Volumetric Neuroimaging of the Atlantic White-Sided Dolphin (Lagenorhynchus acutus) Brain from in situ Magnetic Resonance Images

Department of Biology, Woods Hole Oceanographic Institution, Woods Hole, MA, USA.
The Anatomical Record Advances in Integrative Anatomy and Evolutionary Biology (Impact Factor: 1.54). 03/2008; 291(3):263-82. DOI: 10.1002/ar.20654
Source: PubMed


The structure and development of the brain are extremely difficult to study in free-ranging marine mammals. Here, we report measurements of total white matter (WM), total gray matter (GM), cerebellum (WM and GM), hippocampus, and corpus callosum made from magnetic resonance (MR) images of fresh, postmortem brains of the Atlantic white-sided dolphin (Lagenorhynchus acutus) imaged in situ (i.e., the brain intact within the skull, with the head still attached to the body). WM:GM volume ratios of the entire brain increased from fetus to adult, illustrating the increase in myelination during ontogeny. The cerebellum (WM and GM combined) of subadult and adult dolphins ranged from 13.8 to 15.0% of total brain size, much larger than that of primates. The corpus callosum mid-sagittal area to brain mass ratios (CCA/BM) ranged from 0.088 to 0.137, smaller than in most mammals. Dolphin hippocampal volumes were smaller than those of carnivores, ungulates, and humans, consistent with previous qualitative results assessed from histological studies of the bottlenose dolphin brain. These quantitative measurements of white matter, gray matter, corpus callosum, and hippocampus are the first to be determined from MR images for any cetacean species. We establish here an approach for accurately determining the size of brain structures from in situ MR images of stranded, dead dolphins. This approach can be used not only for comparative and developmental studies of marine mammal brains but also for investigation of the potential impacts of natural and anthropogenic chemicals on neurodevelopment and neuroanatomy in exposed marine mammal populations.

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    • "Some of the proposed memory functions for this lobule overlap with those of the hippocampus, a structure that is unusually small in the bottlenose dolphin (Jacobs et al., 1979). The fact that dolphins excel at memory and spatial tasks while exhibiting reduced hippocampal structures has led some to suggest that these processes occur elsewhere in the brain (Marino, 2004; Montie et al., 2008). It is tempting to speculate that lobule VI may contribute to such functions. "
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    ABSTRACT: Neuroanatomical research into the brain of the bottlenose dolphin (Tursiops truncatus) has revealed striking similarities with the human brain in terms of size and complexity. However, the dolphin brain also contains unique allometric relationships. When compared to the human brain, the dolphin cerebellum is noticeably larger. Upon closer examination, the lobule composition of the cerebellum is distinct between the two species. In this study, we used magnetic resonance imaging to analyze cerebellar anatomy in the bottlenose dolphin and measure the volume of the separate cerebellar lobules in the bottlenose dolphin and human. Lobule identification was assisted by three-dimensional modeling. We find that lobules VI, VIIb, VIII, and IX are the largest lobules of the bottlenose dolphin cerebellum, while the anterior lobe (I-V), crus I, crus II, and the flocculonodular lobe are smaller. Different lobule sizes may have functional implications. Auditory-associated lobules VIIb, VIII, IX are likely large in the bottlenose dolphin due to echolocation abilities. Our study provides quantitative information on cerebellar anatomy that substantiates previous reports based on gross observation and subjective analysis. This study is part of a continuing effort toward providing explicit descriptions of cetacean neuroanatomy to support the interpretation of behavioral studies on cetacean cognition. Anat Rec, 2013. © 2013 Wiley Periodicals, Inc.
    The Anatomical Record Advances in Integrative Anatomy and Evolutionary Biology 08/2013; 296(8). DOI:10.1002/ar.22726 · 1.54 Impact Factor
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    • "Three-dimensional (3D) models of brain structures constructed from MRI scans can provide a valuable tool to examine spatial relationships among brain structures. In fact, volumetric neuroimaging and 3D modeling have illustrated their powerful utility in studying the brains of the Atlantic white-sided dolphin and California sea lion (Montie et al. 2008, 2009). Traditionally, MRI has been used as a tool in diagnosing causes of neurological disease. "
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    ABSTRACT: Our goal in this study was to compare magnetic resonance images and volumes of brain structures obtained alive versus postmortem of California sea lions Zalophus californianus exhibiting clinical signs of domoic acid (DA) toxicosis and those exhibiting normal behavior. Proton density-(PD) and T2-weighted images of postmortem-intact brains, up to 48 h after death, provided similar quality to images acquired from live sea lions. Volumes of gray matter (GM) and white matter (WM) of the cerebral hemispheres were similar to volumes calculated from images acquired when the sea lions were alive. However, cerebrospinal fluid (CSF) volumes decreased due to leakage. Hippocampal volumes from postmortem-intact images were useful for diagnosing unilateral and bilateral atrophy, consequences of DA toxicosis. These volumes were similar to the volumes in the live sea lion studies, up to 48 h postmortem. Imaging formalin-fixed brains provided some information on brain structure; however, images of the hippocampus and surrounding structures were of poorer quality compared to the images acquired alive and postmortem-intact. Despite these issues, volumes of cerebral GM and WM, as well as the hippocampus, were similar to volumes calculated from images of live sea lions and sufficient to diagnose hippocampal atrophy. Thus, postmortem MRI scanning (either intact or formalin-fixed) with volumetric analysis can be used to investigate the acute, chronic and possible developmental effects of DA on the brain of California sea lions.
    Diseases of Aquatic Organisms 09/2010; 91(3):243-56. DOI:10.3354/dao02259 · 1.75 Impact Factor
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    • "Neuroimaging studies involving post-mortem MRI acquisition of cetacean brain structures may help to answer some of these questions. Cetacean brain MRI studies have been conducted and a growing database will assist in providing reference images for comparison with suspected domoic acid intoxications in these marine mammals [173] [174]. Such a database would be particularly useful if it could include findings from whales and dolphins known to have been unexposed to DA, including through gestation, though it is difficult to envisage how such animals could be identified other than in captive animals, and then only if their food sources had been screened for domoic acid – not a trivial exercise. "
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    ABSTRACT: Temporal lobe epilepsy with hippocampal sclerosis (TLE-HS) is one of the more common forms of chronic epilepsy. Its aetiology is unknown, though an early developmental insult is thought by some to be an important trigger. There is not a strong genetic predisposition; gene-environment interactions are more significant considerations. Environmental risk factors for TLE-HS are under-researched. Domoic acid (DA) is an environmental neurotoxin of algal origin that can contaminate marine food webs. DA can cross the placenta, is significantly more toxic to the developing brain compared to the adult brain, and has affected humans and marine wildlife through mass poisonings. DA coincidentally has a decades-long history of use as a chemical model of temporal lobe epilepsy, along with its close structural analogue kainic acid (also of algal origin). The principal hypothesis presented here is that dietary exposure to doses of DA that are sub-clinical in pregnant women may be sufficient to damage the foetal hippocampus and initiate epileptogenesis. The hypothesis could be tested both experimentally by in vivo proof-of-concept animal studies that expand on current knowledge of prenatal susceptibility to DA neurotoxicity, and by epidemiological investigations directed towards dietary exposure to marine food products. If only a small proportion of the attributable risk for TLE-HS is found to be due to gestational exposure to DA, the public health implications would still be of great significance, as this would represent a potentially preventable exposure. Other potent neurotoxins are produced by marine microalgae and freshwater cyanobacteria. These structurally and mechanistically diverse toxins can also contaminate water supplies, seafood and shellfish. Several operate by modulating ion channels, so may also be of interest to epilepsy researchers. DA is also the subject of preliminary scrutiny in strandings involving odontocete cetaceans. The implications of such work are discussed here.
    Medical Hypotheses 11/2009; 74(3):466-81. DOI:10.1016/j.mehy.2009.10.018 · 1.07 Impact Factor
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