Abstract
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.
Highlights
Retrieval of semantic representations is a central process during overt speech production
Based on the behavioural sequelae in patients with asymmetrical atrophy, that can manifest as more prominent loss of semantic knowledge in a specific modality, some have suggested that verbal semantics is more dependent on the left anterior temporal lobes (ATL) while non-verbal semantics is more dependent on the right ATL (Gainotti, 2012; Mesulam et al, 2013)
For the PL mask, we started with a functionally derived mask of a large parietal lobe region that we have previously shown to be engaged in overt picture description with an independent dataset (region number 3 from Fig. 3 of Geranmayeh et al (2012))
Summary
Retrieval of semantic representations is a central process during overt speech production. 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. Borovsky et al (2007) performed behavioral analyses on 50 patients with aphasic strokes, but none had lesions confined to the parietal lobe alone It was patients with the semantic variant of fronto-temporal lobar degeneration (svFTD) that drew attention to the possibility that it is anterior temporal cortex that provides an amodal route through which semantic representations are accessed (AcostaCabronero et al, 2011; Hodges et al, 1992; McClelland and Rogers, 2003; Patterson et al, 2007; Snowden et al, 1989; Warrington, 1975). In addition to their prominent visuo-spatial deficits, these patients develop a progressive linguistic rather than semantic impairment, the reverse of what is observed in patients with svFTD (Crutch et al, 2012, 2013)
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