Review
The dolphin brain—A challenge for synthetic neurobiology

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Abstract

Toothed whales (odontocetes) are a promising paradigm for neurobiology and evolutionary biology. The ecophysiological implications and structural adaptations of their brain seem to reflect the necessity of effective underwater hearing for echolocation (sonar), navigation, and communication. However, not all components of the auditory system are equally well developed. Other sensory systems are more or less strongly reduced such as the olfactory system and, as an exception among vertebrates, the vestibular system (the semicircular canals and vestibular nuclei). Additional outstanding features are: (1) the hypertrophy of the neocortex, pons, cerebellum (particularly the paraflocculus), the elliptic nucleus, the facial motor nucleus and the medial accessory inferior olive and (2) the reduction of the hippocampus. The screening of brain structures with respect to shared circuitry and shared size correlations resulted in central loops also known from other mammals which overlap in the cerebellum and serve in the integration and processing of sensory input.

It is highly probable that for dolphin navigation the ascending auditory pathway, including the inferior colliculus and the medial geniculate body, is of utmost importance. The extended auditory neocortical fields project to the midbrain and rhombencephalon and may influence premotor and motor areas in such a way as to allow the smooth regulation of sound-induced and sound-controlled locomotor activity as well as sophisticated phonation. This sonar-guided acousticomotor system for navigation and vocalization in the aquatic environment may have been a major factor if not the key feature in the relative size increase seen in dolphin brains.

Introduction

Whales and dolphins (cetaceans) are a fascinating and probably highly heuristic paradigm for evolutionary neurobiology. They originated among ancient even-toed hoofed animals (Artiodactyla) at the end of the cretaceous period (approx. 55 million years ago; [17], [18], [52]). This is particularly remarkable because holaquatic life requires profound modifications in all organ systems [7], [42], [67]. During the last decade, paleontologists presented a large body of evidence on these modifications [14]. They showed that those early mammals gradually acquired a hydrodynamic body profile and explained how ancient toothed whales (odontocetes) may have improved their capacity as to hearing directionality under water [13], [43], [44], [45], [46]. By the Miocene, the descendants had assembled a set of soft tissue structures in their forehead which allow extant odontocetes to echolocate by means of a biosonar system [2], [9], [22], [56].

Although cetacean history is well documented by means of the fossil record [14], [17], [18], the evolution of their central nervous system (CNS) is largely unknown and refers to the external morphology only. This is very unfortunate because the CNS acts as an interface between the body of an animal and its environment. The brain integrates all the afferent information into an adequate reaction useful for the survival of the individual. Moreover, peripheral structures (sensory organs, skin, musculoskeletal system) and the CNS are so closely related that every evolutionary change in the body of a species is reflected in the dimensions, structure and function of the respective brain components and may thus even change total brain size [4], [71]. For instance, size increase of the brain as a whole, and particularly of the neocortex, auditory centers, sensory component of trigeminal nerve, the motor centers and those associated with motor coordination has been shown in semiaquatic insectivores in comparison with terrestrial forms [5] and in predatory bats correlated with behavioral flexibility [57].

In turn, structural and functional relationships between brain areas become obvious in size correlations because functional systems can only evolve as entities [29]. As a result, the overlapping of size correlations and circuitry can help reconstruct the evolutionary adaptations of mammals to a new environment which, in the case of whales and dolphins, may have been rather dramatic. Because there is limited access to information on brain structure in fossil whales, comparison of extant dolphins with other mammals is the adequate methodology for a genuine understanding of their biology. Whereas in the past, a number of investigations were done on toothed whale brains with conventional neuroanatomical (histological) methods, invasive techniques cannot be applied in extant odontocetes because of their strong protection. Non-invasive imaging techniques (MRI, fMRI), however, so far can be used either as a complement to histology at low magnification [49] or for the documentation of dolphin brain metabolism and blood flow [62] but not for experimental analysis of structural relationships. Thus, the most promising tool for in-depth analysis of the cetacean (dolphin) brain today is the determination of qualitative and quantitative characteristics and their synthetic functional interpretation in the light of modern neurobiological findings in terrestrial mammals.

The adult cetacean brain comprises nearly all the structures known from other mammals. With regard to potential ancestors, however, its shape seems to have changed secondarily by means of a shortening in the rostrocaudal direction and a dramatic size increase, resulting in an unusual dorsoventral extension (‘towering’) of the cerebral hemispheres. The brain of most toothed whales is rather large in absolute terms with a maximal mass of approximately 10 kg in the giant sperm whale (Physeter macrocephalus) and possibly large killer whales (Orcinus orca; [63]). Smaller pelagial dolphins (delphinids) attain a relative brain size which is second to that in humans [33], [51], [49], [65]. Obviously, the dramatic change in habitat, apart from other adaptational trends, led to a strong selection pressure as to underwater hearing ability. Other sensory systems seem to have been less favoured in the new environment and were more or less reduced. In particular, this is true for the odontocete olfactory system (see below).

In the following, old and new morphological and experimental data on cetaceans and other mammals are used for a synthetic view of brain function in toothed whales and dolphins, in particular. Instead of aiming at the interpretation of whole brains or single large components (neocortex) as to specific aspects (thermogenesis [33]; complex cognition [36]), this paper gives a short survey over the characteristics of the dolphin brain and focuses on the acousticomotor complex which comprises structures in all major brain areas and seems to be essential for the aquatic life of these animals.

Whereas Table 1 gives a survey on the sensory and motor characteristics of marine toothed whales, Fig. 1 shows the connectivity between the auditory system and premotor and motor brain centers in dolphins, and Fig. 2 focuses on central loops in the brainstem essential for phonation and acousticomotor navigation.

The material used was obtained from the extensive microslide collections of prenatal cetaceans (Klima Collection) and adult cetacean brains (Pilleri Collection) present in the Research Institute and Natural History Museum Senckenberg as well as in the Institute of Anatomy III (Dr. Senckenbergische Anatomie), Johann Wolfgang Goethe University in Frankfurt am Main.

Section snippets

Structural aspects of the toothed whale brain

For an understanding of the potential sensory biology and locomotion in odontocetes, it is useful to review some of the basic neurological facts that characterize their brains and correlate with major adaptations of these animals to their aquatic habitat. Since most of the existing data come from species such as the bottlenose dolphin, delphinid data are emphasized and compared with the data available for other mammals.

The olfactory and somatosensory systems

In dolphins, the sense of smell seems to have been lost. The olfactory nerve, bulb and tract vanish during embryonic and early fetal development [47], [48]. Concomitantly, the region of the upper respiratory tract transforms into a generator of ultrasound and sound signals (the epicranial complex) which is essential for echolocation (orientation, hunting) and for communication [9], [22], [56]. During odontocete evolution, the mechanical impact of pneumatic sonar signal generation may have led

Synthesis of the size correlations and connectivity in the dolphin brain

With respect to the situation in generalized terrestrial mammals, the dolphin brain is characterized by a series of extreme adaptations, ranging from hypertrophy to massive reduction and loss of structures. Size increase or decrease, however, may affect larger or smaller brain areas, depending on their potential functional implications (relay station or integrative area vs. topographic representation) so that their size correlations are only recognizable within the framework of connectivity. As

Acousticomotor navigation

In the first instance, the dolphin brain may be understood as consisting of a few major loops connecting brain structures of relatively large size in comparison with terrestrial mammals of similar body dimensions. Although this view is an oversimplification of the real situation and therefore leaves many questions unanswered, it may help to illustrate the central role of the auditory system within these loops and thus within the dolphin's brain and dolphin behavior. One of these loops (the core

Conclusions

The brains of dolphins attain the same size dimensions and complexity as those of large terrestrial mammals and the human. Because of their long separate evolution in aquatic habitats, however, they differ from the latter in many aspects. In principle, mammalian biology can be reconstructed by interpreting the ensemble of all the brain features characteristic for a particular group. Thus, the hypertrophy or size reduction of brain components can be used to comprehend the functional adaptations

Acknowledgements

The author wishes to thank Gerhard Storch (Research Institute and Natural History Museum Senckenberg in Frankfurt a.M.), Milan Klima (Institute of Anatomy III, Dr. Senckenbergische Anatomie) in Frankfurt a.M. and Giorgio Pilleri (Courgeveaux, Switzerland) for making available the material used in this investigation. I am grateful to Inge Szász-Jacobi and Jutta S. Oelschläger for excellent graphic reconstructions and Laura M. Breindl, Alexander Kern, and Sefer Yildiz for helpful discussions.

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