Functional connectivity and the failure to retrieve meaning from shape in visual object agnosia

The neural mechanisms underlying the access to object knowledge from early representations of shape are little known. Functional imaging studies support the view that representations of visual properties are distributed across occipito-temporal cortex of both cerebral hemispheres. By contrast, brain lesion studies show that focal occipito-temporal damage may lead to object agnosia - a specific impairment of object recognition. How does distributed processing fit with functional specialization implied by the existence of stimulus-specific agnosias? Using fMRI we studied functional connectivity (FC) in a patient with object agnosia following left lateral occipital damage. Despite intact global and local processing of 2D and 3D object structure, the patient made consistent object identification errors. Seven experiments testing naming, visual matching or object priming showed that his errors mainly reflected the global shape similarity between objects. Compared to controls the patient exhibited strongly reduced FC between the damaged left and the intact right medial/lateral occipital cortex. In addition, controls showed stronger connectivity between the right occipital cortex and the left and right inferior and anterior temporal cortices. Interestingly, the patient also showed compensatory increases of FC between dorsal occipital and medial parietal cortex. These findings show that focal damage to the lateral occipital cortex may have global effects on representations of objects in bilateral occipito-temporal cortex, thus supporting the view that bilaterally distributed coding is necessary for the retrieval of associative knowledge from shape.