Neural organization of speech production: A lesion-based study of error patterns in connected speech

Abstract

While numerous studies have explored single-word naming, few have evaluated the behavioral and neural correlates of more naturalistic language, like connected speech, which we produce every day. Here, in a retrospective analysis of 120 participants at least six months following left hemisphere stroke, we evaluated the distribution of word errors (paraphasias) and associated brain damage during connected speech (picture description) and object naming. While paraphasias in connected speech and naming shared underlying neural substrates, analysis of the distribution of paraphasias suggested that lexical-semantic load is likely reduced during connected speech. Using voxelwise lesion-symptom mapping (VLSM), we demonstrated that verbal (real word: semantically related and unrelated) and sound (phonemic and neologistic) paraphasias during both connected speech and naming loaded onto the left hemisphere ventral and dorsal streams of language, respectively. Furthermore, for the first time using both connected speech and naming data, we localized semantically related paraphasias to more anterior left hemisphere temporal cortex and unrelated paraphasias to more posterior left temporal and temporoparietal cortex. The connected speech results, in particular, highlight a gradient of specificity as one translates visual recognition from left temporo-occipital cortex to posterior and subsequently anterior temporal cortex. The robustness of VLSM results for sound paraphasias derived during connected speech was notable, in that analyses performed on sound paraphasias from the connected speech task, and not the naming task, demonstrated significant results following removal of lesion volume variance and related apraxia of speech variance. Therefore, connected speech may be a particularly sensitive task on which to evaluate further lexical-phonological processing in the brain. The results presented here demonstrate the related, though different, distribution of paraphasias during connected speech, confirm that paraphasias arising in connected speech and single-word naming

Functional differentiation in the language network revealed by lesion-symptom mapping

“…However, picture naming, unlike the word fluency task, involves selecting among competing alternatives (e.g., to name a picture of a cat, the competing alternative dog must be suppressed). Interestingly, a recent LSM study of word-level semantic errors in natural, connected speech found that increased errors were associated with temporal and inferior parietal damage, but not frontal damage ( Stark et al, 2019 ). Connected speech differs from confrontation or picture naming in allowing the subject to select alternative words or concepts, which reduces the burden of the task on selection abilities.…”

Damage to Broca’s area does not contribute to long-term speech production outcome after stroke

“…Across the 27 subtests that comprise the CAT, we selected the spoken picture description task as our behavioural index of speech production abilities, with the goal of ensuring the ecological validity of our findings by assessing connected speech production (rather than single word production) in a setting that resembled those encountered in real-world scenarios more closely. Our decision was also motivated by recent efforts to characterise the complex nature of speech production, their deficits and neural correlates using samples of connected speech ( Stark et al , 2019 ; Alyahya et al , 2020; Ding et al ., 2020 ). The CAT spoken picture description task was administered to each patient and the spoken responses scored following standardized procedures described in the assessment battery manual.…”

“…Given the methodological constraints described above, it was not feasible to investigate, within the same study, all the grey or white matter regions that have previously been associated with speech production. For example, we did not examine temporal and parietal regions ( Stark et al , 2019 ; Forkel et al , 2020 ), the internal capsule ( Naeser et al 1982 ), the medial subcallosal fasciculus or the periventricular white matter area ( Naeser et al , 1989 ). Nor did we investigate the inferior fronto-occipital fasciculus or long segment of the arcuate fasciculus because a previous well-powered lesion study was unable to establish a significant relationship between persistent speech production impairments and damage to either of these white matter tracts after controlling for damage to the anterior segment of the arcuate fasciculus ( Fridriksson et al , 2013 ).…”

Language systems from lesion-symptom mapping in aphasia: A meta-analysis of voxel-based lesion mapping studies

“…V Baldo et al (2012) repetition 3 84 2 Døli et al (2020) repetition 12 21 3 Faroqi-Shah et al (2014) nonword repetition 5 31 4 Kümmerer et al (2013) repetition 3 100 5 Sul et al (2019) repetition 3 31 6 Xing et al (2016) repetition 3 32 Naming 1 Reem. S. W Alyahya et al (2018) verb naming 16 48 2 Juliana V Baldo et al (2013) naming 2 43 3 Døli et al (2020) naming 7 21 4 Faroqi-Shah et al (2014) picture naming 5 31 5 Gajardo-Vidal et al (2018a) naming 3 359 6 Harvey and Schnur (2015) naming relatedness effect 2 15 7 Lau et al (2015) object naming 9 280 8 Schwartz et al (2012) naming error 4 106 9 Stark et al (2019) naming error 34 57 …”