Dissociating the roles of ventral versus dorsal pathways in language production: an awake language mapping study
-
1
San Diego State University, School of Speech, Language, and Hearing Sciences, United States
-
2
Radboud University, Donders Centre for Cognition, Netherlands
-
3
Radboud UMC, Department of Medical Psychology, Netherlands
-
4
University of California San Francisco, Department of Neurological Surgery, United States
-
5
University of California Berkeley, Department of Psychology, Helen Wills Neuroscience Institute, United States
-
6
University of California San Francisco, Department of Neurology, United States
Background
The neural basis for human language is thought to be organized along two main processing streams connecting the posterior temporal cortex to the inferior frontal cortex in the left hemisphere: one travelling dorsal, and the other travelling ventral to the Sylvian fissure. The roles of these two streams have been subject to debate. Some views propose a motor (dorsal) versus conceptual/semantic (ventral) division (e.g., Hickok & Poeppel, 2007). Others propose a division along different types of combinatorial mechanisms (the dorsal stream being associated with the ability to combine elements into a sequence, the ventral with the formation of dependencies independent of sequential order and thus associated with semantics; Bornkessel-Schlesewsky, Schlesewsky, Small, & Rauschecker, 2015). However, the causal roles of dorsal and ventral white matter pathways associated with language production have yet to be specified. Here, we present data acquired through direct cortical electrical stimulation and subcortical resection during awake language mapping in 18 neurosurgical patients prior to and during tumor resection.
Methods
Of the 18 patients, 17 were stimulated cortically and 10 were tested during subcortical resection in one or both of our tasks. Our 2 language tasks were designed to test the roles of the ventral and dorsal streams in language production. We used a picture-word interference (PWI) task manipulating semantic interference (the picture to be named and the superimposed distractor word were either semantically-related or semantically-unrelated); and a sentence generation task testing the ability to form sequential dependencies. We analyzed accuracy rates using logistic mixed effect models and used deviance table analysis to test for fixed effects of Task, Stream (ventral or dorsal), and their interaction.
Results
There was no effect of Task, Stream (dorsal vs. ventral), or interaction between Task and Stream during cortical stimulation (all p’s > 0.11). During subcortical testing, there was a main effect of Task (Wald χ2 (1) = 6.58, p=0.010): the sentence generation task elicited more errors than the PWI task (see Table 1). Critically, there was also an interaction between Task and Stream (Wald χ2 (1) = 9.50, p=.002): the sentence generation task elicited more errors when tumor resection was performed in the territory of dorsal stream pathways (i.e., the superior longitudinal fasciculus or the arcuate fasciculus) compared to ventral stream pathways (i.e., the inferior fronto-occipital fasciculus or the uncinate fasciculus). For the PWI task, the opposite pattern was observed: there were more errors when tumor resection was performed in the territory of ventral stream pathways compared to dorsal stream pathways (see Table 1).
Conclusions
Our results support a dorsal/ventral role division for white matter pathways involved in language production. In agreement with the model proposed by Bornkessel-Schlesewsky et al. (2015), our results support that dorsal stream pathways are critical for organizing elements in a sequence, which is particularly needed in the generation of sentences, and that ventral stream pathways are critical for the processing of meaning dependencies, probed here through the picture-word interference task.
References
References
Bornkessel-Schlesewsky, I., Schlesewsky, M., Small, S. L., & Rauschecker, J. P. (2015). Neurobiological roots of language in primate audition: common computational properties. Trends in Cognitive Sciences, 19(3), 142–150. https://doi.org/10.1016/j.tics.2014.12.008
Hickok, G., & Poeppel, D. (2007). The cortical organization of speech processing. Nature Reviews. Neuroscience, 8(5), 393–402. https://doi.org/10.1038/nrn2113
Keywords:
awake language mapping,
Dorsal and ventral streams,
Language production,
Sentence generation,
picture-word interference
Conference:
Academy of Aphasia 55th Annual Meeting , Baltimore, United States, 5 Nov - 7 Nov, 2017.
Presentation Type:
oral presentation
Topic:
General Submission
Citation:
Ries
SK,
Piai
V,
Perry
D,
Griffin
S,
Jordan
K,
Knight
RT and
Berger
MS
(2019). Dissociating the roles of ventral versus dorsal pathways in language production: an awake language mapping study.
Conference Abstract:
Academy of Aphasia 55th Annual Meeting .
doi: 10.3389/conf.fnhum.2017.223.00076
Copyright:
The abstracts in this collection have not been subject to any Frontiers peer review or checks, and are not endorsed by Frontiers.
They are made available through the Frontiers publishing platform as a service to conference organizers and presenters.
The copyright in the individual abstracts is owned by the author of each abstract or his/her employer unless otherwise stated.
Each abstract, as well as the collection of abstracts, are published under a Creative Commons CC-BY 4.0 (attribution) licence (https://creativecommons.org/licenses/by/4.0/) and may thus be reproduced, translated, adapted and be the subject of derivative works provided the authors and Frontiers are attributed.
For Frontiers’ terms and conditions please see https://www.frontiersin.org/legal/terms-and-conditions.
Received:
28 Apr 2017;
Published Online:
25 Jan 2019.
*
Correspondence:
Dr. Stephanie K Ries, San Diego State University, School of Speech, Language, and Hearing Sciences, San Diego, United States, sries@sdsu.edu