Lesion localization of speech comprehension deficits in chronic aphasia

Abstract

Objective: Voxel-based lesion-symptom mapping (VLSM) was used to localize impairments specific to multiword (phrase and sentence) spoken language comprehension.Methods: Participants were 51 right-handed patients with chronic left hemisphere stroke. They performed an auditory description naming (ADN) task requiring comprehension of a verbal description, an auditory sentence comprehension (ASC) task, and a picture naming (PN) task. Lesions were mapped using high-resolution MRI. VLSM analyses identified the lesion correlates of ADN and ASC impairment, first with no control measures, then adding PN impairment as a covariate to control for cognitive and language processes not specific to spoken language.Results: ADN and ASC deficits were associated with lesions in a distributed frontal-temporal parietal language network. When PN impairment was included as a covariate, both ADN and ASC deficits were specifically correlated with damage localized to the mid-to-posterior portion of the middle temporal gyrus (MTG).Conclusions: Damage to the mid-to-posterior MTG is associated with an inability to integrate multiword utterances during comprehension of spoken language. Impairment of this integration process likely underlies the speech comprehension deficits characteristic of Wernicke aphasia. The notion that speech comprehension depends on the posterior left superior temporal gyrus (pSTG) 1 is a persistent one, despite 3 major problems with this model. First, evidence suggests that the principal role of the pSTG is in processing phonologic information for short-term memory and speech production tasks.2-4 Second, language comprehension depends on a broadly distributed network spanning frontal, temporal, and parietal lobes. 5,6 Thus, any model that proposes a strict localization of language comprehension to the pSTG can no longer be seen as tenable. Third, speech comprehension is not a unitary process, but rather encompasses speech sound recognition, retrieval of individual word meanings, and various processes supporting integration of meaning across multiple words. All of these components also depend on the ability to maintain information in short-term memory and on general executive control processes. Given this complexity, which process or processes, if any, are likely to be localized to the superior temporal region?Multiword comprehension requires the rapid combination of individual word meanings, guided by syntactic information.7 Both functional imaging and lesion data suggest extensive cortical involvement in sentence comprehension [8][9][10][11] ; however, these studies have not attempted to separate the combinatorial processes unique to multiword comprehension from executive control processes. On the basis of several prior functional imaging studies, [12][13][14][15][16] we hypothesized that temporal lobe regions inferior to the classic Wernicke area may contain a critical site for combinatorial processing of phrase-level and sentence-level language. We tested this hypothesis

Agrammatism and paragrammatism: a cortical double dissociation revealed by lesion-symptom mapping

“…Previous lesion-deficit mapping studies of basic sentence and syntactic comprehension in the absence of working memory confounds have also primarily identified similar left posterior temporal-parietal areas (Wilson and Saygin, 2004;Thothathiri et al, 2012;Pillay et al, 2017;Fridriksson et al, 2018;Rogalsky et al, 2018;den Ouden et al, 2019). This suggests a role for left posterior temporal-parietal cortex in grammatical processes that underlie both comprehension and production.…”

Cortical and structural‐connectivity damage correlated with impaired syntactic processing in aphasia

“…Lesion-symptom-mapping studies have found damage to left-hemisphere anterior superior temporal gyrus, as well as superior temporal sulcus, middle temporal gyrus, angular gyrus, mid-frontal (BA 46), and IFG (BA 45; 47) to be associated with sentence comprehension difficulty in general, that is, irrespective of canonicity (Dronkers et al, 2004; Henseler et al, 2014; Pillay, Binder, Humphries, Gross, & Book, 2017; Tyler, Wright, Randall, Marslen-Wilson, & Stamatakis, 2010). In a previous study (Magnusdottir et al, 2013), we investigated the correlation of structural lesions with sentence comprehension deficits in a group of Icelandic stroke survivors ( n = 50) and identified damage to left anterior superior and middle temporal gyrus to be predictive of patients having greater problems with processing noncanonical sentences than canonical sentences in a sentence-picture verification task.…”

Post‐stroke cognitive deficits rarely come alone: Handling co‐morbidity in lesion‐behaviour mapping

“…A plethora of VLBM studies utilised nuisance regression or similar approaches to control the variable of interest for the variance explained by additional behavioural variables (e.g., Almairac et al, ; Baldo et al, , ; Finkel et al, ; Gajardo‐Vidal et al, ; Jones et al, ; Lorca‐Puls et al, ; Martin et al, ; Moon et al, ; Pillay et al, , ; Schwartz et al, ; Walker et al, ; Wilson et al, ; Winder et al, ). While some previous studies provide a rationale for covariate control, others do not provide any rationale at all or simply resort to a data driven procedure, where all known variables that correlate with the target symptom are controlled for.…”

“…A plethora of VLBM studies utilised nuisance regression or similar approaches to control the variable of interest for the variance explained by additional behavioural variables (e.g., Almairac et al, 2015;Baldo et al, 2013Baldo et al, , 2018Finkel et al, 2018;Gajardo-Vidal et al, 2018;Jones et al, 2016;Lorca-Puls et al, 2018;Martin et al, 2017;Moon et al, 2018;Pillay et al, 2014Pillay et al, , 2017Schwartz et al, 2011;Walker et al, 2011;Wilson et al, 2015;Winder et al, 2016).…”