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The size and complexity of dolphin brains—a paradox?

Published online by Cambridge University Press:  17 March 2008

Stefan Huggenberger
Stefan Huggenberger*
Affiliation:
Zoological Institute II, University of Cologne, Weyertal 119, 50931 Köln, Germany
*
Correspondence should be addressed to: Stefan Huggenberger, Zoological Institute II, University of Cologne, Weyertal 119, 50931 Köln, Germany email: st.huggenberger@uni-koeln.de
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Abstract

Dolphin brain size with respect to body size ranks between that of apes and humans. The hypertrophic auditory structures, the large cerebrum with extended gyrification and the highly cognitive capabilities of toothed whales seem to be in paradoxical contrast to their thin neocortex with a plesiomorphic or paedomorphic cytoarchitecture. The total number of neurons in the delphinid neocortex is comparable to that of the chimpanzee (Primates), but, in relation to body weight, in the magnitude of the hedgehog (Insectivora) neocortex since cetaceans may be able to obtain larger body sizes than terrestrial mammals due to reduced gravitational effects in water. During evolution, dolphins may have increased the computational performance of their cytoarchitectonically ‘simple’ neocortex by a multiplication of relevant structures (resulting in a hypertrophic surface area) instead of increasing its complexity. Based on this hypothesis, I suggest that the evolution of the large dolphin brain was possible due to a combination of different prerequisites based on adaptations to the aquatic environment including the sonar system. The latter facilitated a successful feeding strategy to support an increased metabolic turnover of the brain and led to a hypertrophic auditory system. Moreover, the rudimentary pelvic girdle did not limit brain size at birth. These adaptations favoured the evolutionary size increase of the cerebral cortex in dolphins facilitating highly cognitive capabilities as well as precise and rapid sound processing using a ‘simple’ kind of neocortical cytoarchitecture.

Keywords

neocortexauditory systemtoothed whalescognitive capabilities
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 88 , Special Issue 6: Marine Mammals , September 2008 , pp. 1103 - 1108
Copyright
Copyright © Marine Biological Association of the United Kingdom 2008

INTRODUCTION

Several recent papers refer to the evolution and development of the large brain size of dolphins, ranking between that of apes and humans with respect to body size (Schwerdtfeger et al., Reference Schwerdtfeger, Oelschläger and Stephan1984; Deacon, Reference Deacon1990; Marino, 1998; Marino et al., 2003, 2004; Hof et al., Reference Hof, Chanis and Marino2005; Manger, Reference Manger2006). The development of this high encephalization level of dolphins and other toothed whales (Odontoceti) has been correlated with social competition (Connor, Reference Connor2007), a lengthened life span (Lefebvre et al., Reference Lefebvre, Marino, Sol, Lemieux-Lefebvre and Arshad2006), water temperature during the Eocene–Oligocene transition period (Manger, Reference Manger2006), and enhanced auditory processing (Oelschläger & Kemp, Reference Oelschläger and Kemp1998; Ridgway & Au, Reference Ridgway, Au, Adelman and Smith1999) as well as audiomotor navigation (Oelschläger, in press). Particularly impressive is the size and gyrification of the neocortex (isocortex) leading to a surface area surpassing that in humans (Ridgway & Brownson, Reference Ridgway and Brownson1979, Reference Ridgway and Brownson1984; Haug, Reference Haug1987; Hof et al., Reference Hof, Chanis and Marino2005; Marino, Reference Marino2007; Oelschläger et al., Reference Oelschläger, Haas-Rioth, Fung, Ridgway and Knauth2008).

Concrete functional implications of brain size, in general, and cortical expansion, in particular in dolphins are still enigmatic. However, the development of an underwater biosonar system in toothed whales during evolution led to profound modifications in the dolphin head (Rauschmann et al., Reference Rauschmann, Huggenberger, Kossatz and Oelschläger2006). Here, the functional synthesis of the unique (hypertrophic) nasal complex representing the sound generator (Cranford et al., Reference Cranford, Amundin and Norris1996; Cranford & Amundin, Reference Cranford, Amundin and Thomas2004) with the structures of the peripheral and central auditory system in toothed whales (Oelschläger & Oelschläger, Reference Oelschläger, Oelschläger and W.F.2002) may have been a primary factor for the evolutionary size increase of the brain as a whole (Oelschläger & Kemp, Reference Oelschläger and Kemp1998; Ridgway & Au, Reference Ridgway, Au, Adelman and Smith1999; Ridgway, 2000; Oelschläger, 2008; Oelschläger et al., in press). Auditory structures in the dolphin's brain are generally large (Figure 1A; Breathnach, Reference Breathnach1960, Bullock & Gurevich, Reference Bullock and Gurevich1979; Ridgway, Reference Ridgway and W.W.L.2000). The medial geniculate body is about seven times larger, the inferior colliculus twelve times and the lateral lemniscus 250 times larger in absolute terms than the equivalent structures in the human brain (Bullock & Gurevich, Reference Bullock and Gurevich1979). Thus, hypertrophic auditory structures may be the primary reason for the large brain in dolphins (Ridgway, Reference Ridgway and W.W.L.2000) and the cerebral cortex may have reached its great extension due to the increased acoustic input in modern dolphins (Langworthy, Reference Langworthy1932; Wood & Evans, Reference Wood, Evans, Busnel and Fish1980; Ridgway, Reference Ridgway, Leatherwood and Reeves1990, Reference Ridgway and W.W.L.2000). Accordingly, it was speculated that the hypertrophy of the dolphin brain results from the animal's need for greater precision and speed in processing sound due to the increased speed of sound in water compared to air (Ridgway & Au, Reference Ridgway, Au, Adelman and Smith1999; Ridgway, Reference Ridgway and W.W.L.2000; Oelschläger & Oelschläger, Reference Oelschläger, Oelschläger and W.F.2002). This hypertrophy correlates with the large diameter of auditory nerve fibres (Bullock & Gurevich, Reference Bullock and Gurevich1979), the short latency in auditory brainstem responses (ABRs), and rapid temporal resolution of successive sounds (Mooney et al., Reference Mooney, Nachtigall and Yuen2006 and references therein). Accordingly, Ridgway (Reference Ridgway and Schusterman1986, Reference Ridgway and W.W.L.2000) hypothesized that the specific neurons forming axes of echo delays (neurons tuned to discriminate target distance and azimuth) may take up considerable space in the cerebrum and could be a major reason for the great expansion of the neocortex in dolphins. This concept is supported by the observation that the ability to echolocate evolved in early toothed whales during the Oligocene period (Oelschläger, 1990; Fordyce & Muizon, Reference Fordyce, de Muizon, Mazin and de Buffrénil2001) in parallel to the increase of the size and scaling of their brain (Marino et al., Reference Marino, McShea and Uhen2004; Manger, Reference Manger2006).

Fig. 1. Brain of a La Plata dolphin (Pontoporia blainvillei), transverse section 20 µm. (A) Heidenhain–Woelcke stain, total slice width 7.61 cm; and (B & C) cresyl violet stain from the lateral cortical gyrus. The arrows and boxes indicate the approximate locations of the samples; note that the slice in (A) is slightly rostral to (B) and (C). Numbers indicate cortical layers. CB, cerebellum; CC, corpus callosum; CN, cochlear nucleus; IC, inferior colliculus; LL, lateral lemniscus; NC, neocortex; SO, superior olive; TB, trapezoid body. Scale bar: 100 µm.

Further parameters that may have led to the development of a large neocortex in toothed whales may have been the highly cognitive capabilities allowing behavioural complexity and ambitious communication skills leading to strong social relationships (Connor et al., Reference Connor, Mann, Tyack and Whitehead1998; Rendell & Whitehead, Reference Rendell and Whitehead2001; Marino, Reference Marino2002; Simmonds, Reference Marino, Uhen, Pyenson and Frohlich2006; Connor, Reference Connor2007). This could be shown, e.g. by the high learning and memory abilities of toothed whales (reviewed in Würsig, Reference Würsig and W.F.2002), the ability of self-monitoring and self-recognition (Reiss & Marino, Reference Reiss and Marino2001; Herman, Reference Herman, Hurley and Nudds2006), tool use (Krützen et al., Reference Krützen, Mann, Heithaus, Connor, Bejdar and Sherwin2005), highly differentiated social behaviour (e.g. Acevedo-Gutiérrez, Reference Acevedo-Gutiérrez and W.F.2002; Tyack, Reference Tyack and W.F.2002; Lusseau & Newman, Reference Lusseau and Newman2004; Connor & Mann, Reference Connor, Mann, Hurley and Nudds2006; Herman, Reference Herman, Hurley and Nudds2006; Connor, Reference Connor2007), understanding of language-like instructions (reviewed in Herman, Reference Herman, Hurley and Nudds2006) and cultural transmission (Rendell & Whitehead, Reference Rendell and Whitehead2001; Krützen et al., Reference Krützen, Mann, Heithaus, Connor, Bejdar and Sherwin2005; Kuczaj et al., Reference Kuczaj, Makecha, Trone, Paulos and Ramos2007). Accordingly, toothed whales should be regarded as ‘intelligent animals’ (Simmonds, Reference Simmonds2006) and the behaviour of dolphins is discussed as being metacognition (Browne, Reference Browne2004).

In dolphins, the need for great precision and speed in processing sound, the highly cognitive capabilities, the hypertrophic cerebrum and the extended gyrification of the latter (see above references) seem to be in paradoxical contrast to the thin neocortical plate (grey matter), the plesiomorphic or paedomorphic lamination of the neocortex and the low density of neurons (Glezer, Reference Glezer and Hoelzel2002; Oelschläger & Oelschläger, Reference Oelschläger, Oelschläger and W.F.2002). The neocortical grey matter is characterized by: (i) the widespread absence of layer IV; (ii) poor granulation with a predominance of large isodendritic stellate cells; (iii) well developed layers I and VI; (iv) an accentuated layer II; and (v) a high number of pyramidal neurons in layers II to VI (Figure 1B,C; Morgane et al., Reference Morgane, Glezer, Jacobs, Jones and Peters1990; Hof et al., Reference Hof, Chanis and Marino2005 and references therein). These characteristics seem to represent a primitive mammalian brain (Glezer et al., Reference Glezer, Jacobs and Morgane1988). However, since the common ancestors of cetaceans and ungulates may have possessed layer IV granule cells (Deacon, Reference Deacon1990; Oelschläger & Oelschläger, Reference Oelschläger, Oelschläger and W.F.2002) at least the absence of this layer should represent a secondary condition in dolphins. Interestingly, cytoarchitectonical studies in several toothed whale species reveal clearly identifiable neocortical areas similar to those identified in other mammals (Fung et al., Reference Fung, Schleicher, Kowalski and Oelschläger2005; Hof et al., Reference Hof, Chanis and Marino2005) but the neocortex exhibits an unusual arrangement of sensory-motor areas (Glezer et al., Reference Glezer, Jacobs and Morgane1988; Morgane et al., Reference Morgane, Glezer, Jacobs, Jones and Peters1990).

COMPARATIVE ASPECTS OF THE NEOCORTEX

Although neuron density is low in the dolphin neocortex (Figure 1C; Haug, Reference Haug1987; Oelschläger & Oelschläger, Reference Oelschläger, Oelschläger and W.F.2002), the synaptic density is high (maximal number of synapses per neuron) and the absolute number of synapses in the neocortex is similar to that in humans (Glezer & Morgane, Reference Glezer and Morgane1990; Morgane et al., Reference Morgane, Glezer, Jacobs, Jones and Peters1990; Oelschläger & Oelschläger, Reference Oelschläger, Oelschläger and W.F.2002). The total number of neurons in the neocortex of the bottlenose dolphin and the false killer whale (a delphinid species; Rice, Reference Rice1998) is similar to that of the chimpanzee and clearly above that of the other mammals included in this study (rat, hedgehog, cat, rhesus monkey and horse) except the elephant and human (Table 1; Roth & Dicke, Reference Roth and Dicke2005). Interestingly, recent studies of the baleen whale (Mysticeti) brain demonstrate that the neocortex of these large mammals, although different in cytoarchitecture (Hof & van der Gucht, Reference Hof and Gucht E.2007) but comparably large in absolute terms (Oelschläger & Oelschläger, Reference Oelschläger, Oelschläger and W.F.2002), approximates the same high absolute neuron number as in dolphins (compared to rats and humans; Eriksen & Pakkenberg, Reference Eriksen and Pakkenberg2007).

Table 1. Comparison of the total number of neocortical neurons with brain weight and body weight in different mammalian species.

Data Sources: A Roth & Dicke (Reference Roth and Dicke2005); B Spector (Reference Spector1956), Leatherwood & Reeves (Reference Leatherwood and Reeves1983), Marino (Reference Marino1998), Shoshani et al. (Reference Shoshani, Kupsky and Marchant2006). Note that the total number of neocortical neurons was calculated using the method of Roth & Dicke (Reference Roth and Dicke2005) but derived from Haug (Reference Haug1987).

The brain weight of the chimpanzee is less than of the two dolphin species studied here and the latter are only surpassed by those in the elephant and the human (Table 1). Accordingly, the dolphins have more neocortical neurons in relation to their brain weight than the chimpanzee (and the elephant) but less than the rhesus monkey (Figure 2). The hedgehog and the rat have approximately the same number of neocortical neurons per gram brain weight as the human which is only surpassed by the cat. In relation to body weight, however, the neuron number in dolphins is in the range of the hedgehog which is lower than in the rat, rhesus monkey, cat, chimpanzee and human (Figure 2). This value is in contrast to the large absolute number of neurons in the dolphin neocortex due to their large body mass (Table 1) which is also true for the elephant and horse (Figure 2).

Fig. 2. Comparison of total cortical neurons in relation to brain weight (left) and body weight (right) of ten mammalian species belonging to seven different orders (based on data in Table 1). The two delphinid species are marked in darker grey.

Due to the high absolute number of neurons contributing to the neocortical network as well as the high number of synapses in the odontocete neocortex (see above references) it is plausible that these morphological peculiarities are the prerequisite for the strong cognitive capabilities of dolphins (cf. Roth & Dicke, Reference Roth and Dicke2005). The low number of neocortical neurons in relation to body weight may be explained by ‘aquatic weightlessness’ (due to fewer gravitational constraints in the aquatic environment) allowing cetaceans to obtain larger bodies than terrestrial mammals, which suggests that the encephalization levels in many cetacean species are probably underestimated (Marino, Reference Marino1998) and body weight may not be a useful reference for brain size (Harvey & Krebs, Reference Harvey and Krebs1990).

INCREASE OF NEOCORTICAL SIZE INSTEAD OF COMPLEXITY

The cetacean cerebral cortex is probably unique and the lack of pronounced neocortical lamination, absence of layer IV, a thin neocortex, low neuronal density, and pyramidal cells in layer II, will probably all compromise the processing capacity of the mammalian neocortical network (Manger, Reference Manger2006). A plausible alternative to compensate for these alterations in structure may be an increase in size of the dolphin brain. The ability to perform precise and fast sound processing and the highly cognitive capabilities may be made possible by an expansion or multiplication of a ‘simple’ neocortex (Figure 3; Glezer et al., Reference Glezer, Jacobs and Morgane1988) instead of the development of a more complex one. This was probably a neurobiological alternative to the situation in primates (Hof & van der Gucht, Reference Hof and Gucht E.2007; Marino et al., Reference Marino2007). Thus, during evolution, dolphins may have increased the computational performance of their brain by a multiplication of relevant structures (resulting in an enlargement of the neocortical surface area and a high number of neurons and synapses) instead of increasing its complexity. This potential evolutionary trend, resulting in the large brain of extant dolphins, was advantageous due to two adaptations to the aquatic environment: (i) the feeding behaviour of toothed whales is highly successful since their ability to echolocate and communicate effectively allows them to fit in ecological niches not available to other marine vertebrates (Figure 3; Oelschläger, Reference Oelschläger, Thomas and Kastelein1990; Fordyce & Muizon, 2001). Thus, the supply of a large brain, which is a considerable metabolic expense, should not be a limiting factor (McFarland et al., Reference McFarland, Jacobs and Morgane1979; Niven, Reference Niven2005; Ridgway et al., Reference Ridgway2006; Connor, Reference Connor2007); and (ii) toothed whales do not have a pelvic girdle. Instead, if developed at all, they have two small bones near the mid-sagittal plane, which are not fused (Adam, Reference Adam and W.F.2002), so that the shape and the size of the birth canal (apertura pelvis) may not limit head size at birth as is the case in humans (Figure 3; e.g. Ruff, Reference Ruff1995). In summary, the size of the dolphin brain does not seem to be in paradoxical contrast to the ‘simple’ neocortical architecture but rather the result of an evolutionary alternative solution to improve its computational performance. This alternative path was probably facilitated by the secondary adaptations of these mammals to the aquatic environment. Due to the general similarities of the toothed whale neocortex (Fung et al., Reference Fung, Schleicher, Kowalski and Oelschläger2005; Hof et al., Reference Hof, Chanis and Marino2005; Manger, Reference Manger2006) and their monophyly (Fordyce & Muizon, 2001; Nikaido et al., Reference Nikaido, Piskurek and Okada2007) the hypothesis mentioned above may be true for all odontocetes.

Fig. 3. Diagram showing different parameters supporting the increase of brain size during dolphin evolution: feeding success, the absence of a pelvic girdle and the combination (indicated by ‘Σ’) of a ‘simple’ neocortical cytoarchitecture with the development of highly cognitive capabilities and the need for precise and fast processing of sound for echo-orientation.

ACKNOWLEDGEMENTS

My sincere thanks go to Helmut H.A. Oelschläger (Institute of Anatomy III, Johann Wolfgang Goethe-University of Frankfurt am Main, Germany) for the donation of photographs of odontocete brain material under his care and I deeply appreciate his advice and assistance contributing to my understanding of cetacean anatomy. Sharon Meyen-Southard (Zoological Institute II, University of Cologne, Germany) kindly corrected the English style and two anonymous referees are thanked for their valuable comments on this paper.

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Figure 0

Fig. 1. Brain of a La Plata dolphin (Pontoporia blainvillei), transverse section 20 µm. (A) Heidenhain–Woelcke stain, total slice width 7.61 cm; and (B & C) cresyl violet stain from the lateral cortical gyrus. The arrows and boxes indicate the approximate locations of the samples; note that the slice in (A) is slightly rostral to (B) and (C). Numbers indicate cortical layers. CB, cerebellum; CC, corpus callosum; CN, cochlear nucleus; IC, inferior colliculus; LL, lateral lemniscus; NC, neocortex; SO, superior olive; TB, trapezoid body. Scale bar: 100 µm.

Figure 1

Table 1. Comparison of the total number of neocortical neurons with brain weight and body weight in different mammalian species.

Figure 2

Fig. 2. Comparison of total cortical neurons in relation to brain weight (left) and body weight (right) of ten mammalian species belonging to seven different orders (based on data in Table 1). The two delphinid species are marked in darker grey.

Figure 3

Fig. 3. Diagram showing different parameters supporting the increase of brain size during dolphin evolution: feeding success, the absence of a pelvic girdle and the combination (indicated by ‘Σ’) of a ‘simple’ neocortical cytoarchitecture with the development of highly cognitive capabilities and the need for precise and fast processing of sound for echo-orientation.