Damage to ventral and dorsal language pathways in acute aphasia

Kümmerer, Dorothee; Hartwigsen, Gesa; Kellmeyer, Philipp; Glauche, Volkmar; Mader, Irina; Klöppel, Stefan; Suchan, J; Karnath, Hans‐Otto; Weiller, Cornelius; Saur, Dorothee

doi:10.1093/brain/aws354

Cited by 238 publications

(210 citation statements)

References 51 publications

(70 reference statements)

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“…One approach to assessing the spatial extent of dual streams is to relate specific measures of speech production or speech comprehension to lesion location in patients (29). However, a limitation of such an approach is that it assumes that the complex aspects of speech production and comprehension can be appreciated with single measures.…”

Section: Significancementioning

confidence: 99%

Revealing the dual streams of speech processing

Fridriksson

Yourganov

Bonilha

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

145

131

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Several dual route models of human speech processing have been proposed suggesting a large-scale anatomical division between cortical regions that support motor-phonological aspects vs. lexical-semantic aspects of speech processing. However, to date, there is no complete agreement on what areas subserve each route or the nature of interactions across these routes that enables human speech processing. Relying on an extensive behavioral and neuroimaging assessment of a large sample of stroke survivors, we used a data-driven approach using principal components analysis of lesionsymptom mapping to identify brain regions crucial for performance on clusters of behavioral tasks without a priori separation into task types. Distinct anatomical boundaries were revealed between a dorsal frontoparietal stream and a ventral temporal-frontal stream associated with separate components. Collapsing over the tasks primarily supported by these streams, we characterize the dorsal stream as a form-to-articulation pathway and the ventral stream as a form-to-meaning pathway. This characterization of the division in the data reflects both the overlap between tasks supported by the two streams as well as the observation that there is a bias for phonological production tasks supported by the dorsal stream and lexical-semantic comprehension tasks supported by the ventral stream. As such, our findings show a division between two processing routes that underlie human speech processing and provide an empirical foundation for studying potential computational differences that distinguish between the two routes.aphasia | speech production | speech comprehension | voxel-based lesionsymptom mapping | speech processing U nderstanding how and where in the brain speech processing occurs has been the focus of concerted scientific endeavor for over one and a half centuries. The most influential model of the neuroanatomical basis of speech processing was proposed by Wernicke (1) and later refined by Lichtheim (2)-the WernickeLichtheim (W-L) model. The W-L model includes two separate routes from a posterior auditory comprehension center to an anterior motor speech production center: a direct route that enables speech repetition and an indirect route via ideation that mediates comprehension and propositional speech. More recently, dual route processing has been recognized as a central principle in the functional organization of the brain. Ungerleider and Mishkin (3) proposed that visual perception in primates is supported by a ventral "what" stream (involving an occipital-temporal lobe route) and a dorsal "where" stream [or later, a "how" stream mediated by an occipital-parietal route (4)]. Similarly, in the auditory domain (5), Rauschecker and Tian (6) proposed a "dual stream" model to account for the identification of what was being heard and from where the sound originated (5, 6). This model, mostly derived from nonhuman primate data, distinguishes between an anterior/ ventral route ("what" stream) involving connections from the left posterior superio...

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Section: Significancementioning

confidence: 99%

Revealing the dual streams of speech processing

Fridriksson

Yourganov

Bonilha

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

145

131

View full text Add to dashboard Cite

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“…Temporal tracts, such as the inferior longitudinal fasciculus (ILF), inferior frontal-occipital fasciculus (IFOF), and potentially also the uncinate fasciculus (UF) and middle longitudinal fasciculus, have been shown to be mainly involved in language comprehension (Ivanova et al, 2016;Kümmerer et al, 2013).…”

Section: Diffusion Mrimentioning

confidence: 99%

What Do Language Disorders Reveal about Brain–Language Relationships? From Classic Models to Network Approaches

Dronkers

Ivanova

Baldo

2017

J Int Neuropsychol Soc

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Studies of language disorders have shaped our understanding of brain-language relationships over the last two centuries. This article provides a review of this research and how our thinking has changed over the years regarding how the brain processes language. In the 19th century, a series of famous case studies linked distinct speech and language functions to specific portions of the left hemisphere of the brain, regions that later came to be known as Broca's and Wernicke's areas. One hundred years later, the emergence of new brain imaging tools allowed for the visualization of brain injuries in vivo that ushered in a new era of brain-behavior research and greatly expanded our understanding of the neural processes of language. Toward the end of the 20th century, sophisticated neuroimaging approaches allowed for the visualization of both structural and functional brain activity associated with language processing in both healthy individuals and in those with language disturbance. More recently, language is thought to be mediated by a much broader expanse of neural networks that covers a large number of cortical and subcortical regions and their interconnecting fiber pathways. Injury to both grey and white matter has been seen to affect the complexities of language in unique ways that have altered how we think about brain-language relationships. The findings that support this paradigm shift are described here along with the methodologies that helped to discover them, with some final thoughts on future directions, techniques, and treatment interventions for those with communication impairments. (JINS, 2017, 23, 741-754)

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“…While the MTG generally has been considered a critical region in the language comprehension network, with multiple fibre pathways converging beneath this region and cortical association areas directly connected to it (Turken & Dronkers, 2011), the more anterior portions of the temporal lobe have been described as an amodal conceptual hub (Patterson et al, 2007) and considered a critical region for semantic memory, although its precise function remains unclear (Bonner & Price, 2013). Evidence from the aphasia literature has shown that lesions in the anterior temporal region are associated with semantic recognition and production deficits and that auditory comprehension deficits are associated with a disruption in the ventral stream pathway which connects regions in the temporal and prefrontal lobes (Kümmerer et al, 2013). In terms of concrete and abstract processing specifically and focal aMTG lesions, the literature has shown mixed results.…”

Section: Discussionmentioning

confidence: 99%

“…In aphasia, focal lesions in the anterior temporal region have been associated with semantic recognition and production impairments while disruption of the ventral stream (a pathway connecting regions in auditory cortex with the anterior temporal lobe and prefrontal cortex) results in auditory comprehension deficits (Kümmerer et al, 2013) and a reduction in accuracy in the conduite d'approche (i.e. multiple repeated attempts to retrieve a target)…”

Section: Relationship Between Chronic Brain Activity and Language Recmentioning

confidence: 99%

“…Functional MRI can be used to complement lesion studies such that anatomical maps can be overlaid with lesion maps and fMRI activation maps to identify regions that are critical to the performance of a language task (Price & Friston, 2002;Vandenberghe & Gillebert, 2009). In addition, the complementary use of voxelwise lesion-behaviour mapping (Rorden, Karnath, & Bonilha, 2007) and DTI has been used to examine how damage to ventral and dorsal language pathways affects language comprehension in acute aphasia (Kümmerer et al, 2013) and future longitudinal studies investigating aphasia recovery would benefit from examining how the relationship between structure and function changes over the course of aphasia recovery.…”

Section: Limitations and Future Directionsmentioning

confidence: 99%

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Neurophysiological Markers of Language Recovery in Subacute Stroke

Roxbury¹

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Most patients with aphasia recover language function to some degree, but there is significant variability in the speed, nature, and extent of language recovery that occurs in the months following a stroke. Currently, there is no effective method available to predict how an individual with aphasia will recover. The most accurate predictors of recovery to date rely on global outcome measures which do not provide relevant information regarding recovery of symptoms that are targeted in therapy. The overall goal of this thesis was to examine whether language-related brain activity predicted recovery of specific symptoms in aphasia. The first aim was to gain a clearer understanding of the neural mechanisms which underpin word processing in healthy individuals.Brain activity associated with spoken word processing was investigated firstly in a group of healthy young adults, then in a healthy older cohort in order to ascertain whether task performance was preserved in ageing and if so, whether a preserved performance was underpinned by age-related changes in the neural mechanisms. The second main aim was to investigate the neural substrates which underpin language processing in the subacute (2-6 weeks) and chronic (6 months) phases of aphasia recovery and to determine whether the timing and extent to which these mechanisms are recruited contributes to a good or poor language outcome. An auditory lexical decision task with a novel pseudoword condition was employed to investigate language recovery mechanisms and was selected to ensure that patients with aphasia in the subacute stage would be able to perform the task with sufficient accuracy. The real word stimuli consisted of concrete and abstract items. The stimuli were presented in an event-related fMRI task to young healthy controls, older healthy controls, and patients with aphasia during the subacute and chronic phases post-stroke. A range of behavioural language measures was administered to all three cohorts and at both time points for patients with aphasia.In the healthy young group, concrete words elicited increased activity in a widely distributed network of brain regions including bilateral angular gyrus (AG), left posterior cingulate and left dorsolateral prefrontal cortex, compared to abstract words. Meanwhile, no region showed increased activity for abstract compared to concrete words, rather differences were only observed in bilateral AG when abstract words were contrasted with pseudowords. In the healthy older group, region of interest (ROI) results identified that a preserved performance was associated with an altered pattern of left hemisphere activity in the inferior and middle frontal regions, the AG and the fusiform gyrus.Differences between the healthy older and healthy young group were identified in key language regions, with the left inferior frontal gyrus (IFG) showing increased activity for abstract and pseudowords compared to concrete words while increased activity in the left AG was observed in the younger group only.ii In patients with a...

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Damage to ventral and dorsal language pathways in acute aphasia

Cited by 238 publications

References 51 publications

Revealing the dual streams of speech processing

Revealing the dual streams of speech processing

What Do Language Disorders Reveal about Brain–Language Relationships? From Classic Models to Network Approaches

Neurophysiological Markers of Language Recovery in Subacute Stroke

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