Face-identity change activation outside the face system: "release from adaptation" may not always indicate neuronal selectivity

Abstract

Face recognition is a complex cognitive process that requires distinguishable neuronal representations of individual faces. Previous functional magnetic resonance imaging (fMRI) studies using the "fMRI-adaptation" technique have suggested the existence of face-identity representations in face-selective regions, including the fusiform face area (FFA). Here, we present face-identity adaptation findings that are not well explained in terms of face-identity representations. We performed blood-oxygen level-dependent (BOLD) fMRI measurements, while participants viewed familiar faces that were shown repeatedly throughout the experiment. We found decreased activation for repeated faces in face-selective regions, as expected based on previous studies. However, we found similar effects in regions that are not face-selective, including the parahippocampal place area (PPA) and early visual cortex (EVC). These effects were present for exact-image (same view and lighting) as well as different-image (different view and/or lighting) repetition, but more widespread for exact-image repetition. Given the known functional properties of PPA and EVC, it appears unlikely that they contain domain-specific face-identity representations. Alternative interpretations include general attentional effects and carryover of activation from connected regions. These results remind us that fMRI stimulus-change effects can have a range of causes and do not provide conclusive evidence for a neuronal representation of the changed stimulus property.

Figure 1.

Stimuli. (a) Stimuli were male faces seen from 2 different views and with 2 different lightings. The lower left and upper right faces are counterlit (incongruent view and lighting). (b) Averaged histograms for red, green, and blue (RGB) color channels that were imposed on each image. As a consequence of the color histogram equalization, the images have the same light and spatial-signal energy. (c) Face familiarity was systematically varied, resulting in new, seen, and known faces. The 7 new faces that are shown are a subset of a total of 180 new faces that were used in this study. The 4 familiar faces are the 4 right-most faces.

Figure 2.

Reaction times for face-identity change (rep0) were higher than for face-identity repetition. The upper panel shows mean reaction times across subjects and associated error bars (random-effects standard error of the mean) for new faces, face-identity change trials, and face-identity consecutive repetition trials. Values for the rep3, rep4, and rep5 predictors are not shown because these were based on only few trials. Four relevant contrasts (new vs. rep0, rep0 vs. rep1_different (rep1d), rep1_different vs. rep1_exact (rep1e), and rep1_exact vs. rep2) were tested for significance using paired t-tests. Significant contrasts are shown and denoted with **(P < 0.01). The lower panel shows the reaction times of each individual subject for the conditions shown in the upper panel, in order to give a more detailed picture of the between-subject variation.

Figure 3.

Face-identity change (rep0) elicited more activation than face-identity repetition across early visual and posterior inferior temporal cortex (including regions that are not face-selective). Effects were more widespread for exact-image than different-image repetition. (a) Face-identity change (rep0) versus first consecutive different-image face-identity repetition (rep1_different) (FDR < 0.05). (b) Face-identity change (rep0) versus first consecutive exact-image face-identity repetition (rep1_exact). In both panels, fixed-effects group results are displayed on single-subject high-resolution anatomical slices. The position of the measured slab is indicated by transparent masks overlaid on sagittal and coronal slices. Slices along different points on the x-, y-, and z-axes show stronger activation for rep0 than rep1 (orange/yellow) in EVC as well as in inferior temporal regions, overlapping with OFA, FFA, and PPA. More activation for rep1 than rep0 is shown in blue/green. The most superior slice along the z-axis shows activation based on only three-quarters of the data (data with very low slab position were removed).

Figure 4.

ROI analysis for face-identity repetition effects. Face-selective regions (OFA, FFA) as well regions that are not face-selective (EVC, PPA) showed more activation for face-identity change (rep0) than repetition. These regions (including left EVC and PPA) showed these effects for both exact-image and different-image repetition. Approximate ROI locations are shown (in green) on a ventral view of the cortex (shown here: MNI template colin27). Graphs show beta-values and associated standard errors for the new (red), rep0 (i.e. identity change; light blue), rep1_different (blue), rep1_exact (blue gray), and rep2 (dark blue) predictors, averaged across subjects. Values for the rep3, rep4, and rep5 predictors are not shown because these were based on only few trials. Six relevant contrasts (new vs. rep0, rep0 vs. rep1_different, rep0 vs. rep1_exact, rep1_different vs. rep1_exact, rep1_different vs. rep2, and rep1_exact vs. rep2) were tested for significance. The new versus rep0 contrast was significant for all tested regions (P < 0.01) (not shown). The rep1_different versus rep2 contrast was significant for bilateral EVC and right OFA, FFA, and PPA (P < 0.05) (not shown). For the other 4 tested contrasts, significant contrasts are shown and denoted with **(P < 0.01) or *(P < 0.05). ROIs were defined using independent data. See Table 1 for abbreviations and ROI details (including ROI-defining contrasts).

Figure 5.

New faces elicited more activation than seen faces across early visual and inferior temporal cortex (t = |4.36|, associated with FDR < 0.05 for seen-known contrast, not shown). Fixed-effects group results are displayed on single-subject high-resolution anatomical slices. Position of the measured slab is indicated by transparent masks overlaid on sagittal and coronal slices. Slices along different points on the x-, y- and z-axes show stronger activation for new than seen faces (orange/yellow) in EVC as well as in (anterior) inferior temporal regions, including OFA, FFA, PPA, hippocampus, and aIT. There were no regions showing more activation for seen than new faces. Note that the most superior slice along the z-axis shows activation based on only three-quarters of the data (data with very low slab position were removed).

Figure 6.

ROI analysis for face-familiarity effects. All ROIs showed more activation to new than seen and known faces. Seen and known faces elicited equal activation. Approximate ROI locations are shown (in green) on a ventral view of the cortex (shown here: MNI template colin27). Graphs show percent signal change and associated standard errors for the new (red), seen (blue), and known (green) predictors, averaged across subjects. All possible contrasts (new vs. seen, new vs. known, and seen vs. known) were tested for significance. Significant contrasts are shown and denoted with **(P < 0.01). ROIs were defined using independent data. See Table 1 for abbreviations and ROI details (including ROI-defining contrasts).