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Copyright 2004 by the International Society for Comparative Psychology
Cetacean Brain Evolution: Multiplication Generates Complexity
Lori Marino Emory University, U.S.A.
Over the past 55-60 million years cetacean (dolphin, whale, and porpoise) brains have become hyperexpanded so that modern cetacean encephalization levels are second only to modern humans. At the same time, brain expansion proceeded along very different lines than in other large-brained mammals so that substantial differences between modern cetacean brains and other mammalian brains exist at every level of brain organization. Perhaps the most profound difference between cetacean and other mammalian brains is in the architecture of the neocortex. Cetaceans possess a unique underlying neocortical organizational scheme that is particularly intriguing in light of the fact that cetaceans exhibit cognitive and behavioral complexity at least on a par with our closest phylogenetic relatives, the great apes. The neurobiological complexity underlying these cognitive capacities may involve the extreme multiplication of vertical structural units in the cetacean neocortex.
The origin and evolutionary history of cetaceans (dolphins, whales, and porpoises) has been the topic of vigorous scientific discussion for decades. The mammalian order Cetacea comprises one extinct and two living suborders. The Eocene suborder, Archaeoceti, contained approximately thirty (described) genera (Thewissen, 1998) and survived from the early Eocene, around 53 million years ago (mya) until the late Eocene, around 38 mya (Bajpai & Gingerich, 1998; Barnes et al., 1985; Uhen, 1998). Of the modern suborders (i.e., Neoceti), Mysticeti (comprising eleven living species of baleen whales) are first found in the fossil record in the latest Eocene (Mitchell, 1989), and Odontoceti (comprising sixty-six living species of toothed whales, dolphins, and porpoises) are first found in the fossil record in the early Oligocene (Barnes et al., 1985). Longstanding molecular evidence (Gatesy, 1998; Milinkovitch et al., 1998; Nikaido et al., 1996; Shimamura et al., 1997) and more recent morphological evidence (Geisler & Uhen, in press; Gingerich et al., 2001; Thewissen et al., 2001) confirm a phylogenetic link between cetaceans and artiodactyls (even-toed ungulates). Figure 1 shows the phylogenetic relationships among cetaceans, artiodactyls, and primates. Along with the major transformations in body form and physiology that occurred during cetacean evolution a less obvious but equally significant transformation occurred in brain size and brain morphology. Evidence for this outcome comes from both examination of fossil endocranial morphology and comparisons of modern cetacean neuroanatomy with other mammals. Studies of Fossil Endocranial Size and Morphology Several estimates of cetacean brain mass from endocranial casts have provided strong evidence that the first suborder of cetaceans, the archaeocetes,
Correspondence concerning this article should be addressed to Lori Marino, Neuroscience and Behavioral Biology Program, Psychology Building, Emory University, Atlanta, Georgia 30322, U.S.A. (email@example.com).
2 g. Cetaceans became highly encephalized throughout the course of their evolution. 1936. 2000a). 1955. 1955. Kellogg... and imprints of cranial nerves (Czyzewska.. Marples. Figure 1.49 (Marino. Gingerich. Dorudon atrox and Zygorhiza kochii are 944. 1936). EQ measures how much larger or smaller a species’ total brain size is from what would be expected solely on the basis of brain-body allometry. EQ values are essentially residuals from the regression line with values standardized as one. 1988. Although estimates of brain size indicate that some archaeocetes had very large brains. 2000a). than many of their modern counterparts (Breathnach. 1998) and significantly smaller. 1936. 1993) the relative size of major structures (Czyzewska. lobular morphology (Czyzewska. The absolute value of EQ varies with the reference group (Harvey & Krebs. and greater than one for relative brain sizes that are average.3 g and 738. The estimated adult brain weights for two relatively well-known archaeocete species. below average. Edinger.25 to 0. The most reliable brain volume estimates for archaeocetes from the limited sample of fossil cetacean endocasts and endocranial volumes suggest an approximate range from 485 cc for Saghacetus osiris to 2620 cc for the large Basilosaurus isis (Gingerich. Kellogg. including cerebral asymmetry (Stefaniak. 1988. 1955. Marino et al. 1955. Kellogg. Gingerich. 1993). less than one. and above average. also with regard to body size. 1993). 2000a. archaeocetes possessed below-average EQ values ranging from 0. 1955. EQ is a measure of observed brain size relative to expected brain size derived from a regression of brain weight on body weight for a sample of species. 1990). Edinger. Dart. The EQ values reported in this paper are based on the parameters of a regression equation derived by Jerison (1973). 1998). Edinger. 2002. Stefaniak. Various morphological features of fossil cetacean endocasts have also been noted in the literature. Marino et al. 1998. 1949). respectively. These kinds .-2- possessed brains that were quite similar in relative size to that of their purported ancestors (Edinger. respectively (Marino et al. 1923. Stefaniak. 1988. A useful way to represent the level of encephalization obtained by a species or taxonomic group is with an Encephalization Quotient (EQ). Phylogenetic relationships among cetaceans artiodactyls and primates.
reveal that there were significant morphological changes in cetacean brains during their evolution. This pattern of elaboration gives the modern cetacean brain a globular shape. my colleagues and I have been able to describe and quantify substantial evolutionary changes in cetacean brain size and morphology (see Marino et al. There is a range of brain weights and encephalization levels among modern cetaceans. Comparative Studies of Brain Size Among Modern Groups Comparative studies of modern cetaceans provide data for inferring the past through comparisons of modern species. Also. Over time. these analyses reveal that there was a considerable increase in encephalization after the transition from archaeocetes to several modern forms. Ongoing analyses of these brain size and morphology data. Modern odontocete adult brain weights range from 221 g for the Franciscana dolphin (Pontoporia blainvillei) to 8028 g for the sperm whale .. cetacean cerebral hemispheres became considerably larger and more complexly convoluted. however. and occipital regions with relatively less elaboration of frontal areas (Figure 2b). Later cetacean brains became highly elaborated and considerably different from the brain of Archaeoceti. Cerebral enlargement. when interpreted cautiously. Archaeocete brains possessed relatively small cerebral hemispheres. as there is in any taxonomic group. temporal. for a review of methods). mainly took place in the parietal. were vertically flattened and elongated in overall shape. 2003a. when registered to our best phylogenetic reconstructions. Illustrations of the brain of an archaeocete from a natural endocast (a) and the brain of a modern dolphin (b) with major structures labeled. rostrally. and ended. olfactory structures regressed and the entire brain became foreshortened antero-posteriorly while maintaining prominent mesencephalic and pontine flexures. in well-developed olfactory peduncles (Figure 2a). Preliminarily.-3- of observations. Figure 2. In a recently completed large-scale study of fossil cetacean endocranial morphology using Computed Tomography (CT)-based data. will provide the most comprehensive and quantitatively rigorous analyses of cetacean brain evolution to date.
24 1.58 to 4. EQs of modern nonhuman anthropoid primates range from 1.78 1.01 2. 1998).55 4. is the only known odontocete with an EQ considerably below 1 and is an example of a species with a disproportionately large body for which the measure of EQ is not particularly meaningful. The EQ of modern humans is 7.97 Mesoplodon europaeus (Gervais’ Beaked Whale) 2.56 (Table 1).17 2.14 4.58.0 (Marino. 1995.39 3.76 2.21 with a mean of 2. Marino.56 In comparison.02 to 3.15 3.56 with a mean of 2.11 Mesoplodon densirostris (Blainville’s Beaked Whale) 1. Marino. 1998).63 2.26 4.51 1.54 4.-4- (Physeter macrocephalus. 2002).39 Ziphius cavirostris (Cuvier’s Beaked Whale) 0.) Table 1 Known EQ Values for Modern Odontocete Species.57 4. The modern odontocete values reveal that . (The sperm whale (Physeter macrocephalus).55 1.67 3. EQs are based on the formula derived by Jerison (1973). 0. The EQs of modern odontocetes range from 0. 1995.24 2.58 1. with an EQ of 0.0 (Marino. ____________________________________________________________________ Species EQ ___________________________________________________________ Family Ziphiidae (Beaked and Bottlenose whales) Mesoplodon mirus (True’s Beaked Whale) 1.92 Family Physeteridae (Sperm whales) Physeter macrocephalus (Sperm Whale) Kogia breviceps (Pygmy Sperm Whale) Kogia simus (Dwarf Sperm Whale) Family Monodontidae (Beluga and Narwhal) Delphinapterus leucas (Beluga or White Whale) Monodon monoceros (Narwhal) Family Platanistidae (Freshwater dolphins) Lipotes vexillifer (Chinese River Dolphin) Inia geoffrensis (Amazon River Dolphin) Platanista gangetica (Ganges River Dolphin) Pontoporia blainvillei (Franciscana Dolphin) Family Phocoenidae (Porpoises) Phocoena phocoena (Harbor Porpoise) Phocoenoides dalli (Dall’s Porpoise) Family Delphinidae (Oceanic Dolphins) Tursiops truncatus (Bottlenose Dolphin) Lagenorhynchus obliquidens (Pacific White-sided Dolphin) Delphinus delphis (Common Dolphin) Grampus griseus (Risso’s Dolphin) Globicephala melaena (Long-finned Pilot Whale) Stenella longirostris (Spinner Dolphin) Orcinus orca (Killer Whale) Sotalia fluviatilis (Tucuxi Dolphin) Note.
0. and Risso’s dolphin (Grampus griseus) with EQs of 4. 4.. For instance. The preservation of the amygdala is obviously due to the maintenance of substantial nonolfactory sources of input to this structure. Therefore. the adult blue whale (Balaenoptera musculus) has been measured at approximately 7085 g. and mammillary bodies are all unusually small (Jacobs et al. However. as in humans. Studies of fossils can only offer information on surface morphology and size. It is not possible to directly determine how developed the limbic system was in archaeocetes because these internal structures are not visible on endocasts. Morgane et al. Comparative studies of modern species are. This information can inform us about how the relative importance of various functions changed throughout cetacean evolution. respectively (Marino. One of the more obvious morphological changes that occurred in cetacean brain evolution that is also highly detectable in fossils is the regression of olfactory system structures. 2002). even in mysticetes the olfactory system has clearly regressed substantially. Nevertheless. In addition to examining total brain size it is important to identify which specific structures and systems became enlarged and. . the Pacific white-sided dolphin (Lagenorhynchus obliquidens).-5- some odontocetes have achieved a level of encephalization second only to modern humans and significantly higher than any of the modern nonhuman anthropoid primates. the limbic system in modern (and particularly odontocete) cetaceans. These include the Tucuxi dolphin (Sotalia fluviatilis). 1955). and 4. 2002). the common dolphin (Delphinus delphis). Furthermore. related to reduction in olfactory function. However. The high-end of the EQ range in odontocetes is occupied by several delphinid species with EQs above 4. This condition is. Marino et al. Oelschlager and Oelschlager. 1980. In addition to olfactory structures. the EQs of mysticetes are all substantially below one (Marino 2002) because mysticetes have undergone extraordinary increases in body size without allometric increases in brain size. a thin olfactory peduncle. In modern adult odontocetes olfactory structures are completely missing except for the infrequent appearance of a short olfactory peduncle in adult sperm whales (Physeter macrocephalus) and northern bottlenosed whales (Hyperoodon ampullatus. the large size. the amygdala is large and welldeveloped in cetaceans. 2001) that regress completely by birth. 2002).14. 4. critical for obtaining a level of morphological detail not attainable from fossil endocasts. in all likelihood. the brain of the largest cetacean.55. Fetal odontocetes possess small olfactory structures (Buhl & Oelschlager.26.. Adult mysticetes have maintained small olfactory bulbs. 2002) The brains of modern mysticetes are also very large..01. EQ is not particularly meaningful in mysticetes because the general rules about brain and body relationships that underlie EQ do not hold for this group. Olfactory peduncles and bulbs were visibly well-developed in archaeocetes (Edinger. high cortical convolutional index and highly derived morphology of mysticete brains establish that these brains have indeed undergone substantial enlargement and elaboration during the course of their evolution (Oelschlager & Oelschlager. therefore. regressed during the course of cetacean evolution. the bottlenose dolphin (Tursiops truncatus). 2002). 4. is exiguous compared with terrestrial mammals. Specifically. 1988. fornix. the hippocampus (archicortex). and an olfactory tubercle (Oelschlager & Oelschlager.56. Oelschlager & Oelschlager. 1979.
This is a peculiar . This juxtaposition of a vastly reduced archicortex and a highly elaborated periarchicortical/entorhinal zone leads to intriguing questions about whether there was a transfer of hippocampuslike functions from the olfactory-based hippocampal domain to other cortical regions. As others have suggested.. Another notably undersized structure in cetacean brains is the corpus callosum. It is also noteworthy that in cetaceans. Therefore. the relatively weaker interhemispheric connections in cetacean brains may facilitate the unihemispheric sleep patterns exhibited by cetaceans. In odontocetes the inferior colliculus. 2003). particularly in the pulvinar region). has been electrophysiologically mapped in cetaceans and is located on the vertex of the hemisphere in the suprasylvian gyrus immediately lateral to the visual cortex. as well as in other large-brained mammals. This feature of cetacean brains has been given considerable attention in the literature and can be summarized as follows. 1994). The diameter of the vestibulocochlear nerve in cetaceans is prodigious and. The human and killer whale (Orca orcinus) corpora callosa. which receives afferent thalamic projections. An interesting corollary feature to the small limbic system is the extremely well-developed cortical limbic lobe (periarchicortical field above the corpus callosum and the entorhinal cortex) in cetaceans (Marino et al. An interesting feature of the dolphin brain is the adjacency among the sensory cortical projection regions. Tarpley and Ridgway (1994) found that corpus callosum midsagittal area in delphinids was considerably smaller in relation to brain mass than in other mammals and that dolphins with larger brains possessed relatively smaller corpora callosa. the cetacean brain is characterized by a hyperproliferation of tissue in other regions. 1978). projects to the large medial geniculate nucleus in the thalamus (which is massive itself. 2003b. larger brains (in larger species) maintain less interhemispheric connectivity. However. and inferior colliculi are all greatly enlarged in comparison with terrestrial mammals. Among those structures that are highly elaborated in cetacean brains are those related to the processing of auditory information. 1986). possess the same crosssectional area despite the fact that the killer whale brain is over five times the weight of a human brain (Ridgway. The ventral cochlear nucleus. lateral lemniscus. for example. Primary auditory cortex. the main body of connectivity between the two hemispheres. the relatively small size of the corpus callosum is not compensated for by enlargement of other commissures (Tarpley & Ridgway.. Oelschlager & Oelschlager. Secondary auditory cortex lies lateral to the primary auditory field in the medial ectosylvian gyrus (Supin et al. we cannot be absolutely certain that the small size of limbic structures in modern cetaceans is due to regression from a well-developed condition or a maintenance of initial structures without elaboration relative to the rest of the brain.-6- Therefore. Despite the regression of several olfactory and limbic features. including periarchicortical and entorhinal regions. although the exact proportions of auditory to vestibular fibers are not agreed upon. 2002). 2002). which can be four times the size of the superior colliculus (Marino et al. it is composed of mainly auditory components (Oelschlager & Oelschlager. trapezoid bodies.. the fact that archaeocetes had well-developed olfactory peduncles and bulbs strongly suggests that archaeocete limbic systems were well developed and that the condition in modern cetaceans is the result of regression of the limbic system over time.
1936). The high degree of cortical gyrification in many cetacean brains and resulting neocortical surface area of approximately 3745 cm2 is unsurpassed among mammals. from both the point of view of total brain size and neocorticalization cetacean brains are highly elaborated. 1984). 1971. Jansen & Jansen. despite variation across species. However. The telencephalon is arranged into three concentric tiers of tissue comprising limbic. is relatively larger than in humans and other primates (Marino et al. elaborated at the expense of visual functions (Ridgway. including echolocatory. There is evidence from natural endocasts that archaeocete cerebella were large in proportion to the rest of the brain (Edinger. 1969. The cetacean brain has apparently exploited a highly conserved neocortical organizational scheme to evolve an extremely elaborated brain capable . What is apparent is that auditory functions were not. medulla oblongata. abilities. Most notable among the regions of enlargement in the cetacean brain is the neocortex. Several brainstem nuclei are extremely large (Oelschlager & Oelschlager.) Another augmented region of the cetacean brain is the hindbrain. 1955. 1969. (The only examples of reduced visual function in cetaceans are found among the Platanistidae. The regions of the hemispheres that are among the most hypertrophied in odontocetes are the paraflocculus and paramedian lobules (Breathnach. Although the cerebellum of early cetaceans may have been well developed. This combination of extreme surface area and narrow cortical width in cetaceans betrays a unique underlying neocortical organizational scheme that has been the focal point of longstanding and unresolved controversy about the computational capacities of the dolphin brain. can be identified as distinctly cetacean. It is to this discussion that we turn next. 1960. 1969. there is a certain combination of shared characteristics that. Therefore. The cetacean cerebellum contains two voluminous highly convoluted hemispheres and a relatively narrow vermis.0 mm thick human neocortex (Haug. 1984). Ridgway & Brownson. 2002) and the cerebellum.-7- arrangement for brains as large as those of cetaceans. and supralimbic regions. All species within this family appear to have well-developed auditory.3 and 1. the freshwater dolphins. and cerebellum. the cetacean neocortex is relatively thin with a width between 1.. paralimbic. Ridgway. However. in any obvious way. 1990). 2000b). including pons. 1990). The extent of neocortical areas involved in more integrated levels of auditory processing is not known but there is an extensive hemispheric field of “association” cortex that remains unmapped. Comparative Studies of Brain Organization and Morphology in Modern Groups The study of cetacean neocortex has been limited to a few species and a subset of neocortical areas. Ridgway & Brownson. as compared with the 3. Kellogg. Kesarev.8 mm. Elias & Schwartz. which averages about 15% of total brain size in several odontocete species. It is clear that the elaboration of the auditory system in cetaceans occurred after they adopted an aquatic existence but answers to questions of when and how auditory elaboration occurred in cetacean evolution are largely unknown. more comprehensive morphometric analyses are needed to determine just how extensively the cerebellum changed in relative size during cetacean evolution. including humans (2275 cm2.
cetacean sensory neocortex possesses five layers (but see below). 1988). these zones are all clustered in the rostral region of the brain and. This feature is not found in insectivores. artiodactyls (Glezer et al. The strong pyramidalization of layer II is also a key feature of cetacean neocortex (Morgane et al. Moreover. respectively. Morgane et al. exhibit an organizational pattern known as cortical adjacency. and posterior parietal regions. Regarding lamination patterns. Apart from the question of whether modern insectivores are “primitive. In general and not surprisingly.e. the visual and auditory areas occupy the lateral convexity cortex. is the expansive field of nonprojection or “association” cortex that apparently occupies the remainder of the large hemispheres.. The large cetacean neocortex represents a striking alternative to the forms of elaboration one sees in other large brains.. Nonprojection regions. 1988). the cetacean brain is uniquely valuable for revealing the wide range of structural and functional possibilities that the mammalian neocortex can express... (i. 1990). 1999... One of the most salient features of cetacean neocortex is the general lack of granularity.-8- of complex cognitive processing. the entirety of thalamocortical afferents feed into the thick layer I and through the extraverted neurons of layer II to deeper levels (Glezer et al. and the visual and auditory fields. the projection regions are separated by intervening nonprojection cortex that cause the auditory and visual projection regions to occupy temporal and occipital areas. the chemoarchitecture of the cetacean neocortex is dissimilar in many respects to that of primates and very similar to that of their closest phylogenetic relatives.. as a result. In primates. Furthermore. As mentioned earlier.” this observation is based on a superficial similarity between the cetacean and insectivore pattern. 1988). the projection zones lie adjacent to one another with no cortex intervening between them. the functionally distinct somatosensory and motor regions. Some investigators have remarked that the cetacean pattern of projection zones is reminiscent of the positions of projection zones in mammals considered to be less derived. 1988. 1986). It is characterized by a very thick layer I that contains apical dendrites of extraverted pyramidal cells from a highly accentuated layer II (Glezer et al. The striking feature of the arrangement of projection zones in cetacean brains. This arrangement is dissimilar to that found in primates and other large mammals. barely identifiable) granular layer IV. “association” cortex). The maintenance of a conservative neocortical theme is thought to be due to the early divergence of cetaceans from other mammal lineages.. (1988) also recognize. Hof et al. occipital. (1988) identified two types of visual cortex in the bottlenose dolphin. in cetaceans. Layer I also possesses large calretinincontaining neurons (Hof et al. For this reason. which is due primarily to the absence of (or. 1999). at best. It has been suggested that. The major features of cetacean neocortical architecture that have been the focus of much attention are the following. That is.. such as those of primates. Heterolaminar cortex appears to contain a very . there is evidence from the highly developed nature of the thalamic pulvinar in cetaceans that the nonprojection or integrative neocortical regions in cetaceans are vast (Morgane et al. The topography of the primary and secondary neocortical projection zones in cetaceans is strikingly different from many other large mammals. Morgane et al. 1988. which Glezer et al. such as basal Insectivora (Glezer et al.. occupies the substantial field of surrounding tissue in the temporal.. Morgane et al. for instance. 1999).
Also. however. Stenella coeruleoalba. Despite the importance of the evolutionary status of layer IV in cetacean neocortex the nature of this condition in cetaceans is far from settled and there still remain many critical unanswered questions about this feature in cetacean neocortex. In cetaceans the majority of afferents appear to go through the very thick layer I to synapse en passage on extraverted neurons of layer II (Glezer et al.. albeit indirectly. 1988.. (1985) observed a rudimentary granular layer IV in the visual cortex of an 18-day old bottlenose dolphin. that is. 1995.-9- meager layer IV. to the question of whether the lack or scarceness of layer IV granular cells in cetacean neocortex is primary (conserved). Kesarev et al. The authors noted that these columns were more highly conserved than those in other mammals.. 1990) and chemoarchitectural level (Hof et al. Granularity in this layer was scarcer but still detectable in a 3-year old dolphin. specifically. 1988).. Despite the relative homogeneity of cetacean neocortex and. 1988. Garey et al. 1986). In addition to the above characteristics. the overall dysgranularity of cetacean neocortex is one of the most striking and primary features signifying the conservative nature of cetacean neocortex. and. several researchers have remarked on the relative uniformity of the cetacean neocortex on both a cytoarchitectural (Morgane et al.. The general dysgranularity of the cetacean neocortex is viewed as evidence that cetaceans diverged from the mammalian line prior to the neocortical granularization trend evinced in other mammals. apparently. 1990). 1985. 1990). the general lack of layer IV in cetaceans has important implications for afferentation patterns. the cetacean neocortex has expanded on a highly conserved theme that almost entirely misses a stage of cortical evolution found in many other mammals. Some investigators view the segregation of afferents to layer IV and layer I to be a later evolutionary development than the pattern evinced in cetacean neocortex (Kesarev et al. In homolaminar cortex. Furthermore. due to cetaceans not having attained a granular stage of neocortical evolution.. Also. or. “evo-devo”) studies of cetacean neocortex are critically needed for determining the evolutionary status of layer IV and other characteristic features of cetacean neocortex. This finding speaks. according to this view. (1988. Morgane et al. absent in an adult. that is. layer IV is entirely absent. For instance. 1975. there is adequate evidence for another level of organization in the cetacean neocortex that depends on integration of nonhorizontal modules. Glezer et al. A small portion of afferents go to layers III and V as well (Garey & Revishchin. in cetaceans.. Morgane et al. evolutionary-developmental (or. Morgane et al. the presence of numerous “transitional” types of neurons has been noted (Garey et al. Revishchin & Garey. in a study of insular . 1986. due to cetaceans losing layer IV (and re-organizing thalamocortical inputs) throughout their evolution. 2000). 1989. To most investigators. 1977. Therefore. layer IV may be present in young animals and subsequently regress during maturation. In primates and other mammals some afferent connections come through layer I to dendritic connections from layer II neurons while other specialized thalamocortical afferents synapse directly on layer IV... Morgane et al. 1999. 1990) reported the presence of cytoarchitectonic vertically oriented columns in both homolaminar and heterolaminar visual cortex of the striped dolphin. Although ontogeneticdevelopmental patterns are not direct windows onto evolutionary processes. there is some evidence suggesting that.. secondary (derived). relatively weak lamination patterns.
Glezer et al. In the case of cetaceans. the level of nonlaminar connectivity in the neocortex. expected on the basis of general levels of encephalization and neocortical elaboration. such a cortex is of special interest in that the total number of functional cortical modules may be very great but the fundamental organization is one of relative simplicity compared to those of more progressive terrestrial mammalian forms. Morgane et al. cetacean brains are highly derived and elaborated overall. However. more conservatively organized brains such as seen in basal insectivores and bats. Furthermore. Therefore. brain complexity is revealed by the cognitive and behavioral complexity of an organism. (1999) reported the prevalence of calretinin and calbindin-immunoreactive neurons over parvalbuminimmunoreactive neurons in dolphin neocortex and noted that. Manger et al. This level of cognitive convergence might be unexpected on the basis of their deep phylogenetic divergence. on the other hand. use the term progressive to refer descriptively to the kind of neocortex that primates possess and it would be a mistake to interpret their remark as implying that the cetacean brain is more primitive or simpler than primate brains. adaptation to very different physical environments. in many cases considerably larger than in the human brain. the cognitive-behavioral literature demonstrates that cetacean intelligence is on a par with that of many primates. consequently. as mentioned before. represents the most highly developed version of a particular kind of expansion that involved an enormous multiplication of these modules and. Cetacean Brains and Cognition Evidence points to a striking degree of convergence between primates and cetaceans in terms of the complexity. . Computationally. including primates. given the role of calretinin and calbindin neurons in inhibiting intracolumnar signals. as in other mammals. The cetacean brain. the level of encephalization in many cetaceans is exceeded only by modern humans and the anatomical evidence demonstrates that. in the final analysis. This extreme expansion of the quantity of uniform units and connections in the cetacean neocortex is a special way of achieving computational complexity that represents an alternative to the evolutionary route taken by other large mammals. but one in which the fundamental cortical structural plan is similar to that of smaller. (1998) reported distinct cellular clumps or modular subdivisions that are different from the vertical columns noted by Morgane and his colleagues. the preponderance of vertical flow of inhibition along the columnar axis over laminar or horizontal flow is a chemoarchitectural indicator of strong verticality in cetacean neocortex.-10- cortex in the bottlenose dolphin. despite building on an apparently conservative laminar theme. On the contrary. diversity. non-laminar modularity imposes another level of complexity on the cetacean neocortex. and flexibility of cognition and behavior across many domains. (1990) remarked on the intriguing nature of the cetacean neocortex with the following: “ …we are dealing with a very unique situation of a massive cerebral cortex.” Here Morgane et al. however. and divergent neuroanatomical evolution but.
Richards et al. thoughts and feelings.. 1998. the beluga whale.e. 1997. These are a bonobo (Savage-Rumbaugh et al. Competence in comprehension of symbolic references and rule-based sequences appears to be limited to great apes. capacities within the context of these studies. for a review of this literature) but not monkeys or lesser apes (Anderson & Roeder. Tursiops truncatus. Shaffer & Renner. 1988). Hyatt. 1985. 1998). Furthermore. as in any taxonomic group. human devised) communication system based upon symbols and rules. 2002a. both dolphins in our study used a mirror to investigate parts of their bodies that were marked (Figure 3). Bayart & Anderson. 1986). and a tiny subset of other odontocete species. Herman. 1976). 1984. Another exceedingly rare capacity demonstrated by bottlenose dolphins is mirror self-recognition. Bottlenose dolphins have also demonstrated extensive capacities in the ability to understand an artificial (i. Reiss & McCowan. if not definitive. However. 1999). 2000. Xitco. which is a component of the more general capacity for self-awareness. 1994). innovation (Braslau-Schneck. These capacities appear to be at a level typically only demonstrated by great apes and humans. Delphinapterus leucas. the more extensive literature on behavioral ecological and social complexity in natural populations from a wider range of odontocetes and mysticetes is congruent with indications of a high-level intelligence from the experimental literature. physical make-up. Up until recently. it is interesting that only these very few species have been able to meaningfully participate in such studies and also demonstrate compelling. a common chimpanzee (Premack. Reiss and Marino (2001) reported the first conclusive evidence of mirror self-recognition in a nonprimate species. and an African Grey Parrot (Pepperberg. 1994. In a series of controlled variations of the procedures used with primates. Only three species have demonstrated the capacity to understand that symbol or “word” order has meaning. 2002b). Therefore. vocal and behavioral mimicry (Braslau-Schneck. 1999). The fact that studies of comprehension of artificial communication systems can only be attempted with these very few species suggests that they all have converged toward a level of cognitive complexity that allows them to understand a simple symbolic and rulebased system of communication. Bottlenose dolphins have demonstrated sophisticated capacities in the realms of memory (Mercado III et al. the sizeable literature on the bottlenose dolphin can serve as an indication or “existence proof” of cognitive and behavioral abilities in cetaceans in general. and abstract rule comprehension and formation (Herman et al.. 1994.. mirror self-recognition had been demonstrated only in humans and great apes (see Povinelli et al. 1998. and bottlenose dolphins (Herman.. bottlenose dolphins. 1993. one should expect cognitive and behavioral differences across cetacean species. Orcinus orca. Self-awareness refers to the ability to think about one’s own behavior. .. 1989. and. Mercado III. Although the comparability of primate and cetacean (as well as avian) studies of artificial communication system comprehension must be carefully considered. 1993)..-11- It should be noted that an overwhelming majority of experimental research on cognition and behavior in cetaceans has focused on the bottlenose dolphin. with a relatively small proportion of studies on other odontocetes such as the killer whale. Suarez & Gallup. the bottlenose dolphin.
Many investigators have hypothesized that the cortical circuitry of the prefrontal cortex in humans and great apes is the necessary neuroanatomical substrate for self-recognition and other dimensions of self-awareness (Keenan et al... Stuss et al. Mercado et al. 1999).-12- These findings revealed. once again. the importance of examining the cognitive and behavioral capacities of cetaceans and primates within the context of their respective neuroanatomies is that it affords the opportunity to resolve questions . Bottlenose dolphins also show related capacities in the domains of awareness of one’s own body parts and behavior (Herman et al.. that dolphins possess cognitively complex capacities that are found in only a small subset of primates with highly elaborated brains. Furthermore. 1998. Miller et al. 2001. Photograph by D. Reiss. Figure 3. the excellent performance of dolphins on tasks that rely on sophisticated memory abilities leaves open the interesting question of how cetaceans possess such high-level memory capacities while possessing a highly reduced hippocampus. This finding challenges the view that self-awareness is specific to primate frontal lobe architecture and suggests that self-awareness could be more of a holistic property of brains of any species that achieve a certain threshold of elaboration regardless of how that elaboration occurred. The Reiss and Marino findings show that dolphins are capable of mirror self-recognition despite possession of unelaborated frontal lobes (or homologous frontal lobe structures) and an overall cortical organizational pattern that is very different from that of primates.. 2001). In general. Bottlenose dolphins use mirrors to investigate marks on their bodies. 2001. 2000..
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