Functional MRI Reveals Compromised Neural Integrity of the Face Processing Network in Congenital Prosopagnosia

Galia Avidan,Marlene Behrmann

doi:10.1016/j.cub.2009.04.060

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.

Highlights

Individuals with congenital prosopagnosia responded significantly more slowly than did controls (mean 6 standard error of the mean (SEM): congenital prosopagnosia group, 832 6 63 ms; controls, 694 6 30 ms; F(1,16) = 5.90; p < 0.03) and, as above, there were main effects of repetition (p < 0.0001) and familiarity (p < 0.03), but no significant interactions (F < 1; p > 0.3 for all interactions). These findings confirm the behavioral impairment in congenital prosopagnosia and indicate that the two groups were affected by the repetition manipulation and by the familiarity of the faces
To explore the underlying neural profile, via an independent face localizer scan, we identified in each individual in each hemisphere, regions of interest (ROIs), showing a selective response for faces compared with all other stimuli
Given the normal ventral occipitotemporal cortex (VOTC) activation profile in parallel with the ongoing behavioral impairment, we explored the differential impact of familiarity on the blood oxygenation level-dependent (BOLD) signal of the two groups across the entire cortex, by contrasting all trials containing famous versus unknown faces via a multisubject general linear model analysis

Summary

Introduction

The presence of an adaptation signal in individuals with congenital prosopagnosia, of equivalent strength to that of the controls, is consistent with results indicating normal face-selective activation in VOTC in these individuals [10, 21]. The repetition index (different versus same picture), calculated in FFA and OFA for famous and unknown faces, for each individual with congenital prosopagnosia is within the range of controls, corroborating the results of the ANOVA and replicating the result at the individual subject level (see Figure S2).

Results

Conclusion