Semantic retrieval during overt picture description: Left anterior temporal or the parietal lobe?

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.

Keywords: Anterior temporal lobe; Semantic.

Fig. 1

ICA restricted to a left parietal lobe (PL) and a left anterior temporal lo be (ATL) mask resulted in 15 regions of interest (ROI) within each mask. Sagittal T1 weighted slices from the MNI standard space are shown with superimposed ROIs in blue. Different shades of blue show the number of overlapping ROIs. The red ROI within the anterior STS has a unique functional connectivity to a distributed brain system engaged in the Speech task shown in Fig. 2. The red ROI within the superior parietal lobe has a unique functional connectivity with a distributed brain system engaged in the Speech task shown in Fig. 3. Numbers refer to MNI152 atlas coordinates along the x-axis. A, anterior; P, posterior. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

Fig. 2

The distributed whole-brain system in blue, is functionally connected with the left anterior superior temporal sulcus (antSTS) in red. Activity in this system showed a positive correlation with behavioral measures of speech production during the scan. Activity is overlaid on standard T1-weighted anatomical slices, FWE corrected P<0.01, t>5.6. Numbers above the slices refer to MNI152 atlas coordinates along the y-axis. The numbered regions are: 1, left inferior frontal gyrus including pars triangularis and opercularis; 2, bilateral primary and association auditory cortices; 3, left more than right insular activity extending into putamen; 4, bilateral sensory-motor cortices; 5, left hippocampus and parahippocampus extending into the anterior temporal fusiform cortex. 6, on the left the superior temporal cortex activity borders the most ventral part of the inferior parietal lobe; 7, small amount of activity is also seen in supplementary motor cortex. See Table 1 for peak coordinates. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

Fig. 3

The distributed whole-brain system in blue, is functionally connected with the left superior parietal lobe (supPL) in red. Activity in this system was significantly related to the Speech task compared to the higher-level baseline Count and Decision tasks. Activity is overlaid on standard T1-weighted anatomical slices, FWE corrected P<0.05, t>5.6. Numbers above the coronal slices refer to MNI152 atlas coordinates along the y-axis and those above sagittal slices refer to coordinates along the x-axis. One axial slice is shown at z=48 mm. The numbered regions are: 1 bilateral lateral occipital cortices 2 cuneal cortices, 3 superior parietal lobes 4 occipital poles extending anteriorly to posterior fusiform gyrus/lingual gyrus, 5 left angular gyrus and posterior supramarginal gyrus, 6 left superior frontal gyrus extending into dorsal anterior cingulate, 7 posterior inferior frontal gyrus, 8 superior frontal sulcus extending into middle frontal gyrus and inferior frontal sulcus 9 left lateralized posterior superior temporal gyrus. A, anterior; P, posterior. See Table 2 for peak coordinates. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

Fig. 4

Correlation matrix showing the pairwise spatial correlation of networks derived from dual-regression analyses. Top three rows show the spatial correlation between the system shown in Fig. 2 (blue) and all the networks linked to the ATL ROIs derived from 10, 15 and 25 decomposition of the ATL. Bottom three rows show the spatial correlation between the system shown in Fig. 3 (green) and all the networks linked to PL ROIs derived from 10, 15 and 25 decomposition of the PL. The numbers on the y-axis denote the dimensionality of the ICA used to derive the ROIs. The color bar refers to the correlation coefficient. Blue colors have a low correlation coefficient; red colors have a high correlation coefficient. “X” denotes the correlation of the systems in Figs. 2 and 3 with themselves (r=1). The top two “*” refer to the networks that connect to the left antSTS and have the highest spatial correlation to the system in Fig. 2. The bottom two “*” refer to the networks that connect to the left supPL and have the highest spatial correlation to the system in Figs. 3. These analyses suggest that the systems identified in Figs. 2 and 3 are spatially robust. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

Fig. 5

Persistent susceptibility artifact in the inferior-medial ATL despite measures to minimize this effect. Activity from Fig. 2 is superimposed on the mean functional image from the study transformed into the standard MNI space. One coronal and one axial slice are shown at the MNI coordinates specified. The activity in the parahippocampus and fusiform cortex in blue extends into the edge of the susceptibility artifact as shown with an asterix. The activation is FWE corrected at P>0.01, t>5.6.