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

Language Imaging Laboratory, Department of Neurology, Medical College of Wisconsin, Milwaukee, WI 53226, USA.
Cerebral Cortex (Impact Factor: 8.67). 04/2009; 19(12):2767-96. DOI: 10.1093/cercor/bhp055
Source: PubMed


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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    • "When new memories are integrated into long-term memory, this function is taken over by the neocortex so that permanent storage in semantic memory relies on a broadly distributed cortical network (McClelland et al., 1995; Squire and Alvarez , 1995). Previous neuropsychological and neuroimaging studies have further demonstrated this view by showing that anterior temporal neocortices are important for the storage of (long-term) visual and auditory semantic knowledge (Binder et al., 2009; Patterson et al., 2007; Rice et al., 2015; Visser et al., 2010). A meta-analysis has shown that semantic processing in the anterior temporal lobes may depend on the stimulus type: visual object processing (written words, pictures) often recruits ventral anterior temporal lobe structures, while auditory and linguistic processing (spoken words, environmental sounds) tends to rely on lateral anterior temporal lobe structures (Visser et al., 2010). "
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    ABSTRACT: Previous research has indicated that the medial temporal lobe (MTL), and more specifically the perirhinal cortex, plays a role in the feeling of familiarity for non-musical stimuli. Here, we examined contribution of the MTL to the feeling of familiarity for music by testing patients with unilateral MTL lesions. We used a gating paradigm: segments of familiar and unfamiliar musical excerpts were played with increasing durations (250, 500, 1000, 2000, 4000 ms and complete excerpts), and participants provided familiarity judgments for each segment. Based on the hypothesis that patients might need longer segments than healthy controls (HC) to identify excerpts as familiar, we examined the onset of the emergence of familiarity in HC, patients with a right MTL resection (RTR), and patients with a left MTL resection (LTR). In contrast to our hypothesis, we found that the feeling of familiarity was relatively spared in patients with a right or left MTL lesion, even for short excerpts. All participants were able to differentiate familiar from unfamiliar excerpts as early as 500 ms, although the difference between familiar and unfamiliar judgements was greater in HC than in patients. These findings suggest that a unilateral MTL lesion does not impair the emergence of the feeling of familiarity. We also assessed whether the dynamics of the musical excerpt (linked to the type and amount of information contained in the excerpts) modulated the onset of the feeling of familiarity in the three groups. The difference between familiar and unfamiliar judgements was greater for high than for low-dynamic excerpts for HC and RTR patients, but not for LTR patients. This indicates that the LTR group did not benefit in the same way from dynamics. Overall, our results imply that the recognition of previously well-learned musical excerpts does not depend on the integrity of either right or the left MTL structures. Patients with a unilateral MTL resection may compensate for the effects of unilateral damage by using the intact contralateral temporal lobe. Moreover, we suggest that remote semantic memory for music might depend more strongly on neocortical structures rather than the MTL.
    Neuropsychologia 09/2015; DOI:10.1016/j.neuropsychologia.2015.09.007 · 3.30 Impact Factor
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    • "However, even though percentage of correct responses was equivalent for both groups, the pattern of brain activity that emerged from the semantic task differed between younger and older participants . Consistent with our hypothesis, significant age-related changes were found within several key regions of the semantic network: the left IPC, the temporoparietal region bilaterally and, more surprisingly, the left ATL (Binder et al., 2009; Jefferies, 2013; Jefferies & Lambon Ralph, 2006; Patterson et al., 2007; Whitney et al., 2011). The left IPC was more activated in younger participants, while the temporoparietal cortices and the left ATL were more activated in older participants during semantic processing . "
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    ABSTRACT: Semantic memory recruits an extensive neural network including the left inferior prefrontal cortex (IPC) and the left temporoparietal region, which are involved in semantic control processes, as well as the anterior temporal lobe region (ATL) which is considered to be involved in processing semantic information at a central level. However, little is known about the underlying neuronal integrity of the semantic network in normal aging. Young and older healthy adults carried out a semantic judgment task while their cortical activity was recorded using magnetoencephalography (MEG). Despite equivalent behavioral performance, young adults activated the left IPC to a greater extent than older adults, while the latter group recruited the temporoparietal region bilaterally and the left ATL to a greater extent than younger adults. Results indicate that significant neuronal changes occur in normal aging, mainly in regions underlying semantic control processes, despite an apparent stability in performance at the behavioral level. Copyright © 2015 Elsevier Inc. All rights reserved.
    Brain and Language 08/2015; 149:118-127. DOI:10.1016/j.bandl.2015.07.003 · 3.22 Impact Factor
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    • "R. P. Spunt et al. | 7 Lieberman, 2012a,b; Spunt and Adolphs, 2014). These regions partially overlap with several meta-analytically defined functional networks, including: (i) the so-called 'theory-of-mind' or 'mentalizing' network associated with tasks of mental-state reasoning (Gallagher and Frith, 2003; Amodio and Frith, 2006; Saxe, 2006; Carrington and Bailey, 2009; Van Overwalle and Baetens, 2009; Schurz et al., 2014); (ii) the default mode network (DMN), especially its dorsomedial PFC component (Raichle et al., 2001; Buckner et al., 2008; Andrews-Hanna et al., 2010, 2014); (iii) the network associated with mentally simulating episodes both past and future (Hassabis and Maguire, 2007; Spreng et al., 2009; Schacter et al., 2012); (iv) the network associated with comprehending narrative discourse (Ferstl and von Cramon, 2001; Ferstl et al., 2008; Mar, 2011; Nijhof and Willems, 2015); (v) the network associated with transmodal semantic processing (Binder et al., 2009; Binder and Desai, 2011) and (vi) the network associated with comprehending abstract compared to concrete words (Binder et al., 2009; Wang et al., 2010; Binder and Desai, 2011). Decreasing LOAs were associated with the majority of the left hemisphere regions reliably associated with the How > Why contrast in previous work. "
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    ABSTRACT: People can conceptualize the same action (e.g., "riding a bike") at different levels of abstraction (LOA), where higher LOAs specify the abstract motives that explain why the action is performed (e.g., "getting exercise"), while lower LOAs specify the concrete steps that indicate how the action is performed (e.g., "gripping handlebars"). Prior neuroimaging studies have shown that why and how questions about actions differentially activate two cortical networks associated with mental-state reasoning and action representation, respectively; however, it remains unknown whether this is due to the differential demands of the questions per se or to the shifts in LOA those questions produce. We conducted functional MRI while participants judged pairs of action phrases that varied in LOA and that could be framed either as a why question (Why ride a bike? Get exercise.) or a how question (How to get exercise? Ride a bike.). Question framing (why vs. how) had no effect on activity in regions of the two networks. Instead, these regions uniquely tracked parametric variation in LOA, both across and within trials. This suggests that the human capacity to understand actions at different levels of abstraction is based in the relative activity of two cortical networks.
    Social Cognitive and Affective Neuroscience 07/2015; in press. · 7.37 Impact Factor
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