Dataset Information

Oscillatory Dynamics Supporting Semantic Cognition: MEG Evidence for the Contribution of the Anterior Temporal Lobe Hub and Modality-Specific Spokes.

ABSTRACT: The "hub and spoke model" of semantic representation suggests that the multimodal features of objects are drawn together by an anterior temporal lobe (ATL) "hub", while modality-specific "spokes" capture perceptual/action features. However, relatively little is known about how these components are recruited through time to support object identification. We used magnetoencephalography to measure neural oscillations within left ATL, lateral fusiform cortex (FC) and central sulcus (CS) during word-picture matching at different levels of specificity (employing superordinate vs. specific labels) for different categories (manmade vs. animal). This allowed us to determine (i) when each site was sensitive to semantic category and (ii) whether this was modulated by task demands. In ATL, there were two phases of response: from around 100 ms post-stimulus there were phasic bursts of low gamma activity resulting in reductions in oscillatory power, relative to a baseline period, that were modulated by both category and specificity; this was followed by more sustained power decreases across frequency bands from 250 ms onwards. In the spokes, initial power increases were not stronger for specific identification, while later power decreases were stronger for specific-level identification in FC for animals and in CS for manmade objects (from around 150 ms and 200 ms, respectively). These data are inconsistent with a temporal sequence in which early sensory-motor activity is followed by later retrieval in ATL. Instead, knowledge emerges from the rapid recruitment of both hub and spokes, with early specificity and category effects in the ATL hub. The balance between these components depends on semantic category and task, with visual cortex playing a greater role in the fine-grained identification of animals and motor cortex contributing to the identification of tools.

SUBMITTER: Mollo G

PROVIDER: S-EPMC5226830 | biostudies-literature | 2017

REPOSITORIES: biostudies-literature

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Oscillatory Dynamics Supporting Semantic Cognition: MEG Evidence for the Contribution of the Anterior Temporal Lobe Hub and Modality-Specific Spokes.

Mollo Giovanna G Cornelissen Piers L PL Millman Rebecca E RE Ellis Andrew W AW Jefferies Elizabeth E

PloS one 20170111 1

The "hub and spoke model" of semantic representation suggests that the multimodal features of objects are drawn together by an anterior temporal lobe (ATL) "hub", while modality-specific "spokes" capture perceptual/action features. However, relatively little is known about how these components are recruited through time to support object identification. We used magnetoencephalography to measure neural oscillations within left ATL, lateral fusiform cortex (FC) and central sulcus (CS) during word- ...[more]

PMID: 28076421

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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).

Project description:Making sense of the world around us depends upon selectively retrieving information relevant to our current goal or context. However, it is unclear whether selective semantic retrieval relies exclusively on general control mechanisms recruited in demanding non-semantic tasks, or instead on systems specialised for the control of meaning. One hypothesis is that the left posterior middle temporal gyrus (pMTG) is important in the controlled retrieval of semantic (not non-semantic) information; however this view remains controversial since a parallel literature links this site to event and relational semantics. In a functional neuroimaging study, we demonstrated that an area of pMTG implicated in semantic control by a recent meta-analysis was activated in a conjunction of (i) semantic association over size judgements and (ii) action over colour feature matching. Under these circumstances the same region showed functional coupling with the inferior frontal gyrus - another crucial site for semantic control. Structural and functional connectivity analyses demonstrated that this site is at the nexus of networks recruited in automatic semantic processing (the default mode network) and executively demanding tasks (the multiple-demand network). Moreover, in both task and task-free contexts, pMTG exhibited functional properties that were more similar to ventral parts of inferior frontal cortex, implicated in controlled semantic retrieval, than more dorsal inferior frontal sulcus, implicated in domain-general control. Finally, the pMTG region was functionally correlated at rest with other regions implicated in control-demanding semantic tasks, including inferior frontal gyrus and intraparietal sulcus. We suggest that pMTG may play a crucial role within a large-scale network that allows the integration of automatic retrieval in the default mode network with executively-demanding goal-oriented cognition, and that this could support our ability to understand actions and non-dominant semantic associations, allowing semantic retrieval to be 'shaped' to suit a task or context.

Project description:Built upon a wealth of neuroimaging, neurostimulation, and neuropsychology data, a recent proposal set forth a framework termed controlled semantic cognition (CSC) to account for how the brain underpins the ability to flexibly use semantic knowledge (Lambon Ralph et al., 2017; Nature Reviews Neuroscience). In CSC, the 'semantic control' system, underpinned predominantly by the prefrontal cortex, dynamically monitors and modulates the 'semantic representation' system that consists of a 'hub' (anterior temporal lobe, ATL) and multiple 'spokes' (modality-specific areas). CSC predicts that unfamiliar and exacting semantic tasks should intensify communication between the 'control' and 'representation' systems, relative to familiar and less taxing tasks. In the present study, we used functional magnetic resonance imaging (fMRI) to test this hypothesis. Participants paired unrelated concepts by canonical colours (a less accustomed task - e.g., pairing ketchup with fire-extinguishers due to both being red) or paired well-related concepts by semantic relationship (a typical task - e.g., ketchup is related to mustard). We found the 'control' system was more engaged by atypical than typical pairing. While both tasks activated the ATL 'hub', colour pairing additionally involved occipitotemporal 'spoke' regions abutting areas of hue perception. Furthermore, we uncovered a gradient along the ventral temporal cortex, transitioning from the caudal 'spoke' zones preferring canonical colour processing to the rostral 'hub' zones preferring semantic relationship. Functional connectivity also differed between the tasks: Compared with semantic pairing, colour pairing relied more upon the inferior frontal gyrus, a key node of the control system, driving enhanced connectivity with occipitotemporal 'spoke'. Together, our findings characterise the interaction within the neural architecture of semantic cognition - the control system dynamically heightens its connectivity with relevant components of the representation system, in response to different semantic contents and difficulty levels.

Project description:Retrieval of semantic representations is a central process during overt speech production. There is an increasing consensus that an amodal semantic 'hub' must exist that draws together modality-specific representations of concepts. Based on the distribution of atrophy and the behavioral deficit of patients with the semantic variant of fronto-temporal lobar degeneration, it has been proposed that this hub is localized within both anterior temporal lobes (ATL), and is functionally connected with verbal 'output' systems via the left ATL. An alternative view, dating from Geschwind's proposal in 1965, is that the angular gyrus (AG) is central to object-based semantic representations. In this fMRI study we examined the connectivity of the left ATL and parietal lobe (PL) with whole brain networks known to be activated during overt picture description. We decomposed each of these two brain volumes into 15 regions of interest (ROIs), using independent component analysis. A dual regression analysis was used to establish the connectivity of each ROI with whole brain-networks. An ROI within the left anterior superior temporal sulcus (antSTS) was functionally connected to other parts of the left ATL, including anterior ventromedial left temporal cortex (partially attenuated by signal loss due to susceptibility artifact), a large left dorsolateral prefrontal region (including 'classic' Broca's area), extensive bilateral sensory-motor cortices, and the length of both superior temporal gyri. The time-course of this functionally connected network was associated with picture description but not with non-semantic baseline tasks. This system has the distribution expected for the production of overt speech with appropriate semantic content, and the auditory monitoring of the overt speech output. In contrast, the only left PL ROI that showed connectivity with brain systems most strongly activated by the picture-description task, was in the superior parietal lobe (supPL). This region showed connectivity with predominantly posterior cortical regions required for the visual processing of the pictorial stimuli, with additional connectivity to the dorsal left AG and a small component of the left inferior frontal gyrus. None of the other PL ROIs that included part of the left AG were activated by Speech alone. The best interpretation of these results is that the left antSTS connects the proposed semantic hub (specifically localized to ventral anterior temporal cortex based on clinical neuropsychological studies) to posterior frontal regions and sensory-motor cortices responsible for the overt production of speech.

Dataset Information

Oscillatory Dynamics Supporting Semantic Cognition: MEG Evidence for the Contribution of the Anterior Temporal Lobe Hub and Modality-Specific Spokes.

Publications

Oscillatory Dynamics Supporting Semantic Cognition: MEG Evidence for the Contribution of the Anterior Temporal Lobe Hub and Modality-Specific Spokes.

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