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. 2008 Nov 5;28(45):11435-44.
doi: 10.1523/JNEUROSCI.2388-08.2008.

Dissociating the human language pathways with high angular resolution diffusion fiber tractography

Stephen Frey  1 , Jennifer S W Campbell, G Bruce Pike, Michael Petrides
Affiliations

Dissociating the human language pathways with high angular resolution diffusion fiber tractography

Stephen Frey et al. J Neurosci. .

Abstract

The anatomical connectivity of ventrolateral frontal areas 44 and 45, which in the human brain constitute Broca's region, has been revisited on the basis of experimental anatomical tracer evidence in the nonhuman primate that the homologues of areas 44 and 45 have distinct bidirectional corticocortical connections. Here we show, using high angular resolution diffusion imaging in the living human brain, a dissociation between the specific projections from the pars opercularis (area 44) and the pars triangularis (area 45) in the ventrolateral frontal lobe. As in the macaque monkey, area 44 has distinct connections with the rostral inferior parietal lobule via the third branch of the superior longitudinal fasciculus. In contrast, area 45 connects with the superior temporal gyrus, anterior to Heschl's gyrus, via the extreme capsule fiber system. These results highlight the differences in connectivity between areas 44 and 45 which had previously been thought to be uniformly connected with the posterior temporal region via the arcuate fasciculus. We also provide evidence in the human brain that the arcuate fasciculus, as in the macaque monkey brain, connects the posterior superior temporal region with dorsolateral frontal areas 8 and rostral 6 that lie above areas 44 and 45. Thus, monkey and human evidence suggests that the connections of areas 44 and 45 are much more differentiated than had previously been thought and provide the basis for studies searching for their differential contribution in function.

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Figures

Figure 1.
Figure 1.
Schematic representations of the regions of interest (areas 44 and 45) in the human and monkey brains. a, Experimental anatomical tract tracing in the monkey have demonstrated that the majority of the bidirectional connections of area 44 are made with regions in the anterior part of the inferior parietal lobule (the homolog of the supramarginal gyrus) via the third branch of the SLF III, whereas area 45 is connected to the superior temporal gyrus and sulcus via the ECFS. The AF, ECFS, FOF, SLFII and SLFIII, and MDLF, as well as the ILF are also presented in this diagram. b, Illustration of the ROIs that were drawn on each subject's anatomical scan (color coded).
Figure 2.
Figure 2.
Tractography input. a, The diffusion orientation distribution function is calculated using QBI reconstruction. The maxima are extracted, and streamlines are propagated in all directions within the solid angle dictated by the finite angular resolution of the acquisition. b, The maximum and associated cone closest to the incoming streamline direction are chosen at each voxel. The voxel shown here indicates a two fiber crossing.
Figure 3.
Figure 3.
Tractography in the left hemisphere of a single subject for areas 44 and 45. The tractography revealed that the connections (shown in green) between the large Broca area ROI (purple) and the ROI in the rostral inferior parietal lobule within the supramarginal gyrus (yellow) began mainly in area 44. In contrast, the connections (shown in red) between the large Broca area ROI and the ROI in the superior temporal gyrus and sulcus originated mainly in area 45. The colored pathways are surfaces encompassing all nonzero voxels in the connectivity map for each connection. Although the tract data displayed here are projected on a single plane, investigation using our 3D tract display demonstrated that projections from area 44 likely travel along the SLF III to the inferior parietal cortex. In contrast, the projections of area 45 traveled through the ECFS into the superior temporal gyrus and sulcus, anterior to Heschl's gyrus. This is demonstrated in the coronal sections within a single subject (a–h).
Figure 4.
Figure 4.
Group data showing connections from areas 44 and 45: MIPs of the sum of the coregistered individual connectivity maps for these connections. The MIP of the group sum connectivity maps for the connection from the ROI in Broca's area to the ROI in the rostral inferior parietal lobule within the supramarginal gyrus (a, b), and the connection from the ROI in Broca's area and the ROI in the superior temporal gyrus and sulcus (c, d), depicted in the left hemisphere for the 12 subjects. The former projects from area 44 and the latter from area 45. The projections are superimposed on the average anatomical brain of the 12 subjects presented here in the axial and sagittal planes. The color intensity scales refer to the amount of overlap for each pathway for all 12 subjects. Brighter colors signify greater overlap.
Figure 5.
Figure 5.
Dissociation of the projections from Broca's area. Group data demonstrating the dissociation of the projections from areas 44 (green) and 45 (red) in all subjects in the left hemisphere. Only the part of the pathway that lay within the ROI centered on Broca's area is shown. The data have been superimposed onto the average anatomical brain of the 12 subjects. An anterior to posterior dissociation of Broca's area is evident.
Figure 6.
Figure 6.
Tractography in a single subject. The tractography results revealed that the ROI at the most posterior extent of the superior temporal gyrus in the left hemisphere (equivalent to the monkey's Tpt region) (red), and the ROI that was located in areas 8 and rostral area 6 (blue) were connected via a pathway that courses around the Sylvian fissure and comes into close proximity with the SLF III (orange tract). The resolution of the voxel size used limits the separation of these individual pathways as evidenced by a connection between this same posterior ROI and the ROI in Broca's area. This is demonstrated in the coronal sections within a single subject (a–f). Areas of overlap between the two pathways are shown in white in the coronal sections.
Figure 7.
Figure 7.
Tractography in a single subject demonstrating connections from the posterior left temporal cortex to the ventral parietal region. The tractography results revealed that there are connections in the human brain that link the caudal superior temporal region to the inferior parietal region. These connections (MDLF; ILF) likely originate to convey auditory and visual information.
Figure 8.
Figure 8.
Three-dimensional reconstruction of the MRI of a human brain to illustrate the course of the SLF III (green tract) and the ECFS (red tract) from the posterior part of the ventrolateral frontal region on the lateral hemispheric surface.
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References

    1. Amunts K, Schleicher A, Bürgel U, Mohlberg H, Uylings HB, Zilles K. Broca's region revisited: cytoarchitecture and intersubject variability. J Comp Neurol. 1999;412:319–341. - PubMed
    1. Amunts K, Weiss PH, Mohlberg H, Pieperhoff P, Eickhoff S, Gurd JM, Marshall JC, Shah NJ, Fink GR, Zilles K. Analysis of neural mechanisms underlying verbal fluency in cytoarchitectonically defined stereotaxic space—the roles of Brodmann areas 44 and 45. Neuroimage. 2004;22:42–56. - PubMed
    1. Anwander A, Tittgemeyer M, von Cramon DY, Friederici AD, Knösche TR. Connectivity-based parcellation of Broca's area. Cereb Cortex. 2007;17:816–825. - PubMed
    1. Belin P, Zatorre RJ, Lafaille P, Ahad P, Pike B. Voice-selective areas in human auditory cortex. Nature. 2000;403:309–312. - PubMed
    1. Binder JR, Frost JA, Hammeke TA, Bellgowan PSF, Springer JA, Kaufman JN, Possing ET. Human temporal lobe activation by speech and nonspeech sounds. Cereb Cortex. 2000;10:512–528. - PubMed

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