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Sensory and semantic category subdivisions within the anterior temporal lobes.

ABSTRACT: In the semantic memory literature the anterior temporal lobe (ATL) is frequently discussed as one homogeneous region when in fact, anatomical studies indicate that it is likely that there are discrete subregions within this area. Indeed, the influential Hub Account of semantic memory has proposed that this region is a sensory-amodal, general-purpose semantic processing region. However review of the literature suggested two potential demarcations: sensory subdivisions and a social/nonsocial subdivision. To test this, participants were trained to associate social or non-social words with novel auditory, visual, or audiovisual stimuli. Later, study participants underwent an fMRI scan where they were presented with the sensory stimuli and the task was to recall the semantic associate. The results showed that there were sensory specific subdivisions within the ATL - that the perceptual encoding of auditory stimuli preferentially activated the superior ATL, visual stimuli the inferior ATL, and multisensory stimuli the polar ATL. Moreover, our data showed that there is stimulus-specific sensitivity within the ATL - the superior and polar ATLs were more sensitive to the retrieval of social knowledge as compared to non-social knowledge. No ATL regions were more sensitive to the retrieval of non-social knowledge. These findings indicate that the retrieval of newly learned semantic associations activates the ATL. In addition, superior and polar aspects of the ATL are sensitive to social stimuli but relatively insensitive to non-social stimuli, a finding that is predicted by anatomical connectivity and single-unit studies in non-human primates. And lastly, the ATL contains sensory processing subdivisions that fall along superior (auditory), inferior (visual), polar (audiovisual) subdivisions.

SUBMITTER: Skipper LM

PROVIDER: S-EPMC3192293 | biostudies-literature | 2011 Oct

REPOSITORIES: biostudies-literature

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Sensory and semantic category subdivisions within the anterior temporal lobes.

Skipper Laura M LM Ross Lars A LA Olson Ingrid R IR

Neuropsychologia 20110822 12

In the semantic memory literature the anterior temporal lobe (ATL) is frequently discussed as one homogeneous region when in fact, anatomical studies indicate that it is likely that there are discrete subregions within this area. Indeed, the influential Hub Account of semantic memory has proposed that this region is a sensory-amodal, general-purpose semantic processing region. However review of the literature suggested two potential demarcations: sensory subdivisions and a social/nonsocial subdi ...[more]

PMID: 21889520

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Project description:Assessment of regional language lateralization is crucial in many scenarios, but not all populations are suited for its evaluation via task-functional magnetic resonance imaging (fMRI). In this study, the utility of structural connectome features for the classification of language lateralization in the anterior temporal lobes (ATLs) was investigated. Laterality indices for semantic processing in the ATL were computed from task-fMRI in 1038 subjects from the Human Connectome Project who were labeled as stronger rightward lateralized (RL) or stronger leftward to bilaterally lateralized (LL) in a data-driven approach. Data of unrelated subjects (n = 432) were used for further analyses. Structural connectomes were generated from diffusion-MRI tractography, and graph theoretical metrics (node degree, betweenness centrality) were computed. A neural network (NN) and a random forest (RF) classifier were trained on these metrics to classify subjects as RL or LL. After classification, comparisons of network measures were conducted via permutation testing. Degree-based classifiers produced significant above-chance predictions both during cross-validation (NN: AUC-ROC[CI] = 0.68[0.64-0.73], accuracy[CI] = 68.34%[63-73.2%]; RF: AUC-ROC[CI] = 0.7[0.66-0.73], accuracy[CI] = 64.81%[60.9-68.5]) and testing (NN: AUC-ROC[CI] = 0.69[0.53-0.84], accuracy[CI] = 68.09[53.2-80.9]; RF: AUC-ROC[CI] = 0.68[0.53-0.84], accuracy[CI] = 68.09[55.3-80.9]). Comparison of network metrics revealed small effects of increased node degree within the right posterior middle temporal gyrus (pMTG) in subjects with RL, while degree was decreased in the right posterior cingulate cortex (PCC). Above-chance predictions of functional language lateralization in the ATL are possible based on diffusion-MRI connectomes alone. Increased degree within the right pMTG as a right-sided homologue of a known semantic hub, and decreased hubness of the right PCC may form a structural basis for rightward-lateralized semantic processing.

Project description:Even though the anterior temporal lobe (ATL) comprises several anatomical and functional subdivisions, it is often reduced to a homogeneous theoretical entity, such as a domain-general convergence zone, or "hub", for semantic information. Methodological limitations are largely to blame for the imprecise mapping of function to structure in the ATL. There are two major obstacles to using fMRI to identify the precise functional organization of the ATL: the difficult choice of stimuli and tasks to activate, and dissociate, specific regions within the ATL and poor signal quality due to magnetic field distortions near the sinuses. To circumvent these difficulties, we developed a data-driven parcellation routine using resting-state fMRI data (24 females, 64 males) acquired using a sequence that was optimized to enhance signal in the ATL. Focusing on patterns of functional connectivity between each ATL voxel and the rest of the brain, we found that the ATL comprises at least 34 distinct functional parcels that are arranged into bands along the lateral and ventral cortical surfaces, extending from the posterior temporal lobes into the temporal poles. In addition, the anterior region of the fusiform gyrus, most often cited as the location of the semantic hub, was found to be part of a domain-specific network associated with face and social processing, rather than a domain-general semantic hub. These findings offer a fine-grained functional map of the ATL and offer an initial step towards using more precise language to describe the locations of functional responses in this heterogeneous region of human cortex.SIGNIFICANCE STATEMENTThe functional role of the anterior aspects of the temporal lobes (ATL) is a contentious issue. While it is likely that different regions within the ATL subserve unique cognitive functions, most studies revert to vaguely referring to particular functional regions as "the ATL" and, thus, the mapping of function to anatomy remains unclear. We used resting-state fMRI connectivity patterns between the ATL and the rest of the brain to reveal that the ATL comprises at least 34 distinct functional parcels that are organized into a three-level functional hierarchy. These results provide a detailed functional map of the anterior temporal lobes that can guide future research on how distinct regions within the ATL support diverse cognitive functions.

Project description:How does the brain represent and process different types of knowledge? The Dual Hub account postulates that anterior temporal lobes (ATL) support taxonomic relationships based on shared physical features (mole - cat), while temporoparietal regions, including posterior middle temporal gyrus (pMTG), support thematic associations (mole - earth). Conversely, the Controlled Semantic Cognition account proposes that ATL supports both aspects of knowledge, while left pMTG contributes to controlled retrieval. This study used magnetoencephalography to test these contrasting predictions of functional dissociations within the temporal lobe. ATL and pMTG responded more strongly to taxonomic and thematic trials respectively, matched for behavioural performance, in line with predictions of the Dual Hub account. In addition, ATL showed a greater response to strong than weak thematic associations, while pMTG showed the opposite pattern, supporting a key prediction of the Controlled Semantic Cognition account. ATL showed a stronger response for word pairs that were more semantically coherent, either because they shared physical features (in taxonomic trials) or a strong thematic association. These effects largely coincided in time and frequency (although an early oscillatory response in ATL was specific to taxonomic trials). In contrast, pMTG showed non-overlapping effects of semantic control demands and thematic judgements: this site showed a larger oscillatory response to weak associations, when ongoing retrieval needed to be shaped to suit the task demands, and also a larger response to thematic judgements contrasted with taxonomic trials (which was reduced but not eliminated when the thematic trials were easier). Consequently, time-sensitive neuroimaging supports a complex pattern of functional dissociations within the left temporal lobe, which reflects both coherence versus control and distinctive oscillatory responses for taxonomic overlap (in ATL) and thematic relations (in pMTG).

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Sensory and semantic category subdivisions within the anterior temporal lobes.

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Sensory and semantic category subdivisions within the anterior temporal lobes.

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