The visual white-matter matters! Innovation, data, methods and applications of diffusion MRI and fiber tractography

Organizers: Franco Pestilli & Ariel Rokem; Stanford University
Presenters: Ariel Rokem, Andrew Bock, Holly Bridge, Suzy Scherf, Hiromasa Takemura, David Van Essen

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Symposium Description

For about two decades, functional MR imaging has allowed investigators to map visual cortex in the living human brain. Vision scientists have identified clusters of cortical regions with different functional properties. The function of these maps is determined by both the selectivity of their neurons, as well as their connections. Communication between cortical regions is carried by long-range white-matter fascicles. The wiring of these fascicles is important for implementing the perceptual functions of the visual maps in the occipital, temporal and parietal cortex. Magnetic resonance diffusion imaging (dMRI) and computational tractography are the only technologies that enable scientists to measure the white matter in the living human brain. In the decade since their development, these technologies revolutionized our understanding of the importance of human white-matter for health and disease. Recent advances in dMRI and fiber tractography have opened new avenues of understanding the white-matter connections in the living human brain. With the advent of these technologies we are for the first time in a position to draw a complete wiring diagram of the human visual system. By probing the motion of water molecules at the micron scale, dMRI can be used to study the microstructural properties and geometric organization of the visual white-matter fascicles. These measurements in living brains can help clarify the relationship between the properties of the tissue within the fascicles and visual perception, both in healthy individuals and in cases where vision is impeded through disease. Prior to these measurements, the white matter was thought of as a passive cabling system. But modern measurements show that white matter axons and glia respond to experience and that the tissue properties of the white matter are transformed during development and following training. The white matter pathways comprise a set of active wires and the responses and properties of these wires predict human cognitive and perceptual abilities. This symposium targets a wide range of investigators working in vision science by providing an introduction to the principles of dMRI measurements, algorithms used to identify anatomical connections and models used to characterize white-matter properties. The speakers have pioneered the use of diffusion and functional MRI and fiber tractography to study the human visual white-matter in answering a wide range of scientific questions: connectivity, development, plasticity. The symposium will also introduce publicly available resources (analysis software and data) to help advance the study of the human visual cortex and white-matter, with special emphasis on the high-quality MR measurements provided by the Human Connectome Project (HCP).


Measuring and modelling of diffusion and white-matter tracts

Speaker: Ariel Rokem; Stanford University
Authors: Franco Pestilli

This talk will present a general methodological overview of diffusion MRI (dMRI), with a special focus on methods used to image connectivity and tissue properties in the human visual system. We will start by describing the principles of dMRI measurements. We will then provide an overview of models that are used to describe the signal and make inferences about the properties of the tissue and the trajectories of fiber fascicles in white-matter. We will focus on the classical Diffusion Tensor Model (DTM), which is used in many applications, and on the more recent development of Sparse Fascicle Models (SFM), which are more realistic representations of the signal as a combination of signals from different fascicles. Using cross-validation, we have found that DTM provides an accurate representation of the data, better than the reliability of a repeated measurement. SFM provide even more accurate models of the data, and particularly in regions where different fiber tracts cross. In the second part of the talk, we will focus on tractography. With special emphasis on probabilistic and deterministic tractography. We will introduce ideas about validation of white-matter trajectories and to perform statistical inferences about connectivity between different parts of the visual system. A major problem of the field is that different algorithms provide different estimates of connectivity. This problem is solved by choosing the fiber estimates that best account for the data in a repeated measurement (cross-validation).

Gross topographic organization in the corpus callosum is preserved despite abnormal visual input.

Speaker: Andrew Bock; University of Washington
Authors: Melissa Saenz, University of Laussane; Holly Bridge, Oxford; Ione Fine, University of Washington.

The loss of sensory input early in development has been shown to induce dramatic anatomical and functional changes within the central nervous system. Using probabilistic diffusion tractography, we examined the retinotopic organization of splenial callosal connections within early blind, anophthalmic, achiasmatic and control subjects. Early blind subjects experience prenatal retinal “waves” of spontaneous activity similar to those of sighted subjects, and only lack postnatal visual experience. In anophthalmia, the eye is either absent or arrested at an early prenatal stage, depriving these subjects of both pre- and postnatal visual input, while in achiasma there is a lack of crossing at the optic chiasm such that the white matter projection from each eye is ipsilateral. Comparing these groups provides a way of separating the influence of pre- and postnatal retinal deprivation and abnormal visual input on the organization of visual connections across hemispheres. We found that retinotopic mapping within the splenium was not measurably disrupted in any of these groups compared to visually normal controls. These results suggest that neither prenatal retinal activity nor postnatal visual experience plays a role in the large-scale topographic organization of visual callosal connections within the splenium, and the general method we describe provides a useful way of quantifying the organization of large white matter tracts.

Using diffusion-weighted tractography to investigate dysfunction of the visual system

Speaker: Holly Bridge; Oxford
Authors: Rebecca Millington; James Little; Kate Watkins

The functional consequences of damage to, or dysfunction of, different parts of the visual pathway have been well characterized for many years. Possibly the most extreme dysfunction is the lack of eyes (anophthalmia) which prevents any stimulation of this pathway by light input. In this case, functional MRI indicates the use of the occipital cortex for processing of language, and other auditory stimuli. This raises the question of how this information gets to the occipital cortex; are there differences in the underlying anatomical connectivity or can existing pathways be used to carry different information? Here I’ll describe several approaches we have taken to try to understand the white matter connectivity in anophthalmia using diffusion tractography. Damage to the visual pathway can also be sustained later in life, either to the periphery or to the post-chiasmatic pathway (optic tract, lateral geniculate nucleus, optic radiation or visual cortex). When damage occurs in adulthood, any changes to white matter are likely to be the result of degeneration. Sensitive measures of white matter integrity can be used to illustrate patterns of degeneration in patient populations. However, it is also the case that in the presence of lesions, and where white matter tracts are relatively small (e.g. optic tract) measures derived from diffusion-weighted imaging can be misleading. In summary I will present an overview of the potential for employing diffusion tractography to understand plasticity and degeneration in the abnormal visual system, highlighting potential confounds that may arise in patient populations.

Structural properties of white matter circuits necessary for face perception

Speaker: Suzy Scherf; Penn State
Authors: Marlene Behrmann, Carnegie Mellon University; Cibu Thomas, NIH; Galia Avidan, Beer Sheva University; Dan Elbich, Penn State University

White matter tracts, which communicate signals between cortical regions, reportedly play a critical role in the implementation of perceptual functions. We examine this claim by evaluating structural connectivity, and its relationship to neural function, in the domain of face recognition in both developing individuals and those with face recognition deficits. In all studies, we derived the micro- as well as macro-structural properties of the inferior longitudinal fasciculus (ILF) and of the inferior fronto-occipital fasciculus (IFOF), which connect distal regions of cortex that respond preferentially to faces. In participants aged 6-23 years old, we observed age-related differences in both the macro- and micro-structural properties of the ILF. Critically, these differences were specifically related to an age-related increase in the size of the functionally defined fusiform face area. We then demonstrated the causal nature of the structure-function relationship in individuals who are congenitally prosopagnosic (CP) and in an aging population (who exhibits an age-related decrement in face recognition). The CPs exhibited reduced volume of the IFOF and ILF, which was related to the severity of their face processing deficit. Similarly, in the older population there were also significant reductions in the structural properties of the ILF and IFOF that were related to their behavioral performance. Finally, we are exploring whether individual differences in face-processing behavior of normal adults are related to variations in these structure-function relations. This dynamic association between emerging structural connectivity, functional architecture and perceptual behavior reveals the critical role of neural circuits in human cortex and perception.

A major white-matter wiring between the ventral and dorsal stream

Speaker: Hiromasa Takemura; Stanford University
Authors: Brian Wandell

Over the last several decades, visual neuroscientists have learned how to use fMRI to identify multiple visual field maps in the living human brain. Several theories have been proposed to characterize the organization of these visual field maps, and a key theory with substantial support distinguishes dorsal stream involving with spatial processing and ventral stream involving categorical processing. We combined fMRI, diffusion MRI and fiber tractography to identify a major white matter pathway, the Vertical Occipital Fasciculus (VOF), connecting maps within the dorsal and ventral visual streams. We use a model-based method, LInear Fascicle Evaluation (LIFE), to assess the statistical evidence supporting the VOF wiring pattern. There is strong evidence supporting the hypothesis that dorsal and ventral streams of visual maps communicate through the VOF. This pathway is large and its organization suggests that the human ventral and dorsal visual maps communicate substantial information through V3A/B and hV4/VO-1. We suggest that the VOF is crucial for transmitting signals between regions that encode object properties including form, identity and color information and regions that map spatial location to action plans. Findings on the VOF will extend the current understandings of the human visual field map hierarchy.

What is the Human Connectome Project telling us about human visual cortex?

Speaker: David Van Essen; Washington University

The Human Connectome Project (HCP) is acquiring and sharing vast amounts of neuroimaging data from healthy young adults, using high-resolution structural MRI, diffusion MRI, resting-state fMRI, and task-fMRI. Together, these complementary modalities provide invaluable information and insights regarding the organization and connectivity of human visual cortex. This presentation will highlight recent results obtained using surface-based analysis and visualization approaches to characterize structural and functional connectivity of visual cortex in individuals and group averages.

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