Cargando…

Recursive hierarchical embedding in vision is impaired by posterior middle temporal gyrus lesions

The generation of hierarchical structures is central to language, music and complex action. Understanding this capacity and its potential impairments requires mapping its underlying cognitive processes to the respective neuronal underpinnings. In language, left inferior frontal gyrus and left poster...

Descripción completa

Detalles Bibliográficos
Autores principales: Martins, Mauricio J D, Krause, Carina, Neville, David A, Pino, Daniele, Villringer, Arno, Obrig, Hellmuth
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6763734/
https://www.ncbi.nlm.nih.gov/pubmed/31560064
http://dx.doi.org/10.1093/brain/awz242
_version_ 1783454261593505792
author Martins, Mauricio J D
Krause, Carina
Neville, David A
Pino, Daniele
Villringer, Arno
Obrig, Hellmuth
author_facet Martins, Mauricio J D
Krause, Carina
Neville, David A
Pino, Daniele
Villringer, Arno
Obrig, Hellmuth
author_sort Martins, Mauricio J D
collection PubMed
description The generation of hierarchical structures is central to language, music and complex action. Understanding this capacity and its potential impairments requires mapping its underlying cognitive processes to the respective neuronal underpinnings. In language, left inferior frontal gyrus and left posterior temporal cortex (superior temporal sulcus/middle temporal gyrus) are considered hubs for syntactic processing. However, it is unclear whether these regions support computations specific to language or more generally support analyses of hierarchical structure. Here, we address this issue by investigating hierarchical processing in a non-linguistic task. We test the ability to represent recursive hierarchical embedding in the visual domain by contrasting a recursion task with an iteration task. The recursion task requires participants to correctly identify continuations of a hierarchy generating procedure, while the iteration task applies a serial procedure that does not generate new hierarchical levels. In a lesion-based approach, we asked 44 patients with left hemispheric chronic brain lesion to perform recursion and iteration tasks. We modelled accuracies and response times with a drift diffusion model and for each participant obtained parametric estimates for the velocity of information accumulation (drift rates) and for the amount of information accumulated before a decision (boundary separation). We then used these estimates in lesion-behaviour analyses to investigate how brain lesions affect specific aspects of recursive hierarchical embedding. We found that lesions in the posterior temporal cortex decreased drift rate in recursive hierarchical embedding, suggesting an impaired process of rule extraction from recursive structures. Moreover, lesions in inferior temporal gyrus decreased boundary separation. The latter finding does not survive conservative correction but suggests a shift in the decision criterion. As patients also participated in a grammar comprehension experiment, we performed explorative correlation-analyses and found that visual and linguistic recursive hierarchical embedding accuracies are correlated when the latter is instantiated as sentences with two nested embedding levels. While the roles of the inferior temporal gyrus and posterior temporal cortex in linguistic processes are well established, here we show that posterior temporal cortex lesions slow information accumulation (drift rate) in the visual domain. This suggests that posterior temporal cortex is essential to acquire the (knowledge) representations necessary to parse recursive hierarchical embedding in visual structures, a finding mimicking language acquisition in young children. On the contrary, inferior frontal gyrus lesions seem to affect recursive hierarchical embedding processing by interfering with more general cognitive control (boundary separation). This interesting separation of roles, rooted on a domain-general taxonomy, raises the question of whether such cognitive framing is also applicable to other domains.
format Online
Article
Text
id pubmed-6763734
institution National Center for Biotechnology Information
language English
publishDate 2019
publisher Oxford University Press
record_format MEDLINE/PubMed
spelling pubmed-67637342019-10-02 Recursive hierarchical embedding in vision is impaired by posterior middle temporal gyrus lesions Martins, Mauricio J D Krause, Carina Neville, David A Pino, Daniele Villringer, Arno Obrig, Hellmuth Brain Original Articles The generation of hierarchical structures is central to language, music and complex action. Understanding this capacity and its potential impairments requires mapping its underlying cognitive processes to the respective neuronal underpinnings. In language, left inferior frontal gyrus and left posterior temporal cortex (superior temporal sulcus/middle temporal gyrus) are considered hubs for syntactic processing. However, it is unclear whether these regions support computations specific to language or more generally support analyses of hierarchical structure. Here, we address this issue by investigating hierarchical processing in a non-linguistic task. We test the ability to represent recursive hierarchical embedding in the visual domain by contrasting a recursion task with an iteration task. The recursion task requires participants to correctly identify continuations of a hierarchy generating procedure, while the iteration task applies a serial procedure that does not generate new hierarchical levels. In a lesion-based approach, we asked 44 patients with left hemispheric chronic brain lesion to perform recursion and iteration tasks. We modelled accuracies and response times with a drift diffusion model and for each participant obtained parametric estimates for the velocity of information accumulation (drift rates) and for the amount of information accumulated before a decision (boundary separation). We then used these estimates in lesion-behaviour analyses to investigate how brain lesions affect specific aspects of recursive hierarchical embedding. We found that lesions in the posterior temporal cortex decreased drift rate in recursive hierarchical embedding, suggesting an impaired process of rule extraction from recursive structures. Moreover, lesions in inferior temporal gyrus decreased boundary separation. The latter finding does not survive conservative correction but suggests a shift in the decision criterion. As patients also participated in a grammar comprehension experiment, we performed explorative correlation-analyses and found that visual and linguistic recursive hierarchical embedding accuracies are correlated when the latter is instantiated as sentences with two nested embedding levels. While the roles of the inferior temporal gyrus and posterior temporal cortex in linguistic processes are well established, here we show that posterior temporal cortex lesions slow information accumulation (drift rate) in the visual domain. This suggests that posterior temporal cortex is essential to acquire the (knowledge) representations necessary to parse recursive hierarchical embedding in visual structures, a finding mimicking language acquisition in young children. On the contrary, inferior frontal gyrus lesions seem to affect recursive hierarchical embedding processing by interfering with more general cognitive control (boundary separation). This interesting separation of roles, rooted on a domain-general taxonomy, raises the question of whether such cognitive framing is also applicable to other domains. Oxford University Press 2019-10 2019-09-27 /pmc/articles/PMC6763734/ /pubmed/31560064 http://dx.doi.org/10.1093/brain/awz242 Text en © The Author(s) (2019). Published by Oxford University Press on behalf of the Guarantors of Brain. http://creativecommons.org/licenses/by-nc/4.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com
spellingShingle Original Articles
Martins, Mauricio J D
Krause, Carina
Neville, David A
Pino, Daniele
Villringer, Arno
Obrig, Hellmuth
Recursive hierarchical embedding in vision is impaired by posterior middle temporal gyrus lesions
title Recursive hierarchical embedding in vision is impaired by posterior middle temporal gyrus lesions
title_full Recursive hierarchical embedding in vision is impaired by posterior middle temporal gyrus lesions
title_fullStr Recursive hierarchical embedding in vision is impaired by posterior middle temporal gyrus lesions
title_full_unstemmed Recursive hierarchical embedding in vision is impaired by posterior middle temporal gyrus lesions
title_short Recursive hierarchical embedding in vision is impaired by posterior middle temporal gyrus lesions
title_sort recursive hierarchical embedding in vision is impaired by posterior middle temporal gyrus lesions
topic Original Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6763734/
https://www.ncbi.nlm.nih.gov/pubmed/31560064
http://dx.doi.org/10.1093/brain/awz242
work_keys_str_mv AT martinsmauriciojd recursivehierarchicalembeddinginvisionisimpairedbyposteriormiddletemporalgyruslesions
AT krausecarina recursivehierarchicalembeddinginvisionisimpairedbyposteriormiddletemporalgyruslesions
AT nevilledavida recursivehierarchicalembeddinginvisionisimpairedbyposteriormiddletemporalgyruslesions
AT pinodaniele recursivehierarchicalembeddinginvisionisimpairedbyposteriormiddletemporalgyruslesions
AT villringerarno recursivehierarchicalembeddinginvisionisimpairedbyposteriormiddletemporalgyruslesions
AT obrighellmuth recursivehierarchicalembeddinginvisionisimpairedbyposteriormiddletemporalgyruslesions