Investigation of feline brain anatomy for the detection of cortical spreading depression with magnetic resonance imaging

Abstract

Cortical spreading depression (CSD) and peri-infarct depolarisation (PID) are related phenomena that have been associated with the human clinical syndromes of migraine (CSD), head injury and stroke (PID). Nevertheless the existence of CSD in man remains controversial, despite the detection of this phenomenon in the brains of most, if not all, other animal species investigated. This failure to unambiguously detect CSD clinically may be at least partly due to the anatomically complex, gyrencephalic structure of the human brain. This study was designed to establish conditions for the study of CSD in the brain of a gyrencephalic species using the noninvasive technique of magnetic resonance imaging (MRI). The 3-dimensional (3D) gyrencephalic anatomy of the cat brain was examined to determine the imaging conditions necessary to detect CSD events. Orthogonal transverse, sagittal and horizontal T " -weighted image slices showed that the marginal and suprasylvian gyri were the most appropriate cortical structures to study CSD. This was in view of (1) their simple geometry : (2) their lengthy extent of grey matter orientated rostrocaudally in the cortex : (3) their separation by a sulcus across which CSD spread could be studied and (4) the discontinuity in the grey matter in these regions between the right and left hemispheres dorsal to the corpus callosum. The structure suggested by the T " -weighted images was corroborated by systematic diffusion tensor imaging to map the fractional anisotropy and diffusion trace. Thus a single horizontal image plane could visualise the neighbouring suprasylvian and marginal gyri of both cerebral hemispheres, whereas its complex shape and position ruled out the ectosylvian gyrus for CSD studies. With the horizontal imaging plane, CSD events were reproducibly detected by animating successive diffusion-weighted MR images following local KCl stimulation of the cortical surface. In single image frames, CSD detection and characterisation required image subtraction or statistical mapping methods that, nevertheless, yielded concordant results. In repeat experiments, CSD events were qualitatively similar in appearance whether elicited by sustained or transient KCl applications. Our experimental approach thus successfully describes cat brain anatomy in vivo, and elucidates the necessary conditions for the application of MRI methods to detect CSD propagation.

Distinct Spatiotemporal Patterns of Spreading Depolarizations during Early Infarct Evolution: Evidence from Real-Time Imaging

“…Waves typically crossed all 25 analyzed ROIs, and we suspect that they spread over the entire cortex. Concentric wave propagation of CSDs has been described in rats and cats under physiological conditions after induction with high potassium (Farkas et al, 2008;Smith et al, 2001;Tomita et al, 2002). In focal ischemia, in contrast, rostral-caudal or circumferential propagation around the ischemic core seems to be the predominant pattern (Hartings et al, 2003;Luckl et al, 2009;Nakamura et al, 2010).…”

Development of cerebral sulci and gyri in ferrets (Mustela putorius)

“…Ferrets (Mustela putorius) are the smallest laboratory animals in terms of the highly convoluted surface of the cerebrum, forming striking patterns of sulci and gyri (Smart and McSherry 1986a;Lawes and Andrews, 1998;Neal et al 2007; Barnette et al 2009), which are comparable to those in cats (Ferrer et al 1988;Smith et al 2001) and dogs (Wosinski et al 1996). The advantageous characteristic of this animal is that neurodevelopmental events occurred in utero in primates (i.e., early stage of neurogenesis and sulcal infolding) are experienced following birth (Smart and McSherry 1986a;Clancy et al 2001).…”

The Brain Anatomy of the Brown Bear (Carnivora, Ursus arctos L., 1758) Compared to That of Other Carnivorans: A Cross-Sectional Study Using MRI

“…The brain surface of the brown bear is highly visually convoluted with a presence of secondary sulci and gyri. It is more convoluted with respect to the dog (Uemura, 2015), the cat (Smith et al, 2001) or to Mustelidae (Radinsky, 1975) and Viverridae species (Radinsky, 1975). However, it is less convoluted than in Pinnipedia: Zalophus californianus (Montie et al, 2009), northern fur seal ( Callorhinus ursinus ) and Steller sea lion ( Eumetopias jubatus ) (based on specimens available in CMBC).…”

“…The same observation was made for giant panda ( Ailuropoda melanoleuca ) (Mettler and Goss, 1946; Dong, 2008), U. maritimus (Dong, 2008) and the sun bear ( Helarctos malayanus ) (Kamiya and Pirlot, 1988b). The consequence of that reduction is lowering of SSsR and SSsC from dorsal to lateral surface of the hemisphere, their considerable shortening and shape change in comparison to the dog (Uemura, 2015) and the cat (Smith et al, 2001). SSsR and SSsC are together arcuate in the cat and dog, but in U. arctos are more hairpin-shaped, therefore the sulcus suprasylvius medius is absent.…”

“…The structure, GFM and GFV are all apparent in Ursidae (Mettler and Goss, 1946; Kamiya and Pirlot, 1988b; Welker et al, 2009) and Pinnipedia (Montie et al, 2009; Welker et al, 2009). On the other hand only one gyrus frontalis is present in the dog (Meyer, 1964; Uemura, 2015) and in the cat none of the gyri frontales is observed (Smith et al, 2001; Kobryń and Kobryńczuk, 2004). The course of SCr (Figure 1A) is variable in our samples.…”