The Neural Organization of Semantic Control: TMS Evidence for a Distributed Network in Left Inferior Frontal and Posterior Middle Temporal Gyrus

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Abstract

Assigning meaning to words, sounds, and objects requires stored conceptual knowledge plus executive mechanisms that shape semantic retrieval according to the task or context. Despite the essential role of control in semantic cognition, its neural basis remains unclear. Neuroimaging and patient research has emphasized the importance of left inferior frontal gyrus (IFG)—however, impaired semantic control can also follow left temporoparietal lesions, suggesting that this function may be underpinned by a large-scale cortical network. We used repetitive transcranial magnetic stimulation in healthy volunteers to disrupt processing within 2 potential sites in this network—IFG and posterior middle temporal cortex. Stimulation of both sites selectively disrupted executively demanding semantic judgments: semantic decisions based on strong automatic associations were unaffected. Performance was also unchanged in nonsemantic tasks—irrespective of their executive demands—and following stimulation of a control site. These results reveal that an extended network of prefrontal and posterior temporal regions underpins semantic control.

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A dual-networks architecture of top-down control.

Nico Dosenbach, Damien A. Fair, Alexander Cohen … (2008)

Complex systems ensure resilience through multiple controllers acting at rapid and slower timescales. The need for efficient information flow through complex systems encourages small-world network structures. On the basis of these principles, a group of regions associated with top-down control was examined. Functional magnetic resonance imaging showed that each region had a specific combination of control signals; resting-state functional connectivity grouped the regions into distinct 'fronto-parietal' and 'cingulo-opercular' components. The fronto-parietal component seems to initiate and adjust control; the cingulo-opercular component provides stable 'set-maintenance' over entire task epochs. Graph analysis showed dense local connections within components and weaker 'long-range' connections between components, suggesting a small-world architecture. The control systems of the brain seem to embody the principles of complex systems, encouraging resilient performance.

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Dorsal and ventral streams: a framework for understanding aspects of the functional anatomy of language.

Gregory Hickok, David Poeppel (2004)

Despite intensive work on language-brain relations, and a fairly impressive accumulation of knowledge over the last several decades, there has been little progress in developing large-scale models of the functional anatomy of language that integrate neuropsychological, neuroimaging, and psycholinguistic data. Drawing on relatively recent developments in the cortical organization of vision, and on data from a variety of sources, we propose a new framework for understanding aspects of the functional anatomy of language which moves towards remedying this situation. The framework posits that early cortical stages of speech perception involve auditory fields in the superior temporal gyrus bilaterally (although asymmetrically). This cortical processing system then diverges into two broad processing streams, a ventral stream, which is involved in mapping sound onto meaning, and a dorsal stream, which is involved in mapping sound onto articulatory-based representations. The ventral stream projects ventro-laterally toward inferior posterior temporal cortex (posterior middle temporal gyrus) which serves as an interface between sound-based representations of speech in the superior temporal gyrus (again bilaterally) and widely distributed conceptual representations. The dorsal stream projects dorso-posteriorly involving a region in the posterior Sylvian fissure at the parietal-temporal boundary (area Spt), and ultimately projecting to frontal regions. This network provides a mechanism for the development and maintenance of "parity" between auditory and motor representations of speech. Although the proposed dorsal stream represents a very tight connection between processes involved in speech perception and speech production, it does not appear to be a critical component of the speech perception process under normal (ecologically natural) listening conditions, that is, when speech input is mapped onto a conceptual representation. We also propose some degree of bi-directionality in both the dorsal and ventral pathways. We discuss some recent empirical tests of this framework that utilize a range of methods. We also show how damage to different components of this framework can account for the major symptom clusters of the fluent aphasias, and discuss some recent evidence concerning how sentence-level processing might be integrated into the framework.

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Meta-analyzing left hemisphere language areas: phonology, semantics, and sentence processing.

M Vigneau, V Beaucousin, P Hervé … (2006)

The advent of functional neuroimaging has allowed tremendous advances in our understanding of brain-language relationships, in addition to generating substantial empirical data on this subject in the form of thousands of activation peak coordinates reported in a decade of language studies. We performed a large-scale meta-analysis of this literature, aimed at defining the composition of the phonological, semantic, and sentence processing networks in the frontal, temporal, and inferior parietal regions of the left cerebral hemisphere. For each of these language components, activation peaks issued from relevant component-specific contrasts were submitted to a spatial clustering algorithm, which gathered activation peaks on the basis of their relative distance in the MNI space. From a sample of 730 activation peaks extracted from 129 scientific reports selected among 260, we isolated 30 activation clusters, defining the functional fields constituting three distributed networks of frontal and temporal areas and revealing the functional organization of the left hemisphere for language. The functional role of each activation cluster is discussed based on the nature of the tasks in which it was involved. This meta-analysis sheds light on several contemporary issues, notably on the fine-scale functional architecture of the inferior frontal gyrus for phonological and semantic processing, the evidence for an elementary audio-motor loop involved in both comprehension and production of syllables including the primary auditory areas and the motor mouth area, evidence of areas of overlap between phonological and semantic processing, in particular at the location of the selective human voice area that was the seat of partial overlap of the three language components, the evidence of a cortical area in the pars opercularis of the inferior frontal gyrus dedicated to syntactic processing and in the posterior part of the superior temporal gyrus a region selectively activated by sentence and text processing, and the hypothesis that different working memory perception-actions loops are identifiable for the different language components. These results argue for large-scale architecture networks rather than modular organization of language in the left hemisphere.

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Author and article information

Journal

Journal ID (nlm-ta): Cereb Cortex

Journal ID (hwp): cercor

Journal ID (publisher-id): cercor

Title: Cerebral Cortex (New York, NY)

Publisher: Oxford University Press

ISSN (Print): 1047-3211

ISSN (Electronic): 1460-2199

Publication date (Print): May 2011

Publication date (Electronic): 17 September 2010

Publication date PMC-release: 17 September 2010

Volume: 21

Issue: 5

Pages: 1066-1075

Affiliations

[1 ]Department of Psychology and York Neuroimaging Centre, University of York, YO10 5DD York, UK

[2 ]Neuroscience and Aphasia Research Unit, School of Psychological Sciences, University of Manchester, M19 9PL Manchester, UK

Author notes

Address correspondence to Carin Whitney, Department of Psychology, University of York, YO10 5DD York, UK. Email: c.whitney@ 123456psych.york.ac.uk .

Article

DOI: 10.1093/cercor/bhq180

PMC ID: 3077429

PubMed ID: 20851853

SO-VID: d2f71bbb-ace2-4962-a625-f84669dd4d70

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This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License ( http://creativecommons.org/licenses/by-nc/2.5), which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

The Neural Organization of Semantic Control: TMS Evidence for a Distributed Network in Left Inferior Frontal and Posterior Middle Temporal Gyrus

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Abstract

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Karger: Neurology and Neuroscience

Most cited references 72

A dual-networks architecture of top-down control.

Dorsal and ventral streams: a framework for understanding aspects of the functional anatomy of language.

Meta-analyzing left hemisphere language areas: phonology, semantics, and sentence processing.

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