Asymmetry, Connectivity, and Segmentation of the Arcuate Fascicle in the Human Brain
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Brain Struct Funct DOI 10.1007/s00429-014-0751-7 ORIGINAL ARTICLE Asymmetry, connectivity, and segmentation of the arcuate fascicle in the human brain Juan C. Ferna´ndez-Miranda • Yibao Wang • Sudhir Pathak • Lucia Stefaneau • Timothy Verstynen • Fang-Cheng Yeh Received: 2 September 2013 / Accepted: 4 March 2014 Ó Springer-Verlag Berlin Heidelberg 2014 Abstract The structure and function of the arcuate fas- in the left arcuate, but not in the right one. The left arcuate cicle is still controversial. The goal of this study was to fascicle is formed by an inner or ventral pathway, which investigate the asymmetry, connectivity, and segmentation interconnects pars opercularis with superior and rostral patterns of the arcuate fascicle. We employed diffusion middle temporal gyri; and an outer or dorsal pathway, spectrum imaging reconstructed by generalized q-sampling which interconnects ventral precentral and caudal middle and we applied both a subject-specific approach (10 sub- frontal gyri with caudal middle and inferior temporal gyri. jects) and a template approach (q-space diffeomorphic The fiber microdissection results provided further support reconstruction of 30 subjects). We complemented our to our tractography studies. We propose the existence of imaging investigation with fiber microdissection of five primary and supplementary language pathways within the post-mortem human brains. Our results confirmed the dominant arcuate fascicle with potentially distinct func- highly leftward asymmetry of the arcuate fascicle. In the tional and lesional features. template, the left arcuate had a volume twice as large as the right one, and the left superior temporal gyrus provided Keywords Arcuate fascicle Á Diffusion spectrum five times more volume of fibers than its counterpart. We imaging Á Tractography Á Language Á Fiber dissection identified four cortical frontal areas of termination: pars opercularis, pars triangularis, ventral precentral gyrus, and Abbreviations caudal middle frontal gyrus. We found clear asymmetry of AAL Automated anatomical labeling the frontal terminations at pars opercularis and ventral AF Arcuate fascicle precentral gyrus. The analysis of patterns of connectivity BA Brodmann area revealed the existence of a strong structural segmentation CORID Committee for oversight research involving dead DSI Diffusion spectrum imaging DTI Diffusion tensor imaging EPI Echo planar imaging fMRI Functional MRI FoV Field of view J. C. Ferna´ndez-Miranda (&) Á Y. Wang Á L. Stefaneau Department of Neurological Surgery, University of Pittsburgh GQI Generalized q-sampling imaging Medical Center, 200 Lothrop St, Suite B-400, Pittsburgh, ITG Inferior temporal gyrus PA 15213, USA MdLF Middle longitudinal fascicle e-mail: [email protected] MTG Middle temporal gyrus S. Pathak ODF Orientation distribution function Learning Research and Development Center, University of QA Quantitative anisotropy Pittsburgh, Pittsburgh, PA, USA ROI Region of interest SLF Superior longitudinal fascicle T. Verstynen Á F.-C. Yeh Department of Bioengineering, Carnegie Mellon University, STG Superior temporal gyrus Pittsburgh, PA, USA TR Repetition time 123 Brain Struct Funct Introduction of the limitations of DTI studies, here we employ diffusion spectrum imaging (DSI) (Wedeen et al. 2005) recon- The arcuate fascicle (AF) is a white matter fiber tract that structed by generalized q-sampling imaging (GQI) (Yeh links lateral temporal cortex with frontal cortex via a dorsal et al. 2010) as a high angular resolution based approach projection that arches around the Sylvian fissure (Tu¨re that leverages high directional sampling of diffusion et al. 2000; Schmahmann et al. 2007; Fernandez-Miranda imaging space to get better resolution of underlying white et al. 2008b). Classical anatomical and clinical studies matter geometry for tractography. This approach has (Dick and Tremblay 2012) revealed its general trajectory shown to provide accurate replication of complex known along with the superior longitudinal fascicle (SLF) and neuroanatomical features where DTI failed (Fernandez- described the role of the left AF/SLF in language function. Miranda et al. 2012; Yeh et al. 2013), and has facilitated More recent anatomical studies using post-mortem fiber innovative studies on the structural connectivity of several microdissection techniques have proposed the differentia- fiber tracts such as the middle longitudinal fascicle (MdLF) tion of the AF as a fronto-temporal tract and the SLF as a (Wang et al. 2013), the cortico-spinal tract (Verstynen et al. fronto-parietal tract (Fernandez-Miranda et al. 2008b), and 2011), the corpus callosum (Jarbo et al. 2012), dorsal provided further detail regarding the cortical termination of stream visual pathways (Greenberg et al. 2012), and the their fibers (Martino et al. 2013b). cortico-striatal pathways (Verstynen et al. 2011). Here we Modern autoradiography studies in monkeys, have have applied both a subject-specific approach and a tem- suggested that the AF does not link the posterior-superior plate approach, and in an attempt to cross-validate the temporal gyrus (Wernicke’s area) with the posterior infe- ‘‘in vivo’’ fiber tracking results, we have complemented our rior frontal gyrus (Broca’s area), thus supporting the view imaging investigation with fiber microdissection tech- that the left AF is not a language-related tract (Schmah- niques of the left and right AF in post-mortem human mann and Pandya 2006). Although these ‘‘in vivo’’ tract- brains. tracing studies are considered the ‘‘gold standard’’ in connectional Neuroanatomy (Schmahmann et al. 2007), the translation of their results from non-human primates to Materials and methods humans is problematic, especially for language-related tracts (Catani et al. 2005). Participants In the last decade, diffusion tensor imaging (DTI) studies have revealed the significant leftward asymmetry Ten neurologically healthy adults (7 male; all right-handed; and cortical terminations of the AF providing new insights age range 21–36) from the local University of Pittsburgh into the connectivity of the AF and its assumed major community took part in this experiment, conducted as part functional role in language processing (Catani et al. 2005; of a larger data collection effort. All participants were Hagmann et al. 2006; Powell et al. 2006; Vernooij et al. prescreened prior to scanning to rule out any contraindi- 2007). However, DTI-based tractography has several cations to MRI. The internal review board at the University technical limitations, such as inability to map fiber endings of Pittsburgh approved all the procedures used here and of white matter before contacting the cortical mantle, written consent was obtained from all participants prior to failure to solve fiber crossings and to follow bundles within testing. fiber tracts, and excessive false fiber continuity generating In addition to subject-specific analysis, we also con- pseudotracts (Catani et al. 2005; Glasser and Rilling 2008; ducted fiber tracking on a high angular resolution brain Dick and Tremblay 2012; Wang et al. 2013). As a conse- template reflecting an average of 30 adult brains. For this, quence, the connectivity pattern of the AF is still contro- twenty male and ten female subjects were recruited from versial and warrants further investigation. In particular, the local Pittsburgh community and the Army Research Dick and Tremblay (2012) debated: the existence of direct Laboratory in Aberdeen, Maryland. All subjects were posterior temporal-inferior frontal connectivity (Broca– neurologically healthy, with no history of either head Wernicke); the specific location of the rostral (frontal) trauma or neurological or psychiatric illness. Subject ages terminations of the AF; and the extension of the caudal ranged from 21 to 45 years of age at the time of scanning (temporal) component of the AF. Individual differences in and four were left handed (2 male, 2 female). the anatomy of the AF and SLF have also contributed to the uncertain delineation of their fiber pathway connectivity. Image acquisition and reconstruction The goal of this study was to investigate in healthy subjects the asymmetry, connectivity and segmentation DSI data for the subject-specific approach were acquired patterns of the left and right AF. In order to overcome some on 3T Tim Trio System (Siemens) using a 32-channel coil. 123 Brain Struct Funct This involved a 43-min, 257-direction scan using a twice- diffeomorphic reconstruction across all 30 subjects, and the refocused spin-echo EPI sequence and multiple q values resulting template can be used to obtain the representative (TR = 9,916 ms, TE = 157 ms, voxel size = 2.4 9 2.4 9 tractography of the subject population. The white matter 2 2.4 mm, FoV = 231 9 231 mm, bmax = 7,000 s/mm ). For surface is rendered independently from an externally sup- anatomical comparisons, we also included high resolution plied 1 9 1 9 1 mm resolution ICBM-152 white matter anatomical imaging, employing a 9-min T1-weighted axial image (Fonov et al. 2011). MPRAGE sequence (TR = 2,110 ms, TE = 2.63 ms, flip angle = 8°, 176 slices, FoV = 256 9 256 mm2, voxel Fiber tracking and analysis size = 0.5 9 0.5 9 1.0 mm3). DSI data were reconstructed using a GQI approach. The orientation distribution functions Diffusion fiber tracking was conducted using a multiple (ODFs) were reconstructed to 362 discrete sampling direc- fiber version of the streamline tracking algorithm (Basser tions and a diffusion distance ratio of 1.2, as used in the et al. 2000;