Multi-reference global registration of individual A-lines in adaptive optics optical coherence tomography retinal images

Abstract. Significance: Adaptive optics optical coherence tomography (AO-OCT) technology enables non-invasive, high-resolution three-dimensional (3D) imaging of the retina and promises earlier detection of ocular disease. However, AO-OCT data are corrupted by eye-movement artifacts that must be removed in post-processing, a process rendered time-consuming by the immense quantity of data. Aim: To efficiently remove eye-movement artifacts at the level of individual A-lines, including those present in any individual reference volume. Approach: We developed a registration method that cascades (1) a 3D B-scan registration algorithm with (2) a global A-line registration algorithm for correcting torsional eye movements and image scaling and generating global motion-free coordinates. The first algorithm corrects 3D translational eye movements to a single reference volume, accelerated using parallel computing. The second algorithm combines outputs of multiple runs of the first algorithm using different reference volumes followed by an affine transformation, permitting registration of all images to a global coordinate system at the level of individual A-lines. Results: The 3D B-scan algorithm estimates and corrects 3D translational motions with high registration accuracy and robustness, even for volumes containing microsaccades. Averaging registered volumes improves our image quality metrics up to 22 dB. Implementation in CUDA™ on a graphics processing unit registers a 512  ×  512  ×  512 volume in only 10.6 s, 150 times faster than MATLAB™ on a central processing unit. The global A-line algorithm minimizes image distortion, improves regularity of the cone photoreceptor mosaic, and supports enhanced visualization of low-contrast retinal cellular features. Averaging registered volumes improves our image quality up to 9.4 dB. It also permits extending the imaging field of view (∼2.1  ×  ) and depth of focus (∼5.6  ×  ) beyond what is attainable with single-reference registration. Conclusions: We can efficiently correct eye motion in all 3D at the level of individual A-lines using a global coordinate system.

[1]  Gangjun Liu,et al.  Automated three-dimensional registration and volume rebuilding for wide-field angiographic and structural optical coherence tomography , 2017, Journal of biomedical optics.

[2]  Carlo Tomasi,et al.  Automated non-rigid registration and mosaicing for robust imaging of distinct retinal capillary beds using speckle variance optical coherence tomography , 2013, Biomedical optics express.

[3]  Furu Zhang,et al.  Suite of methods for assessing inner retinal temporal dynamics across spatial and temporal scales in the living human eye , 2020, Neurophotonics.

[4]  Dirk R. Padfield,et al.  Masked Object Registration in the Fourier Domain , 2012, IEEE Transactions on Image Processing.

[5]  Donald T. Miller,et al.  In vivo measurement of organelle motility in human retinal pigment epithelial cells. , 2019, Biomedical optics express.

[6]  Fabrice Manns,et al.  Correcting for Miniature Eye Movements in High Resolution Scanning Laser Ophthalmoscopy , 2005 .

[7]  Y. Hwang,et al.  The effect of head tilt on the measurements of retinal nerve fibre layer and macular thickness by spectral-domain optical coherence tomography , 2011, British Journal of Ophthalmology.

[8]  C. Hitzenberger,et al.  Simultaneous SLO/OCT imaging of the human retina with axial eye motion correction. , 2007, Optics express.

[9]  D. Hubel,et al.  The role of fixational eye movements in visual perception , 2004, Nature Reviews Neuroscience.

[10]  Ravi S. Jonnal,et al.  Imaging cone photoreceptors in three dimensions and in time using ultrahigh resolution optical coherence tomography with adaptive optics , 2011, Biomedical optics express.

[11]  Yifan Jian,et al.  Strip-based registration of serially acquired optical coherence tomography angiography , 2017, Journal of biomedical optics.

[12]  Zhuolin Liu,et al.  Adaptive optics optical coherence tomography at 1 MHz. , 2014, Biomedical optics express.

[13]  Mohammad Shorif Uddin,et al.  Image Quality Assessment through FSIM, SSIM, MSE and PSNR—A Comparative Study , 2019, Journal of Computer and Communications.

[14]  Kazuhiro Sasaki,et al.  Extended depth of focus adaptive optics spectral domain optical coherence tomography , 2012, Biomedical optics express.

[15]  E. F. Miller,et al.  Counterrolling of the human eyes produced by head tilt with respect to gravity. , 1962, Acta oto-laryngologica.

[16]  Kazuhiro Kurokawa,et al.  Cellular Scale Imaging of Transparent Retinal Structures and Processes Using Adaptive Optics Optical Coherence Tomography. , 2020, Annual review of vision science.

[17]  B. N. Chatterji,et al.  An FFT-based technique for translation, rotation, and scale-invariant image registration , 1996, IEEE Trans. Image Process..

[18]  Shuichi Makita,et al.  Three-dimensional eye motion correction by Lissajous scan optical coherence tomography. , 2017, Biomedical optics express.

[19]  Nhan Hieu Do,et al.  Parallel processing for adaptive optics optical coherence tomography (AO-OCT) image registration using GPU , 2016 .

[20]  A. Milam,et al.  Distribution and morphology of human cone photoreceptors stained with anti‐blue opsin , 1991, The Journal of comparative neurology.

[21]  Donald T. Miller,et al.  Measuring dysfunction of cone photoreceptors in retinitis pigmentosa with phase-sensitive AO-OCT , 2020, BiOS.

[22]  Jan Kautz,et al.  Local Laplacian filters: edge-aware image processing with a Laplacian pyramid , 2011, ACM Trans. Graph..

[23]  Robert A. Schowengerdt,et al.  IKONOS Spatial Resolution and Image Interpretability Characterization , 2003 .

[24]  Austin Roorda,et al.  Retinal motion estimation in adaptive optics scanning laser ophthalmoscopy. , 2006, Optics express.

[25]  Alfredo Dubra,et al.  Registration of 2D Images from Fast Scanning Ophthalmic Instruments , 2010, WBIR.

[26]  Austin Roorda,et al.  Retinally stabilized cone-targeted stimulus delivery. , 2007, Optics express.

[27]  David R. Haynor,et al.  Nonrigid multimodality image registration , 2001, SPIE Medical Imaging.

[28]  Omer P. Kocaoglu,et al.  3D Imaging of Retinal Pigment Epithelial Cells in the Living Human Retina , 2016, Investigative ophthalmology & visual science.

[29]  Daniel X Hammer,et al.  Adaptive optics optical coherence tomography with dynamic retinal tracking. , 2014, Biomedical optics express.

[30]  Phillip Bedggood,et al.  De-warping of images and improved eye tracking for the scanning laser ophthalmoscope , 2017, PloS one.

[31]  Austin Roorda,et al.  Real-time eye motion compensation for OCT imaging with tracking SLO , 2012, Biomedical optics express.

[32]  Omer P. Kocaoglu,et al.  Phase-sensitive imaging of the outer retina using optical coherence tomography and adaptive optics , 2011, Biomedical optics express.

[33]  Donald T. Miller,et al.  Cone photoreceptor classification in the living human eye from photostimulation-induced phase dynamics , 2019, Proceedings of the National Academy of Sciences.

[34]  Iwona Gorczynska,et al.  Intraframe motion correction for raster-scanned adaptive optics images using strip-based cross-correlation lag biases , 2018, PloS one.

[35]  James G. Fujimoto,et al.  Motion correction in optical coherence tomography volumes on a per A-scan basis using orthogonal scan patterns , 2012, Biomedical optics express.

[36]  Zhihua Ding,et al.  High-resolution optical coherence tomography over a large depth range with an axicon lens. , 2002, Optics letters.

[37]  Frédo Durand,et al.  Fast Local Laplacian Filters , 2014, ACM Trans. Graph..

[38]  R. Leitgeb,et al.  Extended focus depth for Fourier domain optical coherence microscopy. , 2006, Optics letters.

[39]  H. Collewijn,et al.  A direct test of Listing's law—I. Human ocular torsion measured in static tertiary positions , 1987, Vision Research.

[40]  Bernard Sklar,et al.  Digital communications : fundamentals and applications , 2020 .

[41]  Omer P. Kocaoglu,et al.  A Review of Adaptive Optics Optical Coherence Tomography: Technical Advances, Scientific Applications, and the Future , 2016, Investigative ophthalmology & visual science.

[42]  Omer P. Kocaoglu,et al.  In-the-plane design of an off-axis ophthalmic adaptive optics system using toroidal mirrors. , 2013, Biomedical optics express.

[43]  Bo Wang,et al.  Adaptive optics optical coherence tomography in glaucoma , 2017, Progress in Retinal and Eye Research.

[44]  Donald T. Miller,et al.  Imaging and quantifying ganglion cells and other transparent neurons in the living human retina , 2017, Proceedings of the National Academy of Sciences.

[45]  Daniel X Hammer,et al.  Adaptive optics scanning laser ophthalmoscope with integrated wide-field retinal imaging and tracking. , 2010, Journal of the Optical Society of America. A, Optics, image science, and vision.