Spatial Mechanisms within the Dorsal Visual Pathway Contribute to the Configural Processing of Faces

Abstract

Human face recognition is often attributed to configural processing; namely, processing the spatial relationships among the features of a face. If configural processing depends on fine-grained spatial information, do visuospatial mechanisms within the dorsal visual pathway contribute to this process? We explored this question in human adults using functional magnetic resonance imaging and transcranial magnetic stimulation (TMS) in a same-different face detection task. Within localized, spatial-processing regions of the posterior parietal cortex, configural face differences led to significantly stronger activation compared to featural face differences, and the magnitude of this activation correlated with behavioral performance. In addition, detection of configural relative to featural face differences led to significantly stronger functional connectivity between the right FFA and the spatial processing regions of the dorsal stream, whereas detection of featural relative to configural face differences led to stronger functional connectivity between the right FFA and left FFA. Critically, TMS centered on these parietal regions impaired performance on configural but not featural face difference detections. We conclude that spatial mechanisms within the dorsal visual pathway contribute to the configural processing of facial features and, more broadly, that the dorsal stream may contribute to the veridical perception of faces.

Trial registration: ClinicalTrials.gov NCT00001360.

Keywords: TMS; fMRI; face perception; spatial perception.

Figure 1.

Sample trial screens and face stimuli used in the fMRI and TMS experiments. (A) Sample stimulus display used in the main tasks of the fMRI study and TMS experiment, consisting of two face images that differ in the configuration of their internal features (distance between the eyes and between the nose and mouth). (B) Sample stimulus display in which the face images differ in the shape of their internal features (eyes and nose). (C) All the 20 faces used in the fMRI and TMS experiments.

Figure 2.

Cortical activation and brain activity–behavior correlation maps from the fMRI study. The 3D cortical meshes shown are partially inflated so activity within the sulci can be visible. (A) Cortical activation maps (magnitude of activity; difference in beta-weight coefficients) revealed by the fMRI contrast of configural difference detections > featural difference detections at the level of the whole brain (B) Correlation maps revealed by the interaction term in the linear mixed effects model contrasting the brain activity-behavior correlations between the two face tasks. Positive activations (yellow-orange) correspond to regions, within the localized dorsal ROI, where the correlation between brain activity (beta-weight coefficients) and RT (msec) was stronger for configural compared to featural face difference detections (the unit is difference in r² values). Negative activations (cyan-blue) correspond to regions, within the dorsal ROI, where the correlation between brain activity (beta-weight coefficients) and RT (ms) was stronger for featural compared to configural face difference detections. The green outlines illustrate the brain regions identified by the dorsal stream localizer tasks (IPS, intraparietal sulcus; SPL: superior parietal lobule; IPL: inferior parietal lobule). The pink and cyan outlines illustrate the brain regions identified by the ventral stream localizer tasks (pink: stronger activation in response to faces; FFA: fusiform face area; cyan: stronger activation in response to houses; PPA: parahippocampal place area). For clarity, the anatomical locations of the central sulci are shown with dashed white lines.

Figure 3.

Differences in functional connectivity for configural and featural face difference detections between the right FFA (individually localized) as the seed and BOLD activity in: (A) brain regions identified by the dorsal stream localizer task (IPS, intraparietal sulcus; SPL: superior parietal lobule; IPL: inferior parietal lobule; shown as green outlines); and (B) brain regions identified by the ventral stream localizer task (pink: greater activation in response to faces; FFA: fusiform face area; cyan: stronger activation in response to houses; PPA: parahippocampal place area). Positive activations (yellow-orange) indicate that functional connectivity between the activated voxels and those within the right FFA seed region was stronger during configural face difference detections compared to featural difference detections (a difference in Pearson's r). Negative activations (cyan-blue) indicate that functional connectivity between the activated voxels and those within the right FFA seed region was stronger during featural face difference detections compared to configural difference detections. For clarity, the anatomical locations of the central sulci are shown with dashed white lines.

Figure 4.

The figure depicts the behavioral data analysis of the TMS experiment, arranged by the type of trial. (A) Reaction Time (RT, in msec) and (B) Accuracy (ACC, % correct) across all the four different trial types of the TMS experiment. The three-way interaction between TMS site, type of face difference (configural/featural) and TMS (applied or not) in the analysis of RT is shown in (A). The abbreviations depicted on the x-axis are as follows: R PPC: right posterior parietal cortex; L PPC: left posterior parietal cortex. The error bars denote +/− 1 SE.