Nature's experiments in brain diversity

Authors


Abstract

This special issue of The Anatomical Record originates from a symposium on the evolution of neurobiological specializations in mammals held at the American Association of Anatomists annual meeting in San Diego in April 2005. The symposium, co-organized by Patrick R. Hof and Lori Marino, provided the impetus for extending the discussion to a greater range of species. This special issue is the product of that goal and is fueled by the philosophy that it is largely against a backdrop of brain diversity that we can extract the higher-order commonalities across brains that may lead us to uncovering general higher-order principles of brain and behavioral evolution. Several major themes emerge from this issue. These are that there are no simple brains, that brains reflect ecology, and that brain evolution is a detective story. The 12 articles in this issue are outstanding reflections of these themes. © 2005 Wiley-Liss, Inc.

In this issue, we celebrate the fact that the history of biological evolution on this planet has presented us with a stunning variety of brains to study and learn from. Nature has produced innumerable examples of how to build brains of all kinds. Evolution, i.e., “nature's experiment,” provides us with a bounty of raw data on how brains evolve in relation to environmental niches. It is largely against this backdrop of brain diversity that we can extract the higher-order commonalities across brains that may lead us to uncovering general higher-order principles of brain and behavioral evolution.

This special issue of The Anatomical Record originates from a symposium on the evolution of neurobiological specializations in mammals held at the American Association of Anatomists annual meeting in San Diego in April 2005. The symposium, co-organized by Patrick R. Hof and Lori Marino, showcased the work of some of the authors in the current issue. We present articles that focus on an arguably unprecedented range of species in a single issue. Articles include taxa as diverse as birds and primates as well as rarely studied species such as the African elephant (Loxodonta africana). This diversity reflects the different evolutionary paths that species have taken in addressing the particular demands and needs of their environment. Furthermore, each of the articles in this issue moves beyond descriptive neuroanatomy to examine and interpret brain organization in the context of evolution, adaptation, and function. In the process, several new and unexpected results are revealed. Potentially, examples of divergence, conservatism, and convergence will emerge from this issue that provide new perspectives and insights into larger patterns of brain and behavioral evolution.

MAJOR THEMES IN BRAIN DIVERSITY

The collection of topics in this issue reflects several major themes. One of the most important themes to emerge here is that there are no simple brains. Traditional views of small-brained mammals (and birds) as less complex and somehow more primitive than larger-brained mammals are obsolete. A particularly striking example is how the modern Insectivora order has historically been viewed as a group of primitive mammals that retained mostly conservative neuroanatomical features. As a result, they have often been used as substitutes for the ancestral mammalian condition in studies of early mammalian brain evolution. Catania (this issue) exposes the considerable visual, auditory, and somatosensory cortical complexity found in many insectivores. In contrast to historical views of insectivores, Catania shows that species within this group are actually highly derived mammals with discrete and well-organized cortical sensory areas with sharp borders as determined both electrophysiologically and histologically. Catania also analogizes the modular somatosensory cortex of the highly specialized star-nosed mole (Condylura cristata) to visual cortical areas in other mammals. In addition, Catania points out that there is very little evidence that insectivore behavior is simple and primitive. Instead, the elaborated specialized sensory systems in many insectivore species such as the star-nosed mole support a rich array of complex behavioral capacities required by the ecological niche in which they reside.

In keeping with this major theme, Covey (this issue) describes the brains of echolocating bats (Microchiroptera). She shows that the strengths and timing of synaptic inputs to neurons in auditory pathways of echolocating bats have been exquisitely shaped by the behavioral specializations of echolocation. Bats have optimized the mechanisms for analysis of complex sound patterns to derive accurate and highly complex information about objects in their environment and direct behavior toward those objects.

In another example from a very different taxonomic group, Hof et al. (this issue) summarize data on brain size and hemisphere surface configuration in several cetacean species and present a general description of cytoarchitectural characteristics in the cerebral cortex of the bottlenose dolphin (Tursiops truncatus). Cetacean and primate brains can be conceived as alternative evolutionary strategies to neurobiological and cognitive complexity. As such, cetaceans offer a critical opportunity to evaluate and compare how complex behaviors can be based on very different neuroanatomical and neurobiological evolutionary products. The data reported challenge the common conception that the cetacean cortex is rather nondifferentiated, a view that has had historical implications for the perception of cetacean cognitive complexity and intelligence and posed a perplexing inconsistency when considering the evidence for considerable cognitive and behavioral complexity in these species. The authors show that the cytoarchitectural patterns in cetaceans, at least based on the bottlenose dolphin, are far more varied and complex than has been generally believed. Although lamination differs radically from that seen in most terrestrial species, several neocortical regions can be recognized that support much cytoarchitectural differentiation and diversity. Also, despite the modest gross morphological appearance of the frontal lobes, which contrasts with primates, this region is distinctly laminated with its own unique pattern of differentiation and comprises many cortical fields, as in the other lobes. The authors also point to many similarities in cortical organization between cetaceans and large terrestrial herbivores, which is supported by the accepted phylogenetic affinities between cetaceans and artiodactyls.

Finally, Reiner et al. (this issue) move outside of the mammalian domain with their description of the organization and evolution of the avian forebrain. Historically, the dominant view of the avian telencephalon was that it represented a hypertrophied version of the basal ganglia and was quite unlike mammalian neocortex (Edinger et al., 1903; Ariëns-Kappers et al., 1936). Accordingly, birds were viewed as rather behaviorally simple and inflexible. Over the past few decades, investigators have refuted this view and showed that (along with complex behavioral and cognitive abilities) birds are in possession of brains with a very large pallial area that is analogous to mammalian neocortex. It was not until very recently, however, that the terminology was changed to reflect this more updated view of avian brains (Jarvis et al., 2005). In this issue, Reiner et al. show how the large avian cerebrum reflects expansion of pallial regions, which are now recognized as functionally comparable to mammalian cerebral cortex, and which provide the substrate for the substantial behavioral and cognitive skills that we now know birds to possess.

Another main theme to emerge here is that of the fit between brain and ecological niche. Whereas all of the articles in this issue provide informative examples of how brain organization reflects ecological demands, the study by Kaufman et al. (this issue) presents a highly unusual example with their focus on the aye-aye (Daubentonia madagascariensis). Kaufman et al. apply imaging methods in conjunction with histological techniques to provide the first quantitative comparison of imaging data and fiber-stained histology in the aye-aye brain. The aye-aye is a large nocturnal prosimian with a unique ecological niche among primates. The aye-aye is a specialist in extractive foraging, probing for insect larvae that lie deep within tree bark (Ganzhorn and Rabesoa, 1986; Sterling, 1993, 1994). Kaufman et al. provide new data to confirm that the aye-aye has a large frontal cortex, particularly for a prosimian. This is potentially relevant in light of the high level of sensorimotor intelligence thought to be associated with the complex foraging behavior observed in this species (Parker and Gibson, 1977; Gibson, 1986). Kaufman et al. suggest that an enlarged frontal cortex in the aye-aye could also be associated with the need to integrate a large amount of sensory information during foraging. In addition to whole brain size and frontal cortex size, the relative volumes of sensory structures in the aye-aye are also consistent with its ecological niche as a nocturnal extractive forager. For instance, the volumes of lateral geniculate nucleus and visual striate cortex are reduced, while the olfactory bulb appears greatly enlarged. This pattern is in direct opposition to the typical primate pattern of enhanced vision and reduced olfaction (Allman, 2000). Therefore, through their examination of the brain of the aye-aye, Kaufman et al. provide a striking example of how brains can deviate from generally expected phylogenetic patterns and evolve to reflect closely the demands of highly specific ecological niches.

Another example of the fit between ecological demands and brain structure in a prosimian is provided by Collins et al. (this issue) in their study on the brain of the tarsier (Tarsius spectrum). They show that the tarsier brain is unusually large and possesses a distinctly laminated primary visual cortex (VI). Tarsiers also possess a large number of unusual distributions of cones in the retina. Kaufman et al. hypothesize that these features of the tarsier brain are adaptive specializations for the behavioral demands of their particular niche as nocturnal predators.

Sherwood (this issue) provides yet another example of the relationship between brain organization on the one hand and species-specific traits on the other. Instead of focusing on physical ecological demands, however, Sherwood provides evidence that the sociobehavioral characteristics of various primate species can play an important role in shaping neuroanatomy in addition to demands of the physical environment. In his discussion of the comparative anatomy of the facial motor nucleus in mammals, Sherwood shows how the anatomic organization of the facial nerve (VII) is heavily phylogenetically conserved across species but also reflects species-specific specializations in the use of facial muscles for social communication in the socially complex clade of great apes and humans. Sherwood suggests that direct neocortical connections to VII may have evolved to provide voluntary control over complex facial expressions in primates in general.

Hakeem et al. (this issue) provide the first imaging-based description of the elephant brain (Loxodonta africana) and attempt to understand brain structure in this species both in a comparative context and from an ecological and behavioral perspective. The authors use comparisons of elephant brains and cetacean brains to control for the role of scaling factors in the features that emerge from their analysis. The authors find that the elephant brain is similar to the cetacean brain in degree of cortical folding but differs from cetacean brains in major ways. For instance, elephant brains conform to the same scaling trends in relative corpus callosum size as primates while cetaceans possess a deviantly small corpus callosum. Also, unlike cetaceans, elephants possess a substantial hippocampus with a unique dorsal extension. The authors suggest that the large hippocampus is related to their prodigious long-term memory but further work needs to be done to examine this idea.

Finally, Peichl (this issue) provides an overview of the diversity of photoreceptors in mammals and attempts to consider them within the framework of adaptation to particular environments and lifestyles. Peichl shows that there seems to be a basic plan or bauplan in photoreceptor systems across mammals that is shaped by species-specific characteristics. However, this study also serves as an important reminder that the relationship between neurological structure and ecology/environment is not always straightforward and apparent.

Another important theme that emerges from this issue is that of evolution as a detective story. All of the studies in this issue deal with evolutionary issues and questions and it is obviously difficult to imagine any useful comparative neuroanatomy without relating it to evolution and phylogeny. Several of the studies, however, are particularly salient examples of the authors' efforts to piece together how the evolution of a particular neurobehavioral system unfolded over time. For instance, Gannon et al. (this issue) tackle the evolutionary origin of human language areas in the brain. They use the comparative approach to investigate the anatomic representation of various language-related brain regions, in this case the planum parietale, in humans and other primates. The authors provide evidence that the neuroanatomical precursors of language exist in great apes. Using the logic of the comparative approach, they attempt to reconstruct the evolution of language in hominids from a shared neuroanatomical substrate in the ancestor of great apes and humans.

In complement with the approach by Gannon et al., Hunt et al. (this issue) provide an example of how experimental assaying of sensory systems can elucidate mechanisms underlying brain development, plasticity, and, ultimately, evolution. Hunt et al. use neuroanatomical tracers to examine the retinofugal pathway in normal and congenitally deaf mice. They show that aberrant visual inputs to auditory structures in the deaf mice indicate substantial cortical plasticity and reorganization in order to optimize the suite of sensory information utilized by the mouse. These kinds of compensatory anatomical changes in the brain might elucidate the neuromechanistic substrate of ontogenetic and phylogenetic-evolutionary changes.

Another example in uncovering evolutionary patterns, especially as it relates to phylogenetic relationships, is found in Hof and Sherwood (this issue). In spite of many cytoarchitectural studies, the molecular makeup of the various populations of neurons in the cerebral cortex and other brain structures has not been analyzed systematically in an evolutionary context. Hof and Sherwood summarize observations made in a large series of species representative of the major subdivisions of mammals on the morphologic characteristics and distribution of calcium-binding proteins and nonphosphorylated neurofilament protein that are known markers of specific subpopulations of excitatory and inhibitory neurons in the neocortex of these species. The distribution of these neurochemical markers reveals species- and order-specific patterns that permit assessment of neuronal morphomolecular specialization, and cell type distribution the neocortex, as representative of derived or ancestral features and their use in defining taxonomic affinities among species. Independent of the diversity in morphologic and cellular organization that occurred during mammalian neocortical evolution, such patterns reveal several associations among taxa that closely match their phylogenetic relationships.

CONCLUSION

One of the major objectives of comparative neuroanatomy is to use the range of data made available by nature to extract the higher-order commonalities across brains that may lead us to uncovering general higher-order principles of brain and behavioral evolution. The articles in this issue reflect the fact that truly comparative work can provide the potential to uncover those principles. Eventually we may possess a deeper understanding of the relationship between brains, behavior, and environment.

Acknowledgements

The authors thank the participants of the symposium on the evolution of neurobiological specializations in mammals held at the American Association of Anatomists annual meeting in San Diego in April 2005. They also acknowledge Editor Roger R. Markwald and Managing Editor David Bernanke. Special thanks to Associate Editor Jeffrey Laitman for his enduring support for this symposium and special issue and his valuable advice and assistance in bringing the issue to fruition.

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