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- MATERIALS AND METHODS
- LITERATURE CITED
Magnetic resonance imaging offers a means of observing the internal structure of the brain where traditional procedures of embedding, sectioning, staining, mounting, and microscopic examination of thousands of sections are not practical. Furthermore, internal structures can be analyzed in their precise quantitative spatial interrelationships, which is difficult to accomplish after the spatial distortions often accompanying histological processing. For these reasons, magnetic resonance imaging makes specimens that were traditionally difficult to analyze, more accessible. In the present study, images of the brain of a white whale (Beluga) Delphinapterus leucas were scanned in the coronal plane at 119 antero-posterior levels. From these scans, a computer-generated three-dimensional model was constructed using the programs VoxelView and VoxelMath (Vital Images, Inc.). This model, wherein details of internal and external morphology are represented in three-dimensional space, was then resectioned in orthogonal planes to produce corresponding series of “virtual” sections in the horizontal and sagittal planes. Sections in all three planes display the sizes and positions of such structures as the corpus callosum, internal capsule, cerebral peduncles, cerebral ventricles, certain thalamic nuclear groups, caudate nucleus, ventral striatum, pontine nuclei, cerebellar cortex and white matter, and all cerebral cortical sulci and gyri. Anat Rec 262:429–439, 2001. © 2001 Wiley-Liss, Inc.
Odontocetes (toothed whales, dolphins, and porpoises) have undergone a number of evolutionary modifications from their terrestrial ancestral state. Among these changes was a major increase in relative brain size. Several modern odontocete species possess encephalization levels second only to modern humans when brain-body allometry is taken into account (Ridgway and Brownson, 1984; Marino, 1998). An arguably equally dramatic transformation of odontocetes occurred in the anatomical structure and organization of their brains. Compared with many other mammalian brains, odontocete brain morphology is unusual in many respects. Researchers have stated that “…the lobular formations in the dolphin brain are organized in a pattern fundamentally different from that seen in the brains of primates or carnivores” (Morgane et al., 1980). Because of the fifty-five to sixty million year divergence between cetaceans and other mammals, odontocete brains represent a blend of early mammalian features along with unique derived characteristics (Ridgway, 1986, 1990; Glezer et al., 1988; Manger et al., 1998). The differences between odontocete and other mammalian brains of similar size are present at the level of cortical cytoarchitecture and immunohistochemistry (Garey et al., 1985; Garey and Leuba, 1986; Glezer and Morgane, 1990; Hof et al., 1992, 1995; Glezer et al., 1990, 1992a,b, 1993, 1998), cortical surface morphology (Jacobs et al., 1979; Morgane et al., 1980; Haug, 1987), noncortical structures and features (Tarpley and Ridgway, 1994; Glezer et al., 1995a,b), and ontogenesis (Oelschlager and Buhl, 1985; Buhl and Oelschlager, 1988; Oelschlager and Kemp, 1998).
Although there are a number of published descriptions of cetacean neuroanatomy (see Morgane et al., 1986; Ridgway, 1990; for reviews of this literature) there are only a handful of studies in which morphometric analyses were conducted in a systematic way permitting quantitative comparative analysis with other mammals (Jacobs et al., 1984; Johnson et al., 1984; Schwerdtfeger et al., 1984; Garey and Leuba, 1986; Johnson et al., 1994; Tarpley and Ridgway, 1994; Manger et al., 1998; Marino, 1998). Furthermore, with the exception of Morgane et al. (1980), Ridgway and Brownson (1984), Haug (1987), and Tarpley and Ridgway (1994) there are no systematic anatomical descriptions of whole cetacean brains and substructures at the qualitative level. There currently exists no comprehensive cetacean neuroanatomical atlas either in paper or electronic format on which to base studies of cetacean brain organization and function. This situation is mainly due to the time and practicality associated with the preparation of such large brain specimens. Magnetic resonance imaging (MRI) offers a means of observing the internal structure of the brain where traditional procedures of embedding, sectioning, staining, mounting, and microscopic examination of thousands of sections are not practical. Furthermore internal structures can be analyzed in their precise spatial interrelationships, which is difficult to accomplish after the spatial distortions often accompanying histological processing. This study presents an anatomically-labeled three-dimensional atlas, created from MRI images, of the brain of one of the most behaviorally studied odontocetes, the white whale (Delphinapterus leucas).
- Top of page
- MATERIALS AND METHODS
- LITERATURE CITED
This study presents the first MRI-based, anatomically-labeled, three-dimensional atlas of the brain of the white (beluga) whale (Delphinapterus leucas). In addition, we have constructed three-dimensional models of the white whale brain and produced “virtual” horizontal and sagittal sections from these original images. These reconstructed images allow for the visualizing of a range of distinctive white whale brain features from various orientations by preserving the gross morphological and internal structure of the specimen. Because there are none of the distortions associated with histological processing, we have a more realistic view of the brain as it was in situ.
Many cortical features are easily identified from the original MRI scans and “virtual” images. These include the distinctive lobular formations, gyral and sulcal patterns, and general gradient of elaboration in the parietal, occipital, and temporal regions. Subcortical allometry, including that of both gray and white matter structures, is easily assessed as well. Our findings are consistent with what has been noted in the few existing histological studies of the odontocete brain. Moreover, because we are able to preserve the internal structure of the specimen, neuroanatomical studies of brains from MRI set the stage for much-needed accurate and reliable morphometric analyses of various brain structures in odontocetes. These studies are underway.
There is a deep evolutionary divergence of the Order Cetacea (of which Odontoceti is a suborder) from other mammalian lines. Furthermore, cetacean evolution is characterized by distinctive environmental pressures associated with a fully aquatic existence versus a terrestrial lifestyle. These related attributes make the comparative study of structure-function relationships in cetacean brains, compared with those of other mammals, uniquely valuable for improving our understanding of the parameters of mammalian brain evolution.
The brain of the white whale as revealed in this study is characterized by similar morphological trends as those found in the bottlenose dolphin and other cetaceans (Morgane et al., 1980). Although there are differences among cetacean brains, these differences are relatively minor compared with the striking dissimilarities to brains of other mammals. The most obvious difference between cetacean brains and those of other mammals is in the gross morphological configuration of the whole structure and the lobules of the cerebral hemispheres. These are well-visualized in MRI scans. Evolution of overall brain shape in cetaceans may have been partly due to migration of the blowhole and telescoping of the skull, i.e., antorbital elongation and postorbital compression. This in turn may account for the distinctive construction of the midbrain, i.e., the corticopontine, corticobulbar and corticospinal fibers travel high on the lateral surface whereas the ventral surface is occupied by a large continuous mass of gray matter extending from the diencephalon rostrally to the pontine nuclei caudally. There may be distinctive organizational features of the basal ganglia that also contribute to this uniquely cetacean architecture.
There is also adequate evidence that many of the anatomical changes in the cetacean brain represent changes in function, e.g., loss of olfactory structures and enlargement of acoustic structures. Similar, convergent changes in function, along with their neuroanatomical correlates, are observed in several brains of unrelated clades, such as many bats and primates (Johnson et al., 1984; Johnson et al., 1994). In general, the cetacean brain possesses some common mammalian features in combination with specialized and highly unusual features, the function of which we have barely begun to understand.