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Topography of the Human Acoustic Radiation As Revealed by Ex Vivo fibers Micro-Dissection and in Vivo Diffusion-Based Tractography

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Topography of the Human Acoustic Radiation As Revealed by Ex Vivo fibers Micro-Dissection and in Vivo Diffusion-Based Tractography Brain Struct Funct DOI 10.1007/s00429-017-1471-6 ORIGINAL ARTICLE Topography of the human acoustic radiation as revealed by ex vivo fibers micro-dissection and in vivo diffusion-based tractography 1 1 2 3 Chiara Maffei • Jorge Jovicich • Alessandro De Benedictis • Francesco Corsini • 4 3 3 Mattia Barbareschi • Franco Chioffi • Silvio Sarubbo Received: 11 April 2017 / Accepted: 4 July 2017 Ó Springer-Verlag GmbH Germany 2017 Abstract The acoustic radiation is a compact bundle of trajectory of the AR, a transversal course from the midline fibers conveying auditory information from the medial to the lateral convexity of the posterior temporal lobe. geniculate nucleus of the thalamus to the auditory cortex. Blunt dissections demonstrated three portions of this bun- Topographical knowledge of this bundle in primates is dle that we defined as the genu, stem, and fan, revealing the scarce and in vivo diffusion-based tractography recon- intimate relationships that each of these components has structions in humans remains challenging, especially with with neighboring association and projection pathways. the most widely used MRI acquisition protocols. Therefore, Probabilistic tractography and ultra-high b values provided the AR represents a notable anatomical omission in the results comparable to blunt micro-dissections and high- neurobiological investigation of acoustic and linguistic lighted the main limitations in tracking the AR. This is, to functional mechanisms in humans. In this study, we com- our knowledge, the first ex vivo/in vivo integrated study bine blunt micro-dissections and advanced diffusion trac- providing novel and reliable information about the precise tography methods to provide novel insights into the anatomy of the AR, which will be important for future topographical anatomy of this bundle in humans. Evi- investigations in the neuroscientific, clinical, and surgical dences from ex vivo blunt micro-dissection in three human field. (two right) hemispheres are compared to the 3D profile of this bundle as reconstructed by tractography techniques in Keywords Acoustic radiation Á Diffusion tractography Á four healthy adult data sets provided by the Human Con- Post-mortem dissection Á Auditory tract Á Auditory nectome Project. Both techniques show the unique pathways Electronic supplementary material The online version of this article (doi:10.1007/s00429-017-1471-6) contains supplementary Introduction material, which is available to authorized users. The acoustic radiation (AR) constitutes a major sensory & Silvio Sarubbo [email protected] projection pathway, transferring primary auditory infor- mation from the medial geniculate nucleus (MGN) of the 1 CIMeC Center for Mind/Brain Sciences, Trento University, thalamus on the auditory cortex to the transverse temporal Trento, Italy gyrus of Heschl (HG). 2 Neurosurgery Unit, Department of Neuroscience and The connectivity pattern of these fibers has been Neurorehabilitation, Bambino Gesu` Children’s Hospital, described in some detail in cytoarchitectonic and IRCCS, Rome, Italy 3 myeloarchitectonic studies in non-human primates (Mesu- Division of Neurosurgery, Structural and Functional lam and Pandya 1973; Hackett et al. 1998) and to some Connectivity Lab (SFC-LSB) Project, Department of Neurosciences, ‘‘S. Chiara’’ Hospital, Trento APSS, 9, extent in humans (Tardif and Clarke 2001). These studies Largo Medaglie d’Oro, 38122 Trento, Italy mainly provide information on connectivity aspects 4 Department of Histopathology, ‘‘S. Chiara’’ Hospital, Trento between the MGN and the auditory projection cortical APSS, Trento, Italy territory and little emphasis was given to the anatomy of 123 Brain Struct Funct the tract itself. To a more macro-anatomical level, Bu¨rgel bundles is missing or only hypothesized on the base of et al. (2006) described the trajectory of this bundle from the studies on monkeys. MGN to the cortex. However, still, very little is known In this scenario, validation of tractography results is about its topography and, in particular, its relationship with crucial. The spreading of diffusion-based tractography adjacent white matter (WM) bundles. Most of the available techniques has, therefore, renewed the interest in blunt information about the anatomy of the AR traces back to the micro-dissections of human WM (Martino et al. 2010; pioneering work of the anatomists of the 19th and early Wang et al. 2012; Ferna´ndez-Miranda et al. 2015; Sarubbo 20th century, who used gross dissection, myelin staining, et al. 2015; De Benedictis et al. 2016; Wang et al. 2016; and lesion degeneration methods to investigate AR Sarubbo et al. 2016). The unique information provided by topography. These early reports described the AR as a blunt micro-dissections on the trajectory and topographical compact bundle of fibers leaving the MGN and pursuing an organization of the WM bundles constitute a baseline by antero-lateral direction passing through the posterior por- which the methodological process can be improved to tion of the internal capsule, proceeding along the corona overcome the limits of tractography reconstructions. radiata, curving around the inferior sulcus of the insula Successful and reliable reconstructions of the AR will be before reaching the transverse temporal HG (Dejerine crucial for neuroscientific, clinical, and surgical applica- 1895; Flechsig 1920; Pfeifer 1920). While being of unde- tions. Robust AR reconstruction in vivo could help case– niable value, these old maps lack fine anatomo-topo- control studies in pathological groups, but also would allow graphical details and have limited value as references in for the identification of the left–right asymmetries and neuroimaging studies. functional mechanisms sub-served by this bundle, that are Over the past decade, diffusion tractography techniques currently unknown. In particular, evaluating the mecha- have emerged as the main tool for the investigation of the nisms of the anatomo-functional relations of this tract WM architecture in vivo (Catani et al. 2002; Tournier et al. would help to shed a light on the neural basis of language 2011). However, it is still challenging to perform diffusion- comprehension, contributing to enhance the cornerstone based reconstructions of the AR (Maffei et al. 2015) using the model of language processing (Hickok and Poeppel 2007; most widespread MRI acquisition protocols and standard Poeppel et al. 2012). Moreover, reliable tractographic processing pipelines. As a result, the AR is missing from reconstruction of the AR will support neuropsychological, most tractography studies investigating auditory processing clinical, and surgical applications. and the integration of language and non-language auditory In this study, we combine blunt micro-dissection and inputs, as well as from diffusion-based atlases (Thiebaut de advanced diffusion imaging tractography methods with the Schotten et al. 2011). The main challenges in reconstructing following goals: (1) to provide, for the first time to our the trajectory of the AR are related to the intrinsic anatomical knowledge, a detailed and multimodal anatomical features of these projection fibers: short tract length; small description of the trajectory and terminations of the AR in dimensions; atypical medio-lateral course; dense fiber humans and (2) to characterize the topography of this crossing with projection; and association fibers. The inability bundle in respect to the other neighboring tracts. Results to completely solve multiple fibers orientations inside the obtained with ex vivo dissections and in vivo tractography voxel constitutes one of the main limitations of tractography are compared and integrated, and limitations discussed. (Jeurissen et al. 2013). Compared to the classic tensor model (Basser et al. 1994), new algorithms, such as constrained spherical deconvolution (CSD), have been developed to Materials and methods improve this reconstruction issue (Dell’Acqua et al. 2010; Tournier et al. 2008). However, these methods can still Fiber dissection provide inaccurate or ambiguous descriptions of local fiber orientations and thus unreliable 3D reconstructions, in Three human cerebral hemispheres (two right) were pre- regions with very complex fiber architectures and high pared according to the modified Klinger’s preparation density of crossing (Jones and Cercignani 2010). Using previously described (Sarubbo et al. 2015, 2016). Micro- multi-fiber models and probabilistic tractography algo- dissection (59) was performed by an expert anatomist and rithms, few studies have been able to recover the 3D profile neurosurgeon (the senior author, S.S.). The AR was of the AR (Behrens et al. 2007; Crippa et al. 2010; Berman approached posteriorly starting a layer-by-layer dissection et al. 2013; Javad et al. 2014). Nevertheless, AR recon- from the posterior third of the superior temporal sulcus struction is variable across these studies, and no detailed (STS) and its elongation in the inferior parietal lobe (IPL) topographical descriptions are provided. Clear topographical (Sarubbo et al. 2016). U-fibers connecting the supra-mar- information on the course of these fibers from the MGN to ginal gyrus (SMG) and the angular gyrus (AG) with the the HG and on their relationship with neighboring WM cortices of the posterior two-thirds of the STS were 123 Brain Struct Funct removed (Fig. 1a). The stem of the vertical indirect pos- analyzed using MrTrix (Tournier et al. 2012). Data were terior portion of the superior longitudinal fasciculus (SLF) previously preprocessed
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