The ins and outs of meaning: Behavioral and neuroanatomical dissociation of semantically-driven word retrieval and multimodal semantic recognition in aphasia

Abstract

Theories about the architecture of language processing differ with regard to whether verbal and nonverbal comprehension share a functional and neural substrate and how meaning extraction in comprehension relates to the ability to use meaning to drive verbal production. We (re-)evaluate data from 17 cognitive-linguistic performance measures of 99 participants with chronic aphasia using factor analysis to establish functional components and support vector regression-based lesion-symptom mapping to determine the neural correlates of deficits on these functional components. The results are highly consistent with our previous findings: production of semantic errors is behaviorally and neuroanatomically distinct from verbal and nonverbal comprehension. Semantic errors were most strongly associated with left ATL damage whereas deficits on tests of verbal and non-verbal semantic recognition were most strongly associated with damage to deep white matter underlying the frontal lobe at the confluence of multiple tracts, including the inferior fronto-occipital fasciculus, the uncinate fasciculus, and the anterior thalamic radiations. These results suggest that traditional views based on grey matter hub(s) for semantic processing are incomplete and that the role of white matter in semantic cognition has been underappreciated.

Damage to white matter bottlenecks contributes to language impairments after left hemispheric stroke

“…Previous studies using different task paradigms have implicated damage to the left IFG, pSTG/pMTG, and pSMG/AG, in deficits of auditory comprehension and/or discrimination (Bates et al, 2003, Dronkers et al, 2004, Fridriksson et al, 2013, Geva et al, 2012, Pustina et al, 2016, Yourganov et al, 2016), and have implicated anterior temporal lobe lesions in semantic deficits when controlling for deficits in comprehension (Mirman et al, 2015a, Mirman et al, 2015b, Schwartz et al, 2009, Walker et al, 2011). Importantly, all of these regions were identified by our analysis, and are associated with the semantic network recruited by this task (Binder et al, 1997, Binder et al, 2009).…”

Converging evidence from fMRI and aphasia that the left temporoparietal cortex has an essential role in representing abstract semantic knowledge

“…However, it is not clear that this functional connectivity should implicate a single white matter tract such as the SLF or arcuate fasciculus. A recent study of 99 participants with aphasia following left hemisphere stroke found that deficits in recognizing semantic relationships were associated with damage to a frontal “white matter bottleneck” that affected the inferior fronto-occipital fasciculus, the uncinated fasciculus, and the anterior thalamic radiations (Mirman et al, 2015a; 2015b). Mirman et al interpreted this result to mean that semantic cognition requires widespread connectivity between frontal regions and other brain regions involved in semantic memory, rather than a single connection between any two regions.…”

Revealing the dual streams of speech processing

“…citations). Although it has become common practice to explain results of neuroimaging studies of speech processing in the context of dual stream models (16)(17)(18)(19)(20)(21), the specific location and extent of the dorsal and ventral streams involved in speech processing, each of which is a theoretical construct based on either animal data (5) or the combination of lesion and functional neuroimaging data in humans (8), remain elusive.…”

“…Other studies have used a principal components analysis (PCA) step as part of the analysis relating localized brain damage to behavioral impairment (19,31,32). However, those studies differed from this approach in that each carried out PCA on the behavioral data and then, included the components as dependent factors in a voxel-based lesion-symptom mapping (VLSM) analysis.…”