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Laminar Optical Tomography: High-Resolution 3D Functional Imaging of Superficial Tissues

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Laminar Optical Tomography: High-Resolution 3D Functional Imaging of Superficial Tissues Laminar optical tomography: high-resolution 3D functional imaging of superficial tissues Elizabeth M. C Hillman *a, Anna Devor a, Andrew K. Dunn b, David A. Boas a aAthinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Harvard Medical School, CNY 149, 13 th Street, Charlestown MA 02129. bDepartment of Biomedical Engineering, University of Texas at Austin, 1 University Station, C0800, Austin, TX 78712 ABSTRACT Laminar Optical Tomography (LOT) is a new medical imaging modality for high-resolution, depth-resolved, functional imaging of superficial tissue such as rodent cortex, skin and the retina. LOT uses visible laser light to image to depths of >2mm (far deeper than microscopy) and is highly sensitive to absorption and fluorescence contrast, enabling spectroscopic functional information such as hemoglobin oxygenation to be imaged with 100-200 micron resolution. LOT has been used to image the hemodynamic response to stimulus in the somatosensory cortex of rats. The resulting three-dimensional (3D) images through the depth of the cortex can be used to delineate the arterial, capillary and venous responses, revealing new information about the intricacies of the oxygenation and blood flow dynamics related to neuronal activation. Additional applications of LOT are being explored, including the integration of 3D Voltage Sensitive Dye fluorescence imaging. LOT imaging uses a system similar to a confocal microscope, quickly scanning a focused beam of light over the surface of the tissue (~8Hz frame rate). Light is detected from both the focus of the scanning beam, and also at increasing distances from the beam’s focus. This scattered light has penetrated more deeply into the tissue, and allows features at different depths to be distinguished. An algorithm that includes photon migration modeling of light scattering converts the raw data into 3D images. The motivation for functional optical imaging will be outlined, the basic principles of LOT imaging will be described, and the latest in-vivo results will be presented. Keywords: Optical Imaging, Functional imaging, Depth-resolved, Brain, Cortex, High-resolution, hemoglobin 1. INTRODUCTION Optical imaging provides unparalleled sensitivity to functional parameters such as hemoglobin oxygenation, membrane potential and metabolic processes. In-vivo optical imaging of superficial tissues using CCD cameras has provided valuable insights into the underlying physiology of both healthy and diseased tissues. However, CCD-based imaging allows only two-dimensional (2D) imaging of the surface of the tissue. Such 2D images constitute a superficially weighted sum of signals from the first few hundred microns of tissue depth, and provide no way to distinguish whether observed features are shallow or deep. Laminar Optical Tomography (LOT) is a new optical imaging modality which allows high-resolution, depth-resolved optical imaging of tissue to depths of >2mm, with resolution of 100-200 microns, at ~8Hz frame rate. Since LOT is a completely non-contact technique, additional imaging or point measurements can be made simultaneously, such as electrophysiology recordings or speckle-flow imaging 1. To date, LOT has been used to image depth-resolved hemodynamic functional activation in the brains of rats undergoing somatosensory stimulus. The hemodynamic response is imaged using two wavelengths of light (473nm and 532nm) to produce 3D images of oxy-, deoxy- and total hemoglobin (HbO, HbR and HbT) concentration changes. Imaging the hemodynamic response in rat cortex allows the underlying mechanisms of brain activation in both healthy and disease-model animals to be examined in a controlled way. *[email protected] ; phone: 617 643 1917; fax 617 726 7422; www.nmr.mgh.harvard.edu/~ehillman CCD-based 2D imaging provides an important tool for basic research 2, 3 . However, the cortex is an intrinsically 3D structure both in terms of its neuronal organization, and its vascular architecture. Neurons and their dendritic arborizations are organized in layers, with connections to other parts of the brain such as the thalamus at distinct depths. The vascularization of the brain consists of a network of large arteries and veins on the surface of the cortex, which branch and dive perpendicularly to the surface to deeper capillary beds. When imaging of the cortical surface is performed using a camera, there is no way to distinguish between signals originating from deeper cortical layers or superficial structures. Not only does this prevent detailed analysis of the layer-specific dynamics, it also affects the ability to quantitatively analyze the observed data. In rats, the somatosensory cortex is around 2mm thick. LOT has been used to image the hemodynamic response to stimulus of rats through the thickness of the cortex. It was found that LOT gave sufficient separation between superficial and deeper signals, that it was possible to spatio-temporally separate the contributions to the hemodynamic response from arteriolar, capillary and venous vascular compartments. This paper begins by explaining the LOT method in terms of its hardware and image reconstruction algorithm. Performance of LOT imaging is then demonstrated using a phantom consisting of a human hair at varying depths in an absorbing and scattering solution. In-vivo imaging results are then presented, demonstrating LOT’s ability to resolve the depth-dependence of the hemodynamic response in the cortex. Finally, future directions of LOT development are discussed, including its potential for use as a fluorescence imaging tool, and also for depth-resolved functional imaging of other stratified tissues such as skin, the retina and endothelial tissues. 2. METHOD 2.1. Optical design LOT uses a system similar in design to a confocal microscope, raster scanning a focused laser beam over the surface of the tissue being imaged. However, unlike confocal microscopy, LOT does not achieve its depth-resolution by scanning the z-position of the beam’s focus. Instead, LOT detects both confocal and multiply scattered light. Light that has been multiply scattered emerges a distance away from the focus of the scanning spot. The further away that the light emerges, the deeper on average it has traveled. LOT measures this scattered light at 7 different distances away from the scanning spot. In this way, LOT has seven different pieces of information for each spot scanned, each with a differently weighted depth-sensitivity. These measurements can be combined with an image reconstruction algorithm which incorporates a mathematical model of light propagation in scattering tissue to convert raw measurements into 3D images. The measurement geometry achieved using LOT is depicted in Figure 1. Figure 1. LOT scanning measurement geometry. Light from successively increasing distances away from the focused spot is measured as the spot raster scans the tissue. The confocal-type design of the LOT system is shown in Figure 2. Light from one of two lasers is emitted from an optical fiber and collimated. This light passes through a polarizing beam splitter and onto galvanometer scanning mirrors which steer the collimated beam through a scan lens. The scan lens focuses the beam at an intermediate image plane, which is imaged onto the surface of the tissue using an objective lens. Light remitted from the tissue then passes back up through the objective, through the scan lens and is de-scanned by the galvanometers. Since the incident laser light was strongly polarized, specular reflections from optics and from the surface of the tissue will maintain this polarization. However, light which has been multiply scattered should quickly lose its original polarization. Therefore the light returning from the tissue which is reflected from the polarizing beam splitter should represent around 50% of the scattered light emerging from the sample. The use of a polarizing beam splitter not only provides substantially more efficiency than using a 50:50 beam-splitter, but it also dramatically reduces the effects of specular reflections. The light then passes through a lens and is focused onto a linear fiber bundle. In a confocal microscope, this focal plane would hold a pinhole which would isolate only the light returning from the very focus of the scanning beam. However, the line of fibers in the LOT system acts like 7 axially-offset pinholes, each leading to a separate detector. The black dotted lines in Figure 2 trace the path of light coming from a position adjacent to the scanning spot’s focus on the imaged object. As this light passes back up through the system it is also de-scanned and finally is focused at a corresponding adjacent position in the fiber-bundle image plane. This line of optical fibers therefore effectively creates the imaging geometry shown in Figure 2. As the galvanometers scan the focused beam over the surface of the tissue being imaged, each of the seven avalanche photodiode detectors collects the light emerging from the tissue at 7 fixed distances from the scanning spot (between 0 and 2mm away). The result is seven 2D images per raster scan (e.g. 50 x 50 pixels over a 3.5mm square field of view). These images are equivalent to tomographic reflectance measurements from 50 x 50 = 2500 source positions and 50 x 50 x 7 = 17,500 detector positions. Figure 2. Laminar Optical Tomography system for depth-resolved hemodynamic imaging of rat cortex. 50x50 image frames can currently be acquired in 100ms. Apart from the additional detectors and lack of z-scanning, the LOT system also differs from a confocal microscope in that it is generally operated with 1 x magnification and a low NA objective lens. Also, the focal lengths of lenses and distances between each optical element were carefully optimized using a ray-tracing model of the system written in Matlab. This was required since the off-axis light returning from the imaged tissue does not pass through the system in the same way as confocal light does. The system’s elements needed to be carefully designed to optimize the passage of the off-axis light back to the detection plane and to avoid clipping of the optics.
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