Dataset Information

GABA concentrations in the anterior temporal lobe predict human semantic processing.

ABSTRACT: There is now considerable convergent evidence from multiple methodologies and clinical studies that the human anterior temporal lobe (ATL) is a semantic representational hub. However, the neurochemical nature of the ATL in the semantic processing remains unclear. The current study investigated the neurochemical mechanism underlying semantic processing in the ATL. We combined functional magnetic resonance imaging (fMRI) with resting-state magnetic resonance spectroscopy (MRS) to measure task-related blood-oxygen level-dependent (BOLD) signal changes during sematic processing and resting-state GABA concentrations in the ATL. Our combined fMRI and MRS investigation showed that the stronger ATL BOLD response induced by the semantic task, the lower GABA concentration in the same region. Moreover, individuals with higher GABA concentration in the ATL showed better semantic performance and stronger BOLD-related fluctuations in the semantic network. Our data demonstrated that the resting-state GABA concentration predicts neural changes in the human ATL and task performance during semantic processing. Our findings indicate that individuals with higher GABA may have a more efficient semantic processing leading to better task performance and imply that GABAergic neurochemical processes are potentially crucial to the neurobiological contribution of the ATL to semantic cognition.

SUBMITTER: Jung J

PROVIDER: S-EPMC5691052 | biostudies-literature | 2017 Nov

REPOSITORIES: biostudies-literature

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GABA concentrations in the anterior temporal lobe predict human semantic processing.

Jung JeYoung J Williams Stephen R SR Sanaei Nezhad Faezeh F Lambon Ralph Matthew A MA

Scientific reports 20171116 1

There is now considerable convergent evidence from multiple methodologies and clinical studies that the human anterior temporal lobe (ATL) is a semantic representational hub. However, the neurochemical nature of the ATL in the semantic processing remains unclear. The current study investigated the neurochemical mechanism underlying semantic processing in the ATL. We combined functional magnetic resonance imaging (fMRI) with resting-state magnetic resonance spectroscopy (MRS) to measure task-rela ...[more]

PMID: 29146995

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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.

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.

Dataset Information

GABA concentrations in the anterior temporal lobe predict human semantic processing.

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GABA concentrations in the anterior temporal lobe predict human semantic processing.

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