Anterior temporal lobes mediate semantic representation: Mimicking semantic dementia by using rTMS in normal participants

Neuroscience and Aphasia Research Unit, School of Psychological Sciences, University of Manchester, Manchester M13 9PL, United Kingdom.
Proceedings of the National Academy of Sciences (Impact Factor: 9.67). 01/2008; 104(50):20137-41. DOI: 10.1073/pnas.0707383104
Source: PubMed


Studies of semantic dementia and PET neuroimaging investigations suggest that the anterior temporal lobes (ATL) are a critical substrate for semantic representation. In stark contrast, classical neurological models of comprehension do not include ATL, and likewise functional MRI studies often fail to show activations in the ATL, reinforcing the classical view. Using a novel application of low-frequency, repetitive transcranial magnetic stimulation (rTMS) over the ATL, we demonstrate that the behavioral pattern of semantic dementia can be mirrored in neurologically intact participants: Specifically, we show that temporary disruption to neural processing in the ATL produces a selective semantic impairment leading to significant slowing in both picture naming and word comprehension but not to other equally demanding, nonsemantic cognitive tasks.

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Available from: Elizabeth Jefferies, Sep 16, 2015
    • "A similar method of ATL disruption was used very recently by Jackson, Lambon Ralph, and Pobric (2015). Other authors (Pobric et al., 2007, 2009 and 2010; Chiou, Sowman, Etchell, & Rich, 2014; Lambon Ralph et al., 2009) previously used rTMS of the right and left TP to obtain novel evidence supporting the 'semantic hub' hypothesis with an ''offline'' approach, i.e. comparing the performance obtained during the temporary refractory period with that obtained on the same task outside this refractory window. Here we aimed to obtain a time-locked disruption of the neural activity of the right or left TP in concomitance with the presentation of each face and name whose familiarity had to be assessed. "
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    ABSTRACT: The aims of the present experiment was to investigate: (a) if transient disruption of neural activity in the right (RTP) or left temporal pole (LTP) can interfere with the development of a familiarity feeling to the presentation of faces/written names of famous/unknown people; and (b) if this interference specifically affects the familiarity for faces after inhibition of the RTP and for names after inhibition of the LTP. Twenty healthy volunteers took part in the study. Repetitive transcranial magnetic stimulation (rTMS) was administered online; it disrupted the neural activity of the right or left TP in concomitance with the presentation of each face and name whose familiarity had to be assessed. Furthermore, in a control group, each participant was submitted to a single experimental session in which rTMS was delivered to the vertex in association with the presentation of faces and written names. Since previous rTMS studies have shown that the temporary inactivation of the right and left TP influences the response latencies, but not the number of correct responses, in this study we took into account both the number of correct responses obtained in different experimental conditions and the corresponding response latencies. A three-way factorial ANOVA carried out on the Response Scores showed only a general effect of the Type of Stimuli, due to better performances on names than on faces. This greater familiarity of names is consistent with previous data reported in the literature. In the three-way factorial ANOVA carried out on the Latency Scores, post-hoc analyses showed an increased latency of responses to faces after right stimulation in Latency Total, Latency on Correct responses and Latency on Unfamiliar faces. None of these results were obtained in the control group. These data suggest that rTMS at the level of the RTP preferentially affects the development of familiarity feelings to the presentation of faces of famous people.
    Neurobiology of Learning and Memory 09/2015; 125:15-23. DOI:10.1016/j.nlm.2015.07.010 · 3.65 Impact Factor
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    • "In contrast, evidence in support of the social knowledge hypothesis mostly relies on studies in which the person knowledge has been investigated only at a very specific level of representation (i.e., famous or familiar persons ). It is worth noting that specific level entities are also more demanding for the semantic system, and that some recent fMRI (Visser & Lambon Ralph, 2011) and TMS (Pobric, Jefferies and Lambon Ralph, 2007) studies showed that the ATL is also implicated in processing subordinate or basic level concepts. Thus, there are three possible hypotheses about the role plaid by ATL: it might only deal with the specific-level of processing (irrespective of the category), as suggested by Martin (2007), it might selectively process social knowledge (Skipper et al., 2011) or it might represent multimodal semantic concepts (Rogers et al., 2004). "
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    ABSTRACT: A person can be appraised as an individual or as a member of a social group. In the present study we tested whether the knowledge about social groups is represented independently of the living and non-living things. Patients with frontal and temporal lobe tumors involving either the left or the right hemisphere performed three tasks - picture naming, word-to-picture matching and picture sorting - tapping the lexical semantic knowledge of living things, non-living things and social groups. Both behavioral and voxel-based lesion-symptom mapping (VLSM) analyses suggested that social groups might be represented differently from other categories. VLSM analysis carried out on naming errors revealed that left-lateralized lesions in the inferior frontal gyrus, amygdala, insula and basal ganglia were associated with the lexical-semantic processing of social groups. These findings indicate that the social group representation may rely on areas associated with affective processing. Copyright © 2015 Elsevier Ltd. All rights reserved.
    Cortex 07/2015; 70. DOI:10.1016/j.cortex.2015.06.024 · 5.13 Impact Factor
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    • "Research attention has now shifted to exploring how conceptual knowledge is represented within this bilateral system, with a particular focus on the functions of the right and left ATLs (Olson et al. 2007; Pobric et al. 2007; Lambon Ralph et al. 2009; Pobric et al. 2010; Visser, Jefferies, et al. 2010; Drane et al. 2013; Gainotti 2012, 2013; Wong and Gallate 2012; Olson et al. 2013). This largescale meta-analysis focused on this issue and formally evaluated four prominent accounts from the literature. "
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    ABSTRACT: The roles of the right and left anterior temporal lobes (ATLs) in conceptual knowledge are a source of debate between 4 conflicting accounts. Possible ATL specializations include: (1) Processing of verbal versus non-verbal inputs; (2) the involvement of word retrieval; and (3) the social content of the stimuli. Conversely, the "hub-and-spoke" account holds that both ATLs form a bilateral functionally unified system. Using activation likelihood estimation (ALE) to compare the probability of left and right ATL activation, we analyzed 97 functional neuroimaging studies of conceptual knowledge, organized according to the predictions of the three specialized hypotheses. The primary result was that ATL activation was predominately bilateral and highly overlapping for all stimulus types. Secondary to this bilateral representation, there were subtle gradations both between and within the ATLs. Activations were more likely to be left lateralized when the input was a written word or when word retrieval was required. These data are best accommodated by a graded version of the hub-and-spoke account, whereby representation of conceptual knowledge is supported through bilateral yet graded connectivity between the ATLs and various modality-specific sensory, motor, and limbic cortices. © The Author 2015. Published by Oxford University Press.
    Cerebral Cortex 03/2015; DOI:10.1093/cercor/bhv024 · 8.67 Impact Factor
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