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Review
. 2009 Dec;19(12):2767-96.
doi: 10.1093/cercor/bhp055. Epub 2009 Mar 27.

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

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Free PMC article
Review

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

Jeffrey R Binder et al. Cereb Cortex. .
Free PMC article

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.

Figures

Figure 1.
Figure 1.
Distribution of the included studies by year published.
Figure 2.
Figure 2.
One thousand one hundred and thirty-five published activation foci from the included studies projected onto an inflated cortical surface.
Figure 3.
Figure 3.
ALE map of all semantic foci, thresholded at whole-brain corrected P < 0.05. Activations are displayed on serial sagittal sections through the stereotaxic space of Talairach and Tournoux (1988) at 4-mm intervals, with slice locations given at the lower left of each image. Green lines indicate the stereotaxic y and z axes. Tick marks indicate 10-mm intervals. The color scale indicates voxelwise probability values of P < 0.01 (red), P < 0.001 (orange), and P < 0.0001 (yellow).
Figure 4.
Figure 4.
ALE map of 691 foci resulting from general semantic contrasts (see Methods for details). Formatting and thresholding as in Figure 3.
Figure 5.
Figure 5.
ALE map of 29 foci resulting from contrasts targeting knowledge of manipulable artifacts (top) and ALE map of 40 foci from contrasts targeting knowledge of actions (bottom). Formatting and thresholding as in previous figures.
Figure 6.
Figure 6.
ALE maps derived from contrasts comparing perceptual (i.e., pertaining to sensory attributes of concrete objects) with verbal (i.e., abstract or encyclopedic) knowledge. The 113 foci representing perceptual knowledge are shown in warm colors, and the 34 foci representing verbal knowledge are shown in cool colors. Formatting and thresholding as in previous figures.
Figure 7.
Figure 7.
Summary diagrams comparing (A) the large-scale semantic network of the human brain and (B) a probable homologous network in the macaque monkey brain, comprised of posterior inferior parietal cortex (PG/7a), STS, parahippocampal cortex (TF, TH), dorsolateral prefrontal cortex, posterior cingulate and retrosplenial cortex, lateral orbital frontal cortex, and VMPFC. Green lines indicate the principal cortical connections of these regions in the monkey, based on studies using anterograde and retrograde tracer techniques (Jones and Powell 1970; Seltzer and Pandya 1976, 1978, 1984, 1989, 1994; Mesulam et al. 1977; Baleydier and Mauguiere 1980; Leichnitz 1980; Petrides and Pandya 1984; Vogt and Pandya 1987; Selemon and Goldman-Rakic 1988; Cavada and Goldman-Rakic 1989a, 1989b; Andersen et al. 1990; Barbas 1993; Morris et al. 1999; Cavada 2000; Blatt et al. 2003; Kobayashi and Amaral 2003, 2007; Padberg et al. 2003; Parvizi et al. 2006; Saleem et al. 2007). All connections indicated are monosynaptic and reciprocal.
Figure 8.
Figure 8.
Comparison of the left-hemisphere general semantic network indicated in the present ALE meta-analysis (top) and the “default network” (bottom). The latter map represents brain areas that showed task-induced deactivation during performance of a tone discrimination task, that is, higher BOLD signal during a conscious resting baseline compared with the tone task (see Binder et al. 2008 for details). In both types of studies, effects are observed in the AG, posterior cingulate gyrus, DMPFC, VMPFC, ventral temporal lobe, anterior MTG, and ventral IFG. Although effects are stronger in the left hemisphere for both kinds of studies, task-induced deactivation is typically more symmetrical in posterior cingulate and medial prefrontal regions (Shulman et al. 1997; Binder et al. 1999; Mazoyer et al. 2001; Raichle et al. 2001; McKiernan et al. 2003).
Figure 9.
Figure 9.
Composite map of complementary human brain networks for processing internal and external sources of information. Red areas indicate the general semantic network identified in the current meta-analysis. Yellow indicates areas activated in 24 healthy adults during oral reading of visually presented pseudowords (pronounceable but meaningless letter strings) compared with a resting baseline (Binder, Medler, et al. 2005). The latter task activates unimodal visual and auditory areas bilaterally, dorsal attention systems in the IPS and FEF bilaterally, and bilateral motor, premotor, dorsal anterior cingulate, and dorsolateral prefrontal systems involved in response production. Overlap between these 2 major networks is minimal.

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