Neuroanatomy of the killer whale (Orcinus orca) from magnetic resonance images

Abstract

This article presents the first series of MRI-based anatomically labeled sectioned images of the brain of the killer whale (Orcinus orca). Magnetic resonance images of the brain of an adult killer whale were acquired in the coronal and axial planes. The gross morphology of the killer whale brain is comparable in some respects to that of other odontocete brains, including the unusual spatial arrangement of midbrain structures. There are also intriguing differences. Cerebral hemispheres appear extremely convoluted and, in contrast to smaller cetacean species, the killer whale brain possesses an exceptional degree of cortical elaboration in the insular cortex, temporal operculum, and the cortical limbic lobe. The functional and evolutionary implications of these features are discussed. © 2004 Wiley-Liss, Inc. Key words: killer whale; Orcinus orca; delphinid, cetacea; brain; MRICompared with other mammalian brains, the cetacean brain is, in many respects, highly unusual. Morgane et al. (1980: p. 105) state 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." As there is a 55-60 million year divergence between cetaceans and the phylogenetically closest group, the artiodactyls, odontocete brains represent a blend of early mammalian and uniquely derived features (Ridgway, 1986(Ridgway, , 1990Glezer et al., 1988;Manger et al., 1998). Differences between cetacean and other mammalian brains of similar size have been found in cytoarchitecture and histochemistry (Garey et al., 1985;Garey and Leuba, 1986;Glezer et al., , 1992aGlezer et al., , 1992bGlezer et al., , 1993Glezer et al., , 1998Hof et al., 1992Hof et al., , 1995Hof et al., , 1999Hof et al., , 2000, cortical surface configuration (Jacobs et al., 1979;Morgane et al., 1980;Haug, 1987), and subcortical structural morphology (Tarpley and Ridgway, 1994;Glezer et al., 1995aGlezer et al., , 1995b.The brains of a few cetacean species, particularly the bottlenose dolphin (Tursiops truncatus), have been studied relatively extensively. This is primarily due to the fact that bottlenose dolphins are popular in captivity and have been the focus of many long-term field studies. Therefore, much is known about their behavior, cognitive abilities, and social ecology. However, there is little neuroanatomical information on the brain of the largest Delphinid species, the killer whale (Orcinus orca), despite the fact that this species has

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“…Structures of the basal ganglia (such as the caudate nucleus and the putamen) were recognized (Figures 5B,6B,12B,and 13B). Unlike previous reports of odontocete MRI studies of formalin-fixed brains (Marino et al, 2001a;Marino et al, 2001c;Marino et al, 2004a;Marino et al, 2004b;Marino et al, 2003a;Marino et al, 2003b;Marino et al, 2001c), the hippocampus was located and was found to be quite small relative to the overall size of the brain ( Figures 7B, 8B, and 15B). This observation was similar to the findings on the bottlenose dolphin hippocampus observed by Jacobs et al (1979).…”

“…Two-dimensional magnetic resonance images of the subadult (CCSN05-084-La) also revealed distinguishing features of odontocete brains, as previously observed in other MRI studies of formalin-fixed toothed whale brains (Marino et al, 2001a;Marino et al, 2004a;Marino et al, 2004b;Marino et al, 2003a;Marino et al, 2003b;Marino et al, 2001c) (Figures 4-19). Telencephalon.…”

“…Presently, suitable methods do not exist. Magnetic resonance imaging (MRI), a common diagnostic tool in human medicine, has recently been used to study the comparative neuroanatomy of the beluga whale (Marino et al, 2001a), the fetal common dolphin (Delphinus delphis) (Marino et al, 2001b), the bottlenose dolphin (Marino et al, 2001c), the harbor porpoise (Phocoena phocoena) (Marino et al, 2003b), the dwarf sperm whale (Kogia simus) (Marino et al, 2003a), the spinner dolphin (Stenella longirostris orientalis) (Marino et al, 2004b), and the killer whale (Marino et al, 2004a). MR imaging offers a non-invasive and non-destructive method of acquiring a permanent archive of external and internal brain structure data.…”

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“…Therefore, the gyrification indices for these two odontocete species, 2.4 and 2.7, respectively, substantially exceed that of modern humans. Furthermore, a qualitative description of the killer whale (Orcinus orca) brain suggests a neocortical gyrification index even higher than in Tursiops and Delphinus (Marino et al, 2004b).…”

“…The reduction of the hippocampus and related structures in odontocetes is particularly striking in light of the fact that odontocetes possess robust memory and learning skills (Mercado et al, 1998(Mercado et al, , 1999 which, in other mammals, depend highly on the hippocampus. An interesting possibility is that some learning and memory functions were transferred from the reduced hippocampal formation to the extremely well-developed cortical limbic lobe (periarchicortical field above the corpus callosum and the entorhinal cortex) in odontocetes (Oelschlager and Oelschlager, 2002;Marino et al, 2003Marino et al, , 2004b. This hypothesis would account for the copious behavioral evidence for strong learning and memory skills in odontocetes (Herman, 2006).…”