Types of naming errors in chronic post-stroke aphasia are dissociated by dual stream axonal loss

Emilie T Mckinnon,Julius Fridriksson,Leonardo Bonilha,Jens H Jensen,Alexandra Basilakos,Chris Rorden,Joseph A Helpern,Ezequiel Gleichgerrcht,Argye E Hillis,M Vittoria Spampinato,Gregory Hickok

doi:10.1038/s41598-018-32457-4

Abstract

The types of errors during speech production can vary across individuals with chronic post-stroke aphasia, possibly due to the location and extent of brain damage. In this study, we evaluated the relationship between semantic vs. phonemic errors during confrontational naming, and their relationship with the degree of damage to ventral and dorsal white matter pathways extending beyond the necrotic stroke lesion. Based on the dual stream model of language processing, we tested the hypothesis that semantic errors would be associated with ventral stream damage, whereas phonemic errors would be associated with dorsal stream damage, but not vice-versa. Multi-shell diffusion MRI was used to obtain kurtosis-based white matter tractography from 32 chronic stroke survivors. Using diffusion microstructural tissue modeling, we estimated axonal loss along the length of the inferior and superior longitudinal fasciculi (ILF and SLF), representing the main pathways in the ventral and dorsal streams, respectively. The frequency of semantic paraphasias was strongly associated with ILF axonal loss, whereas phonemic paraphasias were strongly associated with SLF axonal loss, but not vice versa. This dissociation between semantic and phonological processing is in agreement with the dual stream model of language processing and corroborates the concept that, during speech production, knowledge association (semantics) depends on the integrity of ventral, whereas form encoding (phonological encoding) is more localized to dorsal pathways. These findings also demonstrate the importance of the residual integrity of specific white matter pathways beyond regional gray matter damage for speech production.

Highlights

Many stroke survivors experience language impairments beyond six months after a dominant hemisphere stroke[1]
We examined whether the degree of ventral vs. dorsal stream damage dissociates the proportion of phonemic and semantic paraphasias in a group of individuals with chronic aphasia
WAB aphasia quotient (WAB-AQ), aphasia types and average Philadelphia Naming Test results for all individuals are summarized in Supplementary Table S1

Summary

Introduction

Many stroke survivors experience language impairments (aphasia) beyond six months after a dominant hemisphere stroke[1]. Paraphasias offer a critical window into the mechanisms of speech production because they represent discrete deficits regarding (1) the spoken sound structure (phonemic) vs (2) speech related knowledge association (semantic) They provide the opportunity to determine if these processes dissociate into different anatomic-functional pathways. Diffusion MRI (dMRI) is ideally suited to study post-stroke residual white matter integrity non-invasively and to test the hypothesis that semantic and phonological processing dissociates between the ventral and dorsal white matter pathways. Since dMRI provides measures sensitive to axonal integrity, it can improve the sensitivity in determining which pathways are associated with phonological vs semantic deficits and resolve the underlying neurobiological mechanisms of regional brain damage that contribute to speech production errors. We hypothesized that in chronic stroke axonal loss, reflected by a decreased AWF in the ventral but not dorsal stream, would directly associate with semantic but not phonological paraphasias and vice versa

Methods

Results

Conclusion