Detection of the Arcuate Fasciculus in Congenital Amusia Depends on the Tractography Algorithm

ORIGINAL RESEARCH ARTICLE published: 21 January 2015 doi: 10.3389/fpsyg.2015.00009 Detection of the arcuate fasciculus in congenital amusia depends on the tractography algorithm Joyce L. Chen 1*, Sukhbinder Kumar 2,3, Victoria J. Williamson 4, Jan Scholz 5, Timothy D. Griffiths 2,3† and Lauren Stewart 6† 1 Department of Physical Therapy and Graduate Department of Rehabilitation Sciences, Heart and Stroke Foundation Canadian Partnership for Stroke Recovery, Sunnybrook Research Institute, University of Toronto, Toronto, ON, Canada 2 Wellcome Trust Centre for Neuroimaging, Institute of Neurology, University College London, London, UK 3 Institute of Neuroscience, University of Newcastle Upon Tyne, Newcastle Upon Tyne, UK 4 Department of Music, University of Sheffield, Sheffield, UK 5 Mouse Imaging Centre, The Hospital for Sick Children, Toronto, ON, Canada 6 Department of Psychology, Goldsmiths, University of London, London, UK Edited by: The advent of diffusion magnetic resonance imaging (MRI) allows researchers to virtually Simone Dalla Bella, University of dissect white matter fiber pathways in the brain in vivo. This, for example, allows us to Montpellier 1, France characterize and quantify how fiber tracts differ across populations in health and disease, Reviewed by: and change as a function of training. Based on diffusion MRI, prior literature reports the Daniela Sammler, Max Planck Institute for Human Cognitive and absence of the arcuate fasciculus (AF) in some control individuals and as well in those with Brain Sciences, Germany congenital amusia. The complete absence of such a major anatomical tract is surprising Dominique Vuvan, International given the subtle impairments that characterize amusia. Thus, we hypothesize that failure Laboratory for Brain, Music, and to detect the AF in this population may relate to the tracking algorithm used, and is not Sound Research, Canada necessarily reflective of their phenotype. Diffusion data in control and amusic individuals *Correspondence: Joyce L. Chen, Department of were analyzed using three different tracking algorithms: deterministic and probabilistic, Physical Therapy and Graduate the latter either modeling two or one fiber populations. Across the three algorithms, Department of Rehabilitation we replicate prior findings of a left greater than right AF volume, but do not find group Sciences, Heart and Stroke differences or an interaction. We detect the AF in all individuals using the probabilistic Foundation Canadian Partnership for Stroke Recovery, Sunnybrook 2-fiber model, however, tracking failed in some control and amusic individuals when Research Institute, University of deterministic tractography was applied. These findings show that the ability to detect Toronto, 2075 Bayview Avenue, the AF in our sample is dependent on the type of tractography algorithm. This raises M6-176, Toronto, ON M4N 3M5 the question of whether failure to detect the AF in prior studies may be unrelated to the Canada e-mail: [email protected] underlying anatomy or phenotype. †Joint last-author. Keywords: arcuate fasciculus, congenital amusia, diffusion magnetic resonance imaging, tractography, deterministic, probabilistic, crossing fibers INTRODUCTION individual behavioral differences and task demands (Williamson Diffusion magnetic resonance imaging (MRI) is widely used to et al., 2012). virtually dissect white matter fiber pathways in the brain. In the Studies of cortical anatomy in amusia show abnormalities in case of failed tracking the question arises as to whether this might the right inferior frontal cortex and superior temporal gyrus have a biological explanation or reflect limitations of the tracking (STG) (Hyde et al., 2006, 2007; Albouy et al., 2013), with reduced algorithm used (Dell’Acqua and Catani, 2012; Campbell and Pike, neural activity in the former and reduced functional connectiv- 2014). In this study we address the basis for the failure to track ity between these regions (Hyde et al., 2011). Abnormal effective a specific white matter tract in a biological disorder: the right connectivity between these regions has also been demonstrated arcuate fasciculus (AF) in congenital amusia or tone deafness. using dynamic causal modeling (Albouy et al., 2013). From first Individuals with amusia lack the ability to process aspects of principles, deficits in effective connectivity might be based on music in the absence of other neurological impairment, learning a physical disconnection caused by structural change in a fiber difficulty or hearing loss (Ayotte et al., 2002). These individu- tract, or be due to another cause in the presence of preserved als have poor pitch perception (Foxton et al., 2004; Hyde and anatomy. The former has been hypothesized in work suggest- Peretz, 2004) and pitch memory (Gosselin et al., 2009; Tillmann ing the reduced volume or absence of the right AF may underlie et al., 2009; Williamson and Stewart, 2010). Some individuals also perception-production impairments exhibited by amusics (Loui have relatively preserved pitch production abilities as compared to et al., 2009). pitch perception (Loui et al., 2008, 2009; Dalla Bella et al., 2009; The AF is a tract that connects auditory with motor brain Hutchins and Peretz, 2013). However, the extent and direction regions (Petrides, 2013) and shows asymmetries that are plausi- of such a perception-production dissociation may be related to bly related to language lateralization (Friederici, 2009). A number www.frontiersin.org January 2015 | Volume 6 | Article 9 | 1 Chen et al. Arcuate fasciculus in congenital amusia of studies have reported the inability to track the AF in the of its fibers run in a rostral-caudal direction, crossing or inter- left (Glasser and Rilling, 2008; Lebel and Beaulieu, 2009)and secting with the corticospinal tract that runs in a dorso-ventral right (Catani et al., 2007; Glasser and Rilling, 2008; Lebel and direction (Behrens et al., 2007). Beaulieu, 2009; Kaplan et al., 2010; Thiebaut de Schotten et al., Given the aforementioned differences between tracking algo- 2011) hemispheres in some healthy individuals. These studies rithms, we used three tracking algorithms all implemented in all used deterministic tracking without the modeling of multi- the FSL software package (http://www.fmrib.ox.ac.uk/fsl). This ple fibers, and in fact, two of these studies suggest that failure to allows us to control for differences that may exist between dif- detect the AF may be due to limitations of this algorithm (Glasser ferent software packages. The first two models used probabilistic and Rilling, 2008; Kaplan et al., 2010). For example, Glasser and tractography. In the first, 2-fiber model, we modeled cross- Rilling (2008) state that the AF was identified in all subjects in ing fibers. In the second, 1-fiber model, we modeled only one another study they conducted using probabilistic tractography fiber population. The third model used a deterministic tracking with crossing fiber modeling (Rilling et al., 2008). approach in which only one fiber orientation per voxel is derived One study that tested individuals with amusia showed the from the first eigenvector or dominant orientation of the diffu- right AF, connecting posterior STG with pars opercularis, could sion tensor. This model more closely resembles those used in the not be tracked in nine out of 10 participants (Loui et al., 2009). aforementioned studies (Catani et al., 2007; Glasser and Rilling, This study also used deterministic tractography without model- 2008; Lebel and Beaulieu, 2009; Loui et al., 2009; Kaplan et al., ing crossing fibers. In light of findings where the AF is undetected 2010; Thiebaut de Schotten et al., 2011) where tracking of the in some neurologically normal controls, it remains to be verified AF failed in some cases. Given that the modeling of crossing whether the disconnection syndrome in amusia is in fact related fibers (e.g., AF and corticospinal tract) is highly relevant and is to their behavioral phenotype. Therefore, the present study inves- shown to influence tractography results (Behrens et al., 2007), we tigates the extent to which the ability to detect the left and right AF hypothesize that the probabilistic 2-fiber model would be more in amusic and control individuals depends on the type of tracking robust to detect the AF compared to the probabilistic 1-fiber and algorithm. deterministic 1-fiber models. Briefly, diffusion MRI acquires a series of images to measure There exists considerable uncertainty over where the human hindrance to intra- and extra-cellular water diffusion in the brain. AF starts and ends, and consequently studies have varied in how Spontaneous water diffusion can be hindered by cellular mem- they define this tract (Dick and Tremblay, 2012). Non-human branes such as the myelin sheath that wrap the axonal tracts primate tracer studies demonstrate that the AF connects caudal of the white matter (Beaulieu, 2002). Water therefore tends to STG (area Tpt) and sulcus (area TPO) with dorsal areas 8 and flow along axons, and its pathway is hindered perpendicular to 6(Petrides and Pandya, 1988, 2002; Schmahmann and Pandya, axons. The local axon orientation estimated from the diffusion 2006). Recently, modest connections to areas 44 and 45 have data can then be used to track potential white matter pathways in been found (Petrides and Pandya, 2009). Work in human rest- the brain (by connecting neighboring voxels depending on their ing state fMRI, also show connectivity patterns that corroborate orientation). In deterministic tractography,

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