the EEG data, ~87% of the trials remained available for further analysis. It is worth noting, however, that the reason of removing a given segment in most cases (8% from the 13% removed trials) was that the familiarity of the given person was misjudged by the subject. EEG epochs were averaged separately for each condition and participant. Averages were band-pass filtered (Butterworth zero phase filter; 0.1–30 Hz; slope: 12 dB/oct) and baseline corrected using a 100 ms pre-stimulus baseline. The peak amplitude and latency of the individually averaged ERPs were extracted using a semiautomatic detection algorithm that identified the global maxima separately for each selected channels in a specific time window as follows. P100 was defined as a main positive deflection in the 80–130 ms time window, whereas the N170 was defined as a negative component in the 135–190 ms time interval. P2 was the second positive component in the 195–250 ms time window, while N250 was defined as the second negative component at around 230–330 ms.
P100 amplitude was measured over O1 (left hemisphere, LH) and O2 (right hemisphere, RH) electrode positions (Herrmann et al.,
In addition, we defined three different types of effects: ADAGENERIC as referred to the No vs. DiffID comparison; ADAIDENTITY as referred to the SameID vs. DiffID comparison; and ADAIMAGE as referred to the SameID vs. RS comparison. The magnitudes of electrophysiological adaptation effects were defined as the absolute value of the differences in amplitude that were calculated by subtracting the P100, N170, P2, and N250 amplitudes obtained during the relevant two adapted conditions. After all, we tested whether the different types of adaptations modify the ERP components differently. Therefore, a Four-way repeated-measures ANOVA was conducted on the electrophysiological adaptation indices with adaptation effect (3; ADAGENERIC, ADAIDENTITY, ADAIMAGE), ERP component (4; P100, N170, P2, N250), hemisphere (2; LH vs. RH), and duration (5; 200, 1200, 2000, 3500, 5000 ms) as within-subject factors. A Greenhouse—Geisser correction was applied to correct for violations of sphericity, while
We observed a main effect of adaptation CONDITION on the d′-values of the behavioral performance [
A main effect of CONDITION was observed [
In the subsequent ERP Results Section, we only focus on the three above-mentioned adaptation effects (GENERIC, IDENTITY-SPECIF, and IMAGE-SPECIFIC EFFECTS) and therefore we only discuss the main effects of CONDITION and DURATION, and the significant CONDITION × DURATION interactions in details. Any other significant main effects and interactions are presented in Tables
COND | ||||
No < SameID |
No > SameID |
No < SameID |
No < RS |
|
No < RS |
No > RS |
No < RS |
DiffID < RS |
|
DiffID > RS |
Diff < RS |
|||
HEM | ||||
RH dominance | RH dominance | RH dominance | strong tendency for LH dominance | |
FAM | n.s. | n.s. | ||
larger for unfamiliar faces | larger for familiar faces |
COND × DUR | n.s. | n.s. | ||
No vs. SameID all |
No vs. SameID all |
|||
No vs. RS all |
No vs. RS all |
|||
DiffID vs. RS all |
DiffID vs. RS all |
|||
COND × FAMIL | n.s. | n.s. | n.s. | |
COND × HEM | n.s. | |||
COND × DUR × HEM | n.s. | n.s. | n.s. | |
No vs. SameID |
||||
No vs. RS all |
||||
DiffID vs. RS all |
Significant GENERIC EFFECT was observed suggested by the larger P100 amplitude values in the DiffID condition when compared with the control (No) (main effect of CONDITION:
The N170 showed a significant main effect of CONDITION [
These results suggest that the N170 adaptation effects strongly depend on the adaptation duration: while for short adaptation durations the N170 reflects only generic, category specific effects, prolonging the adaptation duration leads to the emergence of identity and image specific adaptation effects as well.
Although there was a strong tendency for both GENERIC EFFECT (namely larger P2s in the case of DiffID when compared with No,
Supporting prior studies of N250r (Schweinberger et al.,
By running an analysis based on different types of adaptation effects, we suggest that altogether larger adaptation effects were observed for GENERIC when compared with IDENTITY-SPECIFIC adaptation [main effect of ADAPTATION EFFECT:
The goal of the present work was to study the behavioral and electrophysiological effects of systematically varying adaptation duration and whether this variation leads to a differentiation between the various stages of face processing, such as the generic category coding vs. processing of identity and image specific information. By using a large range of adaptation times we expected to find a differentiation between generic-, identity-, and image-specific processes.
The behavioral results indicated a better performance and faster decisions for the SameID and RS conditions when compared with the DiffID condition, corresponding to a strong priming effect in these cases (Ellis et al.,
In the case of the P100 component, larger amplitudes were observed for all face-adapted conditions when compared with control (No) and the main effect of condition suggests a generic adaptation effect (ADAGENERIC) already at this level. This general signal enhancement is in line with our previous findings (Kovács et al.,
All face adapted conditions caused a signal reduction of the N170 component when compared with noise adaptation (No). This general effect might be related to face detection and can be observed already after the shortest adaptation duration (200 ms). Recently, Feuerriegel et al. (
Regarding the P2 component, in the case of the shortest duration, there was no significant difference between conditions. However, as adaptation duration reached 1200 ms a step-by-step differentiation was found among No, DiffID, SameID, and RS conditions in an ascending manner for both hemispheres. This means that for adaptation durations longer than ~1000 ms the P2 component reflected generic, identity-specific and image-specific effects as well. Whereas the P100 and N170 components are clearly linked to special and well-defined stages of face processing, this does not seem to hold for P2. Some studies linked this component to task difficulty (Philiastides et al.,
Regarding N250, not surprisingly, familiar faces evoked larger N250s, supporting prior results (Begleiter et al.,
Our results show that on the one hand, the observed face-evoked ERP components reflect generic, identity-specific, and image-specific adaptation effects that are modulated by adaptation duration in a way that in the case of the shortest duration (commonly applied in rapid adaptation paradigms) only the earlier P100 and N170 components reflect generic adaptation effects (for summary see our model on Figure
In conclusion, the current study is the first to investigate the relationship between systematically varying the adaptor duration in a broad range and the behavioral and electrophysiological responses elicited by the test stimuli after adapting different processing stages. Our results suggest that after long-term adaptation generic, identity-specific, and image-specific effects are reflected equally and earlier on the ERP components when compared to short-term adaptation conditions. In the case of rapid adaptation, these effects are delayed and can be observed only on the N250 component. Altogether we can summarize the consequences of our findings as follows: (1) While prior results rather suggested a sequential processing of faces, starting with a generic face categorization at about 150 ms (within the time-window of the N170 component), and identification/recognition being associated with three later components at around 250 ms (within the time-window of the N250 component), ours is the first study that clearly shows that with long-term adaptation these processes can all be observed from early components onwards and they are parallel to each other. (2) Our results suggest that in order to see the identity-specific processing steps completely, one needs to apply several seconds-long adaptation. (3) Our results also support those single-cell recording studies that suggest that short- and long-term adaptation have entirely different neural mechanisms (Priebe et al.,
Designed the experiment: MZ, KN, GK; data acquisition: MZ, AZ, KN; data analyses: MZ, AZ, GK; interpretation of the data: MZ, AZ, GK; provided materials: MZ, AZ, KN, GK; wrote the article: MZ, AZ, GK; proofed/revised the article: MZ, AZ, KN, GK.
This work was supported by a Deutsche Forschungsgemeinschaft Grant (KO 3918/1-2; 2-1).
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
We thank Dorottya Bencze for her help in running the experiments.