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

doi:10.1093/CERCOR/BHQ180

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

Journal Article•DOI•

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

Carin Whitney¹, Marie Kirk¹, Jamie O'Sullivan¹, Matthew A. Lambon Ralph², Elizabeth Jefferies¹ - Show less +1 more•Institutions (2)

University of York¹, University of Manchester²

01 May 2011-Cerebral Cortex (Oxford University Press)-Vol. 21, Iss: 5, pp 1066-1075

TL;DR: Stimulation of left inferior frontal gyrus and posterior middle temporal cortex with repetitive transcranial magnetic stimulation reveals that an extended network of prefrontal and posterior temporal regions underpins semantic control.

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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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Journal Article•DOI•

The neural and computational bases of semantic cognition

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Matthew A. Lambon Ralph¹, Elizabeth Jefferies², Karalyn Patterson³, Timothy T. Rogers⁴•Institutions (4)

University of Manchester¹, University of York², Cognition and Brain Sciences Unit³, University of Wisconsin-Madison⁴

01 Jan 2017-Nature Reviews Neuroscience

TL;DR: This Review summarizes key findings and issues arising from a decade of research into the neurocognitive and neurocomputational underpinnings of semantic cognition, leading to a new framework that is term controlled semantic cognition (CSC).

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Abstract: Semantic cognition refers to our ability to use, manipulate and generalize knowledge that is acquired over the lifespan to support innumerable verbal and non-verbal behaviours. This Review summarizes key findings and issues arising from a decade of research into the neurocognitive and neurocomputational underpinnings of this ability, leading to a new framework that we term controlled semantic cognition (CSC). CSC offers solutions to long-standing queries in philosophy and cognitive science, and yields a convergent framework for understanding the neural and computational bases of healthy semantic cognition and its dysfunction in brain disorders.

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1,094 citations

Journal Article•DOI•

Semantic dementia: progressive fluent aphasia with temporal lobe atrophy

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John R. Hodges

01 Jan 1995-Neurocase

TL;DR: The term semantic dementia is proposed, first coined by Snowden et al. (1989), to designate this clinical syndrome characterized by fluent dysphasia with severe anomia, reduced vocabulary and prominent impairment of single-word comprehension, progressing to a stage of virtually complete dissolution of the semantic components of language.

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Abstract: We report five patients with a stereotyped clinical syndrome characterized by fluent dysphasia with severe anomia, reduced vocabulary and prominent impairment of single-word comprehension, progressing to a stage of virtually complete dissolution of the semantic components of language. A marked reduction in the ability to generate exemplars from restricted semantic categories (e.g. animals, vehicles, etc.) was a consistent and early feature. Tests of semantic memory demonstrated a radically impoverished knowledge about a range of living and man-made items. In contrast, phonology and grammar of spoken language were largely preserved, as was comprehension of complex syntactic commands. Reading showed a pattern of surface dyslexia. Autobiographical and day-to-day (episodic) memory were relatively retained. Non-verbal memory, perceptual and visuospatial abilities were also strikingly preserved. In some cases, behavioural and personality changes may supervene; one patient developed features of the Kluver-Bucy Syndrome. Radiological investigations have shown marked focal temporal atrophy in all five patients, and functional imaging by single positron emission tomography and positron emission tomography (one case) have implicated the dominant temporal lobe in all five. In the older literature, such cases would have been subsumed under the rubric of Pick's disease. Others have been included in series with progressive aphasia. We propose the term semantic dementia, first coined by Snowden et al. (1989), to designate this clinical syndrome.

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606 citations

Journal Article•DOI•

Going beyond Inferior Prefrontal Involvement in Semantic Control: Evidence for the Additional Contribution of Dorsal Angular Gyrus and Posterior Middle Temporal Cortex

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Krist A. Noonan, Elizabeth Jefferies¹, Maya Visser², Matthew A. Lambon Ralph²•Institutions (2)

University of York¹, University of Manchester²

30 Sep 2013-Journal of Cognitive Neuroscience

TL;DR: A formal meta-analysis of studies that contrasted semantic tasks with high > low executive requirements to determine whether cortical regions beyond the left pFC show the same response profile to executive semantic demands revealed substantial overlap between the two sets of contrasts within left ventral pFC.

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Abstract: Semantic cognition requires a combination of semantic representations and executive control processes to direct activation in a task- and time-appropriate fashion [Jefferies, E., & Lambon Ralph, M. A. Semantic impairment in stroke aphasia versus semantic dementia: A case-series comparison. Brain, 129, 2132-2147, 2006]. We undertook a formal meta-analysis to investigate which regions within the large-scale semantic network are specifically associated with the executive component of semantic cognition. Previous studies have described in detail the role of left ventral pFC in semantic regulation. We examined 53 studies that contrasted semantic tasks with high > low executive requirements to determine whether cortical regions beyond the left pFC show the same response profile to executive semantic demands. Our findings revealed that right pFC, posterior middle temporal gyrus (pMTG) and dorsal angular gyrus (bordering intraparietal sulcus) were also consistently recruited by executively demanding semantic tasks, demonstrating patterns of activation that were highly similar to the left ventral pFC. These regions overlap with the lesions in aphasic patients who exhibit multimodal semantic impairment because of impaired regulatory control (semantic aphasia)-providing important convergence between functional neuroimaging and neuropsychological studies of semantic cognition. Activation in dorsal angular gyrus and left ventral pFC was consistent across all types of executive semantic manipulation, regardless of whether the task was receptive or expressive, whereas pMTG activation was only observed for manipulation of control demands within receptive tasks. Second, we contrasted executively demanding tasks tapping semantics and phonology. Our findings revealed substantial overlap between the two sets of contrasts within left ventral pFC, suggesting this region underpins domain-general control mechanisms. In contrast, we observed relative specialization for semantic control within pMTG as well as the most ventral aspects of left pFC (BA 47), consistent with our proposal of a distributed network underpinning semantic control.

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412 citations

Cites background from "The Neural Organization of Semantic..."

...…TMS to ventral pFC and pMTG produced equal disruption of two tasks with high semantic control demands tapping the controlled retrieval of distant associations and the selection of specific semantic features respectively but left a low-control semantic task unaffected (Whitney et al., 2010)....
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...…are supported by evidence from TMS studies in healthy control participants: Stimulation of pMTG and ventral pFC produced an equivalent and selective decrement on executively demanding semantic decisions, with sparing of judgments based on automatic semantic associations (Whitney et al., 2010)....
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...In sharp contrast to this strong dissociation between left pFC and pMTG in the expressive domain, TMS to LIFG and pMTG disrupts comprehension tasks with high control demands to an equal degree (Whitney et al., 2010)....
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...…whereas damage or stimulation to pFC, pMTG, or IPS/dAG compromises semantic control (Robson, Sage, & Lambon Ralph, 2012; Pobric et al., 2010; Whitney et al., 2010; Lambon Ralph, Pobric, & Jefferies, 2009; Schwartz et al., 2009; Pobric, Jefferies, & Lambon Ralph, 2007; Jefferies & Lambon…...
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Journal Article•DOI•

The neural basis of semantic cognition: Converging evidence from neuropsychology, neuroimaging and TMS

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Elizabeth Jefferies¹•Institutions (1)

University of York¹

01 Mar 2013-Cortex

TL;DR: The next challenges are to delineate the specific roles of each region within the semantic control network and to specify the way in which control processes interact with semantic representations to focus processing on relevant features of concepts.

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409 citations

Cites background or methods or result from "The Neural Organization of Semantic..."

...…able to demonstrate a functional dissociation between ATL and pMTG within a single fMRI study utilising ambiguous words in a double-prime paradigm (Whitney et al., 2011a): ATL was sensitive to the number of meanings that were retrieved, consistent with a role for this region in semantic…...
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...We have also used TMS to investigate the wider neural network underpinning semantic control for words, by contrasting the effects of stimulation of LIFG and pMTG (Whitney et al., 2011b)....
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...0010-9452/$ e see front matter ª 2012 Elsev http://dx.doi.org/10.1016/j.cortex.2012.10.008 a b s t r a c t Recent studies suggest that a complex, distributed neural network underpins semantic cognition....
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Journal Article•DOI•

Both the middle temporal gyrus and the ventral anterior temporal area are crucial for multimodal semantic processing: Distortion-corrected fmri evidence for a double gradient of information convergence in the temporal lobes

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Maya Visser¹, Elizabeth Jefferies², K.V. Embleton¹, Matthew A. Lambon Ralph¹•Institutions (2)

University of Manchester¹, University of York²

01 Aug 2012-Journal of Cognitive Neuroscience

TL;DR: Both MTG and vATL are activated in common for word and picture semantic processing, and this result follows from two principal axes of convergence in the temporal lobe.

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Abstract: Most contemporary theories of semantic memory assume that concepts are formed from the distillation of information arising in distinct sensory and verbal modalities. The neural basis of this distillation or convergence of information was the focus of this study. Specifically, we explored two commonly posed hypotheses: (a) that the human middle temporal gyrus (MTG) provides a crucial semantic interface given the fact that it interposes auditory and visual processing streams and (b) that the anterior temporal region-especially its ventral surface (vATL)-provides a critical region for the multimodal integration of information. By utilizing distortion-corrected fMRI and an established semantic association assessment (commonly used in neuropsychological investigations), we compared the activation patterns observed for both the verbal and nonverbal versions of the same task. The results are consistent with the two hypotheses simultaneously: Both MTG and vATL are activated in common for word and picture semantic processing. Additional planned, ROI analyses show that this result follows from two principal axes of convergence in the temporal lobe: both lateral (toward MTG) and longitudinal (toward the anterior temporal lobe).

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309 citations

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Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research

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Simone Rossi¹, Mark Hallett, Paolo Maria Rossini, Alvaro Pascual-Leone²•Institutions (2)

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TL;DR: The present updated guidelines review issues of risk and safety of conventional TMS protocols, address the undesired effects and risks of emerging TMS interventions, the applications of TMS in patients with implanted electrodes in the central nervous system, and safety aspects of T MS in neuroimaging environments.

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"The Neural Organization of Semantic..." refers methods in this paper

...A standard offline virtual lesion rTMS protocol was used, which was compatible with established TMS safety guidelines (Wassermann 1998; Rossi et al. 2009)....
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...TMS Protocol A standard offline virtual lesion rTMS protocol was used, which was compatible with established TMS safety guidelines (Wassermann 1998; Rossi et al. 2009)....
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3,672 citations

"The Neural Organization of Semantic..." refers background or methods in this paper

...Cognitive control demands were expected to be minimal in these trials because global shape is visually dominant over local features (Navon 1977)....
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...Nonsemantic control tasks with the same decision/response demands as the semantic trials were constructed from the Navon letter-matching task (Navon 1977)....
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...To examine the specificity of these effects, participants performed easy and difficult versions of a nonsemantic letter-matching task (Navon 1977), for which no...
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...To examine the specificity of these effects, participants performed easy and difficult versions of a nonsemantic letter-matching task (Navon 1977), for which no interference with rTMS was expected....
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Journal Article•DOI•

Where Is the Semantic System? A Critical Review and Meta-Analysis of 120 Functional Neuroimaging Studies

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Jeffrey R. Binder¹, Rutvik H. Desai¹, William W. Graves¹, Lisa L. Conant¹•Institutions (1)

Medical College of Wisconsin¹

01 Dec 2009-Cerebral Cortex

TL;DR: In this article, the authors analyzed 120 functional neuroimaging studies focusing on semantic processing and identified reliable areas of activation in these studies using the activation likelihood estimate (ALE) technique, which formed a distinct, left-lateralized network comprised of 7 regions: posterior inferior parietal lobe, middle temporal gyrus, fusiform and parahippocampal gyri, dorsomedial prefrontal cortex, inferior frontal gyrus and posterior cingulate gyrus.

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Abstract: Semantic memory refers to knowledge about people, objects, actions, relations, self, and culture acquired through experience. The neural systems that store and retrieve this information have been studied for many years, but a consensus regarding their identity has not been reached. Using strict inclusion criteria, we analyzed 120 functional neuroimaging studies focusing on semantic processing. Reliable areas of activation in these studies were identified using the activation likelihood estimate (ALE) technique. These activations formed a distinct, left-lateralized network comprised of 7 regions: posterior inferior parietal lobe, middle temporal gyrus, fusiform and parahippocampal gyri, dorsomedial prefrontal cortex, inferior frontal gyrus, ventromedial prefrontal cortex, and posterior cingulate gyrus. Secondary analyses showed specific subregions of this network associated with knowledge of actions, manipulable artifacts, abstract concepts, and concrete concepts. The cortical regions involved in semantic processing can be grouped into 3 broad categories: posterior multimodal and heteromodal association cortex, heteromodal prefrontal cortex, and medial limbic regions. The expansion of these regions in the human relative to the nonhuman primate brain may explain uniquely human capacities to use language productively, plan, solve problems, and create cultural and technological artifacts, all of which depend on the fluid and efficient retrieval and manipulation of semantic knowledge.

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3,283 citations

Journal Article•DOI•

Common regions of the human frontal lobe recruited by diverse cognitive demands.

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John S. Duncan¹, Adrian M. Owen¹•Institutions (1)

Cognition and Brain Sciences Unit¹

01 Oct 2000-Trends in Neurosciences

TL;DR: In this paper, the authors reviewed patterns of frontal-lobe activation associated with a broad range of different cognitive demands, including aspects of perception, response selection, executive control, working memory, episodic memory and problem solving.

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2,429 citations

"The Neural Organization of Semantic..." refers background or result in this paper

...Moreover, this research is consistent with the view that the prefrontal cortex is of fundamental importance in executive control across a wide range of cognitive domains (Duncan and Owen 2000; Owen et al. 2000; Petrides 2005; Duncan 2006, 2010; Badre and D’Esposito 2007; Badre 2008)....
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...…both semantic and nonsemantic, including inferior frontal sulcus, dorsolateral prefrontal cortex, supplementary motor areas, adjacent cingulate cortex, and areas in and around the intraparietal sulcus (Duncan and Owen 2000; Wager et al. 2004; Dosenbach et al. 2008; Nagel et al. 2008; Duncan 2010)....
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