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. 2014 Jul 28;5(8):2823-36.
doi: 10.1364/BOE.5.002823. eCollection 2014 Aug 1.

Longitudinal Vascular Dynamics Following Cranial Window and Electrode Implantation Measured With Speckle Variance Optical Coherence Angiography

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Free PMC article

Longitudinal Vascular Dynamics Following Cranial Window and Electrode Implantation Measured With Speckle Variance Optical Coherence Angiography

Daniel X Hammer et al. Biomed Opt Express. .
Free PMC article

Abstract

Speckle variance optical coherence angiography (OCA) was used to characterize the vascular tissue response from craniotomy, window implantation, and electrode insertion in mouse motor cortex. We observed initial vasodilation ~40% greater than original diameter 2-3 days post-surgery (dps). After 4 weeks, dilation subsided in large vessels (>50 µm diameter) but persisted in smaller vessels (25-50 µm diameter). Neovascularization began 8-12 dps and vessel migration continued throughout the study. Vasodilation and neovascularization were primarily associated with craniotomy and window implantation rather than electrode insertion. Initial evidence of capillary re-mapping in the region surrounding the implanted electrode was manifest in OCA image dissimilarity. Further investigation, including higher resolution imaging, is required to validate the finding. Spontaneous lesions also occurred in many electrode animals, though the inception point appeared random and not directly associated with electrode insertion. OCA allows high resolution, label-free in vivo visualization of neurovascular tissue, which may help determine any biological contribution to chronic electrode signal degradation. Vascular and flow-based biomarkers can aid development of novel neural prostheses.

Keywords: (110.4500) Optical coherence tomography; (170.1470) Blood or tissue constituent monitoring; (170.3880) Medical and biological imaging; (170.6900) Three-dimensional microscopy.

Figures

Fig. 1
Fig. 1
(a) SD-OCT setup for mouse cortical angiography and (b) photograph showing window preparation (black arrowhead) with implanted electrode (white arrow).
Fig. 2
Fig. 2
Representative depth planes from OCA volumes for electrode animal W41 (day 19). (a,c) Focus depth 1. (b,d) Focus depth 2 (250 µm below focus depth 1). (a,b) Average projection for superficial plane spanning 0-100 µm below window. (c,d) Maximum projection for deep plane spanning 300-400 µm below window. Accompanying video (Media 1) has side-by-side fly-through from 0 to 800 µm for both focus conditions. Each frame of the video is a running average projection of 8 depth slices (32 µm). Scale bar = 200 µm.
Fig. 3
Fig. 3
Illustrated methodology to quantify cortical vascular dynamics, including vasodilation (a-d), vessel growth (e-g), and capillary remapping (h-l). (a) OCA image plane 100-200 µm for control animal W44 indicating 10 profile locations. (b,c) Line and rectangle ROIs for location 6. (d) Single (dashed line) and 30-line average (solid line) profiles across location 6. Symbols indicate FWHM values. OCA image plane 0-100 µm for control animal W38 for 1 (e), 8 (f) and 27 (g) dps. Thresholded ROI is overlaid on each image. (h) OCA image plane 300-400 µm for electrode animal W51 on 1 dps. ROI is indicated as well as electrode location (arrow). Similarity processing: (i) ROI (day 26), (j) Gabor filtered image, (k) local thresholded image, and (l) XNOR image between day 26 and day 34. Scale bar = 200 µm.
Fig. 4
Fig. 4
Example of vasodilation in electrode animal W43. Shown is the 100-200 µm plane on (a) 1, (b) 3, and (c) 56 dps. Arrow indicates large vessel with massive dilation on day 3 that subsides by day 56. Arrowhead indicates medium vessel with dilation on day 3 that persists on day 56. Accompanying video (Media 2) shows registered stack to visualize vasodilation over the entire time course up to 98 dps. Scale bar = 200 µm.
Fig. 5
Fig. 5
Normalized vessel diameter in (a) large and (b) medium vessels measured with OCA. Control and electrode animals are indicated by filled and open symbols and the average and standard deviation of all data is indicated by lines. Each data point represents an average of five profiles for that animal and day.
Fig. 6
Fig. 6
Representative vessel coverage in control animal W38. (a) Fractional area (%) covered by vessels in first depth plane (0-100 µm) in a 500 × 500 µm region delineated by the box in (b) for 133 dps. Accompanying video (Media 3) shows the time-lapsed registered stack. Scale bar = 200 µm.
Fig. 7
Fig. 7
Fractional area (%) covered by vessel in first depth plane (0-100 µm) for control (closed symbols) and electrode (open symbols) animals in a 500 × 500 µm region. For visual clarity, the curves are aligned to the second minimum, which is set to day 0 (i.e., after vessel dilation and before new vessel growth).
Fig. 8
Fig. 8
Capillary remodeling measured by OCA image similarity. (a) Similarity measured between the last week and all preceding weeks (excluding first two weeks). (b) Average similarity as a function of time separation between OCA images. Linear regression (solid line), 95% confidence limits (dashed line and shaded area), and correlation coefficient are shown for both groups. Accompanying video is the time-lapsed registered stack of the raw, Gabor filtered, and thresholded ROI from electrode animal W51 up to 44 dps (Media 4).
Fig. 9
Fig. 9
Cross-sectional reflectance (a) and angiography (b) images of a lesion in animal W49. En face angiography images from the 300-400 µm depth plane are shown in (c) and (d) for day 1, before formation, and day 50. Line in (d) indicates location of B-scan in (a) and (b). Electrode is denoted by arrow and lesion margin with dashed line. Accompanying video (Media 5) shows the growth in 0-200 µm and 300-400 µm depth planes. Scale bars = 100 µm.
Fig. 10
Fig. 10
En face angiography images 300-400 µm below cortical surface for electrode animals W41, W43, W44, W50, and W51. W41 showed no growth. In the others, the growth is indicated by an arrow. Upper row shows vasculature on day 1 before new growth and lower row show vasculature after lesion formation (dps indicated). Each image is 2 × 2 mm. Scale bar = 200 µm.

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