Functional MRI reveals compromised neural integrity of the face processing network in congenital prosopagnosia

Abstract

The summed activity of multiple nodes of a distributed cortical network supports face recognition in humans, including "core" ventral occipitotemporal cortex (VOTC) regions, and "extended" regions outside VOTC. Many individuals with congenital prosopagnosia-an impairment in face processing-exhibit normal blood oxygenation level-dependent (BOLD) activation in the core VOTC regions. These individuals evince a reduction in the structural integrity of the white matter tracts connecting VOTC to anterior temporal and frontal cortices, part of the "extended" face network. The impairment in congenital prosopagnosia may arise, therefore, not from a dysfunction of the core VOTC areas but from a failure to propagate signals between the intact VOTC and the extended nodes of the network. Using the fMR adaptation paradigm with famous and unknown faces, we show that individuals with congenital prosopagnosia evince normal adaptation effects in VOTC, indicating sensitivity to facial identity, but show no differential activation for familiar versus unknown faces outside VOTC, particularly in the precuneus/posterior cingulate cortex and the anterior paracingulate cortex. Normal BOLD activation in VOTC is thus insufficient to subserve intact face recognition, and disrupted information propagation between VOTC and the extended face processing network may explain the functional impairment in congenital prosopagnosia.

Figure 1

a. Experimental design of the face identity repetition experiment and schematic depiction of a trial In each trial, two faces were presented sequentially and subjects performed a ‘same/different’ identity task. In half of the trials, both pictures were of famous individuals and, in the other half, they were of unknown individuals. All conditions were counterbalanced. On each trial, lasting 3000 msec, the pictures were presented consecutively for 300msec each with an ISI of 200 msec. b. Repetition effects in FFA Top row: Activation profiles showing the repetition effect (reduced signal for ‘same picture’ compared to ‘different picture’ condition) for 12 control subjects. The y-axis denotes the averaged beta weights (parameter estimates) and error bars indicate standard error of the mean (SEM) across subjects. Bottom row: Activation profiles showing the repetition effect for the congenital prosopagnosia group. Although the signal magnitude was greater in controls compared to the congenital prosopagnosia subjects, there were no interactions with group, indicating that both groups were equally affected by the repetition manipulation.

Figure 2. Activation foci exhibiting a familiarity effect outside VOTC

a. A statistical test contrasting all famous and unknown faces was conducted separately for two subgroups of controls with 6 participants in each and for the congenital prosopagnosia group (multi subject GLM, fixed effects, p<0.002 Bonferroni corrected). The analysis revealed selective activation for famous compared to unknown faces in the left precuneus/posterior cingulate cortex and the anterior paracingulate cortex in both control groups but not in the congenital prosopagnosia group. The average activation across each control subgroup is overlaid on sagittal, coronal and axial slices of one individual subject. Note the absence of familiarity selective activation in the CP group (lower panel). (L=left hemisphere, R=right hemisphere).