Category-selective deficits are the exception and not the rule: Evidence from a case-series of 64 patients with ventral occipito-temporal cortex damage

Abstract

The organisational principles of the visual ventral stream are still highly debated, particularly the relative association/dissociation between word and face recognition and the degree of lateralisation of the underlying processes. Reports of dissociations between word and face recognition stem from single case-studies of category selective impairments, and neuroimaging investigations of healthy participants. Despite the historical reliance on single case-studies, more recent group studies have highlighted a greater commonality between word and face recognition. Studying individual patients with rare selective deficits misses (a) important variability between patients, (b) systematic associations between task performance, and (c) patients with mild, severe and/or non-selective impairments; meaning that the full spectrum of deficits is unknown. The Back of the Brain project assessed the range and specificity of visual perceptual impairment in 64 patients with posterior cerebral artery stroke recruited based on lesion localization and not behavioural performance. Word, object, and face processing were measured with comparable tests across different levels of processing to investigate associations and dissociations across domains. We present two complementary analyses of the extensive behavioural battery: (1) a data-driven analysis of the whole patient group, and (2) a single-subject case-series analysis testing for deficits and dissociations in each individual patient. In both analyses, the general organisational principle was of associations between words, objects, and faces even following unilateral lesions. The majority of patients either showed deficits across all domains or in no domain, suggesting a spectrum of visuo-perceptual deficits post stroke. Dissociations were observed, but they were the exception and not the rule: Category-selective impairments were found in only a minority of patients, all of whom showed disproportionate deficits for words. Interestingly, such selective word impairments were found following both left and right hemisphere lesions. This large-scale investigation of posterior cerebral artery stroke patients highlights the bilateral representation of visual perceptual function.

Keywords: Face recognition; Prosopagnosia; Pure alexia; Stroke; Visual agnosia; Visual perception; Word recognition.

Fig. 1

Lesion overlap map. Overlap of the lesion areas for each patient sub-group defined by the method described in Seghier et al. (2008). Colour bars indicate the number of patients with lesion in that area. Warmer colours = greater overlap, cooler colours = less overlap.

Fig. 2

Varimax rotated PCA of lower-level and higher-level visual tests. (a) A two-factor solution explained 73% of the variance (KMO = .895). Each point represents the factor loading of each neuropsychological test on the two principal factors extracted from the data. Tests that load significantly on Factor 1 (Word/Object) are shown in white, tests which load significantly on Factor 2 (Face/Object) are shown in black. (b) Patient factor scores on the two principal factors extracted in the data-driven analysis. Each point represents one patient. Points are colour coded according to lesion laterality (left hemisphere strokes in blue, right hemisphere strokes in red, bilateral strokes in purple). The size of each point denotes the size of the stroke (larger points = larger stroke volume). The PCA solution was calculated on the patient group alone, thus 0 on the x and y axis represents the mean performance of the patient group. Solid lines represent the average control group performance on each factor. The dashed lines represent two standard deviations away from the control mean for each factor.

Fig. 3

Single-subject composite score deficit analysis. (a) Raw composite scores for each participant sub-group for word, object and face processing. Patients showing a statistically significant deficit within a domain compared to the control group are highlighted with black circles. (b) Table summarising the pattern of significant deficits (one-tailed) across the patient group. Colours in the table correspond to the shading in Fig. 4.

Fig. 4

Comparison of the PCA solution described in Fig. 2b and the results of the deficit analysis in Fig. 3b. Each point represents one patient. As in Fig. 2b, the border colour of each point is colour coded according to lesion laterality (left hemisphere = blue, right hemisphere = red, bilateral = purple). The size of each point denotes the size of the stroke (larger points = larger stroke volume). The fill of each point is coloured according to the pattern of deficits described in Fig. 3b. Solid lines represent the average control group performance on each factor. Dashed lines represent two standard deviations away from the control mean.