Meaning for reading: the neurocognitive basis of semantic reading impairment after stroke

Abstract

Diagnosis of alexia has historically focused on syndromes such as surface alexia, which capture discrete patterns of reading deficits observed in some patients but do not describe the breadth of reading deficits observed in practice. Aphasia research has recently shifted focus to language process impairments rather than syndromic classifications. A similar shift in focus to reading process impairments might improve our diagnostic approach to alexia. Behavioural evidence suggests that semantic processing influences reading aloud and that semantic deficits in the context of semantic dementia underlie surface alexia. Because stroke rarely causes loss of semantic knowledge and surface alexia as a syndromic diagnosis is unusual after stroke, semantic reading deficits in stroke alexia have not previously been examined systematically. Semantic reading deficits in stroke may not relate to semantic deficits per se, but rather an inability to use semantics to support reading. Imageability, the degree to which a word brings to mind an image, is one index of semantic influences on reading. High-imageability words are read more quickly by healthy persons and more accurately following brain damage. Here, we test whether deficits of semantic reading after stroke, as indexed by reduced imageability effects, result from semantic or post-semantic processes. Examining non-verbal semantic processing, semantics-phonology mapping and semantic control in 56 left-hemisphere stroke survivors, only better semantics-phonology mapping ability predicted better accuracy on high-imageability words. Neither semantic nor post-semantic scores related to low-imageability word accuracy. Support vector regression voxel-based lesion symptom mapping revealed that damage along the superior temporal sulcus and underlying white matter, extending into the middle and superior temporal gyri, reduced the advantage of high-imageability over low-imageability words during reading, reflecting an inability to use semantics to support reading. A similar cluster related to impairments in semantics-phonology mapping. The imageability and semantics-phonology mapping results overlapped in the left posterior superior temporal sulcus. Support vector regression connectome lesion symptom mapping revealed that white matter disconnections within a broad temporoparietal network important for phonological and semantic processing were associated with a reduction of the imageability advantage during reading. These results demonstrate that, irrespective of syndromic classification, semantic reading deficits occur in left-hemisphere stroke survivors owing to impaired integration of semantic and phonological representations and that the left posterior superior temporal sulcus underlies this process. Our results clarify the neurobiology of reading aloud and support the existence of a post-semantic impairment of semantic reading in left-hemisphere stroke survivors.

Keywords: alexia; language; lesion–symptom mapping; reading; semantics; stroke.