Structure and function in acquired prosopagnosia: Lessons from a series of 10 patients with brain damage

Abstract

Acquired prosopagnosia varies in both behavioural manifestations and the location and extent of underlying lesions. We studied 10 patients with adult‐onset lesions on a battery of face‐processing tests. Using signal detection methods, we found that discriminative power for the familiarity of famous faces was most reduced by bilateral occipitotemporal lesions that involved the fusiform gyri, and better preserved with unilateral right‐sided lesions. Tests of perception of facial structural configuration showed severe deficits with lesions that included the right fusiform gyrus, whether unilateral or bilateral. This deficit was most consistent for eye configuration, with some patients performing normally for mouth configuration. Patients with anterior temporal lesions had better configuration perception, though at least one patient showed a more subtle failure to integrate configural data from different facial regions. Facial imagery, an index of facial memories, was severely impaired by bilateral lesions that included the right anterior temporal lobe and marginally impaired by fusiform lesions alone; unilateral right fusiform lesions tended to spare imagery for facial features. These findings suggest that (1) prosopagnosia is more severe with bilateral than unilateral lesions, indicating a minor contribution of the left hemisphere to face recognition, (2) perception of facial configuration critically involves the right fusiform gyrus and (3) access to facial memories is most disrupted by bilateral lesions that also include the right anterior temporal lobe. This supports assertions that more apperceptive variants of prosopagnosia are linked to fusiform damage, whereas more associative variants are linked to anterior temporal damage. Next, we found that behavioural indices of covert recognition correlated with measures of overt familiarity, consistent with theories that covert behaviour emerges from the output of damaged neural networks, rather than alternative pathways. Finally, to probe the face specificity of the prosopagnosic defect, we tested recognition of fruits and vegetables: While face specificity was not found in most of our patients, the data of one patient suggested that this may be possible with more focal lesions of the right fusiform gyrus.

Deficits in face perception in the amnestic form of mild cognitive impairment

“…These show reduced diagnosticity of the eye region of the face [38,39] and fewer ocular fixations on the upper face [40]. Studies with a similar paradigm to ours have also shown in some but not all prosopagnosic patients with occipitotemporal lesions a similar pattern, with selective impairment for eye configuration with spared processing of mouth configuration [29].…”

“…The fact that aMCI patients had difficulty with all facial properties with brief viewing may reflect general reductions in processing speed, attention, or visual efficiency. Indeed, low-level factors like hemianopia reduce accuracy at limited duration, but unlike our aMCI patients, hemianopic patients achieve normal accuracy at unlimited duration [29] hence the important of trials that allow the subject more time.…”

“…Rather, a selective problem with processing the eye region at unlimited durations is reminiscent of the deficit in some studies of acquired prosopagnosia patients, many with fusiform lesions [29,[38][39][40][41][42]. These show reduced diagnosticity of the eye region of the face [38,39] and fewer ocular fixations on the upper face [40].…”

Predictive codes of familiarity and context during the perceptual learning of facial identities

“…Lesions to this region can cause prosopagnosia 25 , the inability to recognize the identity of familiar individuals, while leaving the ability to detect the presence of a face intact. Numerous studies that have employed fMRI adaptation paradigms have demonstrated the sensitivity of the FFA to differences in face identity 21,[26][27][28][29][30] .…”

Structural connectivity in a single case of progressive prosopagnosia: The role of the right inferior longitudinal fasciculus

“…Such lesion studies, combined with functional imaging studies in normal individuals, have demonstrated that regions of the posterior fusiform gyrus, the inferior lateral occipital cortex and the posterior superior temporal sulcus (STS) are involved in face processing (e.g., Allison et al, 1994aAllison et al, , 1999Barton, 2008;Kanwisher et al, 1997;Grill-Spector et al, 2004;Pitcher et al, 2009;Rossion et al, 2003;Sergent et al, 1992). Within these regions, that are part of the so-called 'core system' for face processing (Haxby et al, 2000), the fusiform gyrus seems to be especially important for processing facial identity.…”