Nature’s Experiments in BrainDiversity

LORI MARINO1* AND PATRICK R. HOF2

1Neuroscience and Behavioral Biology Program, Emory University, Atlanta, Georgia2Department of Neuroscience, Mount Sinai School of Medicine, New York, New York

ABSTRACTThis special issue of The Anatomical Record originates from a sympo-

sium on the evolution of neurobiological specializations in mammals held atthe American Association of Anatomists annual meeting in San Diego inApril 2005. The symposium, co-organized by Patrick R. Hof and LoriMarino, provided the impetus for extending the discussion to a greaterrange of species. This special issue is the product of that goal and is fueledby the philosophy that it is largely against a backdrop of brain diversity thatwe can extract the higher-order commonalities across brains that may leadus to uncovering general higher-order principles of brain and behavioralevolution. Several major themes emerge from this issue. These are thatthere are no simple brains, that brains reflect ecology, and that brainevolution is a detective story. The 12 articles in this issue are outstandingreflections of these themes. © 2005 Wiley-Liss, Inc.

Key words: comparative neuroanatomy; evolution; taxondiversity

In this issue, we celebrate the fact that the history ofbiological evolution on this planet has presented us with astunning variety of brains to study and learn from. Naturehas produced innumerable examples of how to buildbrains of all kinds. Evolution, i.e., “nature’s experiment,”provides us with a bounty of raw data on how brainsevolve in relation to environmental niches. It is largelyagainst this backdrop of brain diversity that we can ex-tract the higher-order commonalities across brains thatmay lead us to uncovering general higher-order principlesof brain and behavioral evolution.

This special issue of The Anatomical Record originatesfrom a symposium on the evolution of neurobiological spe-cializations in mammals held at the American Associationof Anatomists annual meeting in San Diego in April 2005.The symposium, co-organized by Patrick R. Hof and LoriMarino, showcased the work of some of the authors in thecurrent issue. We present articles that focus on an argu-ably unprecedented range of species in a single issue.Articles include taxa as diverse as birds and primates aswell as rarely studied species such as the African elephant(Loxodonta africana). This diversity reflects the differentevolutionary paths that species have taken in addressingthe particular demands and needs of their environment.Furthermore, each of the articles in this issue moves be-yond descriptive neuroanatomy to examine and interpretbrain 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 is-sue that provide new perspectives and insights into largerpatterns of brain and behavioral evolution.

MAJOR THEMES IN BRAIN DIVERSITYThe collection of topics in this issue reflects several

major themes. One of the most important themes toemerge here is that there are no simple brains. Tradi-tional views of small-brained mammals (and birds) as lesscomplex and somehow more primitive than larger-brainedmammals are obsolete. A particularly striking example ishow the modern Insectivora order has historically beenviewed as a group of primitive mammals that retainedmostly conservative neuroanatomical features. As a re-sult, they have often been used as substitutes for theancestral mammalian condition in studies of early mam-malian brain evolution. Catania (this issue) exposes the

*Correspondence to: Lori Marino, Neuroscience and BehavioralBiology Program, Emory University, Atlanta, GA 30322.Fax: 404-727-7471. E-mail: lmarino@emory.edu

Received 16 August 2005; Accepted 17 August 2005DOI 10.1002/ar.a.20261Published online 2 October 2005 in Wiley InterScience(www.interscience.wiley.com).

THE ANATOMICAL RECORD PART A 287A:997–1000 (2005)

© 2005 WILEY-LISS, INC.

considerable visual, auditory, and somatosensory corticalcomplexity found in many insectivores. In contrast to his-torical views of insectivores, Catania shows that specieswithin this group are actually highly derived mammalswith discrete and well-organized cortical sensory areaswith sharp borders as determined both electrophysiologi-cally and histologically. Catania also analogizes the mod-ular somatosensory cortex of the highly specialized star-nosed mole (Condylura cristata) to visual cortical areas inother mammals. In addition, Catania points out that thereis very little evidence that insectivore behavior is simpleand primitive. Instead, the elaborated specialized sensorysystems in many insectivore species such as the star-nosed mole support a rich array of complex behavioralcapacities required by the ecological niche in which theyreside.

In keeping with this major theme, Covey (this issue)describes the brains of echolocating bats (Microchirop-tera). She shows that the strengths and timing of synapticinputs to neurons in auditory pathways of echolocatingbats have been exquisitely shaped by the behavioral spe-cializations of echolocation. Bats have optimized themechanisms for analysis of complex sound patterns toderive accurate and highly complex information aboutobjects in their environment and direct behavior towardthose objects.

In another example from a very different taxonomicgroup, Hof et al. (this issue) summarize data on brain sizeand hemisphere surface configuration in several cetaceanspecies and present a general description of cytoarchitec-tural characteristics in the cerebral cortex of the bottle-nose dolphin (Tursiops truncatus). Cetacean and primatebrains can be conceived as alternative evolutionary strat-egies to neurobiological and cognitive complexity. As such,cetaceans offer a critical opportunity to evaluate and com-pare how complex behaviors can be based on very differentneuroanatomical and neurobiological evolutionary prod-ucts. The data reported challenge the common conceptionthat the cetacean cortex is rather nondifferentiated, aview that has had historical implications for the percep-tion of cetacean cognitive complexity and intelligence andposed a perplexing inconsistency when considering theevidence for considerable cognitive and behavioral com-plexity in these species. The authors show that the cyto-architectural patterns in cetaceans, at least based on thebottlenose dolphin, are far more varied and complex thanhas been generally believed. Although lamination differsradically from that seen in most terrestrial species, sev-eral neocortical regions can be recognized that supportmuch cytoarchitectural differentiation and diversity. Also,despite the modest gross morphological appearance of thefrontal lobes, which contrasts with primates, this region isdistinctly laminated with its own unique pattern of differ-entiation and comprises many cortical fields, as in theother lobes. The authors also point to many similarities incortical organization between cetaceans and large terres-trial herbivores, which is supported by the accepted phy-logenetic affinities between cetaceans and artiodactyls.

Finally, Reiner et al. (this issue) move outside of themammalian domain with their description of the organi-zation and evolution of the avian forebrain. Historically,the dominant view of the avian telencephalon was that itrepresented a hypertrophied version of the basal gangliaand was quite unlike mammalian neocortex (Edinger etal., 1903; Ariens-Kappers et al., 1936). Accordingly, birds

were viewed as rather behaviorally simple and inflexible.Over the past few decades, investigators have refuted thisview and showed that (along with complex behavioral andcognitive abilities) birds are in possession of brains with avery large pallial area that is analogous to mammalianneocortex. It was not until very recently, however, that theterminology was changed to reflect this more updatedview of avian brains (Jarvis et al., 2005). In this issue,Reiner et al. show how the large avian cerebrum reflectsexpansion of pallial regions, which are now recognized asfunctionally comparable to mammalian cerebral cortex,and which provide the substrate for the substantial be-havioral and cognitive skills that we now know birds topossess.

Another main theme to emerge here is that of the fitbetween brain and ecological niche. Whereas all of thearticles in this issue provide informative examples of howbrain organization reflects ecological demands, the studyby Kaufman et al. (this issue) presents a highly unusualexample with their focus on the aye-aye (Daubentoniamadagascariensis). Kaufman et al. apply imaging meth-ods in conjunction with histological techniques to providethe first quantitative comparison of imaging data andfiber-stained histology in the aye-aye brain. The aye-aye isa large nocturnal prosimian with a unique ecological nicheamong primates. The aye-aye is a specialist in extractiveforaging, probing for insect larvae that lie deep within treebark (Ganzhorn and Rabesoa, 1986; Sterling, 1993, 1994).Kaufman et al. provide new data to confirm that theaye-aye has a large frontal cortex, particularly for a pro-simian. This is potentially relevant in light of the highlevel of sensorimotor intelligence thought to be associatedwith the complex foraging behavior observed in this spe-cies (Parker and Gibson, 1977; Gibson, 1986). Kaufman etal. suggest that an enlarged frontal cortex in the aye-ayecould also be associated with the need to integrate a largeamount of sensory information during foraging. In addi-tion to whole brain size and frontal cortex size, the relativevolumes of sensory structures in the aye-aye are alsoconsistent with its ecological niche as a nocturnal extrac-tive forager. For instance, the volumes of lateral genicu-late nucleus and visual striate cortex are reduced, whilethe olfactory bulb appears greatly enlarged. This patternis in direct opposition to the typical primate pattern ofenhanced vision and reduced olfaction (Allman, 2000).Therefore, through their examination of the brain of theaye-aye, Kaufman et al. provide a striking example of howbrains can deviate from generally expected phylogeneticpatterns and evolve to reflect closely the demands ofhighly specific ecological niches.

Another example of the fit between ecological demandsand brain structure in a prosimian is provided by Collinset al. (this issue) in their study on the brain of the tarsier(Tarsius spectrum). They show that the tarsier brain isunusually large and possesses a distinctly laminated pri-mary visual cortex (VI). Tarsiers also possess a large num-ber of unusual distributions of cones in the retina. Kauf-man et al. hypothesize that these features of the tarsierbrain are adaptive specializations for the behavioral de-mands of their particular niche as nocturnal predators.

Sherwood (this issue) provides yet another example ofthe relationship between brain organization on the onehand and species-specific traits on the other. Instead offocusing on physical ecological demands, however, Sh-erwood provides evidence that the sociobehavioral char-

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acteristics of various primate species can play an im-portant role in shaping neuroanatomy in addition todemands of the physical environment. In his discussionof the comparative anatomy of the facial motor nucleusin mammals, Sherwood shows how the anatomic orga-nization of the facial nerve (VII) is heavily phylogeneti-cally conserved across species but also reflects species-specific specializations in the use of facial muscles forsocial communication in the socially complex clade ofgreat apes and humans. Sherwood suggests that directneocortical connections to VII may have evolved to pro-vide voluntary control over complex facial expressionsin primates in general.

Hakeem et al. (this issue) provide the first imaging-based description of the elephant brain (Loxodonta afri-cana) and attempt to understand brain structure in thisspecies both in a comparative context and from an ecolog-ical and behavioral perspective. The authors use compar-isons of elephant brains and cetacean brains to control forthe role of scaling factors in the features that emerge fromtheir analysis. The authors find that the elephant brain issimilar to the cetacean brain in degree of cortical foldingbut differs from cetacean brains in major ways. For in-stance, elephant brains conform to the same scalingtrends in relative corpus callosum size as primates whilecetaceans possess a deviantly small corpus callosum. Also,unlike cetaceans, elephants possess a substantial hip-pocampus with a unique dorsal extension. The authorssuggest that the large hippocampus is related to theirprodigious long-term memory but further work needs to bedone to examine this idea.

Finally, Peichl (this issue) provides an overview of thediversity of photoreceptors in mammals and attempts toconsider them within the framework of adaptation to par-ticular environments and lifestyles. Peichl shows thatthere seems to be a basic plan or bauplan in photoreceptorsystems across mammals that is shaped by species-spe-cific characteristics. However, this study also serves as animportant reminder that the relationship between neuro-logical structure and ecology/environment is not alwaysstraightforward and apparent.

Another important theme that emerges from this issueis that of evolution as a detective story. All of the studiesin this issue deal with evolutionary issues and questionsand it is obviously difficult to imagine any useful compar-ative neuroanatomy without relating it to evolution andphylogeny. Several of the studies, however, are particu-larly salient examples of the authors’ efforts to piece to-gether how the evolution of a particular neurobehavioralsystem unfolded over time. For instance, Gannon et al.(this issue) tackle the evolutionary origin of human lan-guage areas in the brain. They use the comparative ap-proach to investigate the anatomic representation of var-ious language-related brain regions, in this case theplanum parietale, in humans and other primates. Theauthors provide evidence that the neuroanatomical pre-cursors of language exist in great apes. Using the logic ofthe comparative approach, they attempt to reconstruct theevolution of language in hominids from a shared neuro-anatomical substrate in the ancestor of great apes andhumans.

In complement with the approach by Gannon et al.,Hunt et al. (this issue) provide an example of how exper-imental assaying of sensory systems can elucidate mech-anisms underlying brain development, plasticity, and, ul-

timately, evolution. Hunt et al. use neuroanatomicaltracers to examine the retinofugal pathway in normal andcongenitally deaf mice. They show that aberrant visualinputs to auditory structures in the deaf mice indicatesubstantial cortical plasticity and reorganization in orderto optimize the suite of sensory information utilized bythe mouse. These kinds of compensatory anatomicalchanges in the brain might elucidate the neuromechanis-tic substrate of ontogenetic and phylogenetic-evolutionarychanges.

Another example in uncovering evolutionary pat-terns, especially as it relates to phylogenetic relation-ships, is found in Hof and Sherwood (this issue). In spiteof many cytoarchitectural studies, the molecularmakeup of the various populations of neurons in thecerebral cortex and other brain structures has not beenanalyzed systematically in an evolutionary context. Hofand Sherwood summarize observations made in a largeseries of species representative of the major subdivi-sions of mammals on the morphologic characteristicsand distribution of calcium-binding proteins and non-phosphorylated neurofilament protein that are knownmarkers of specific subpopulations of excitatory andinhibitory neurons in the neocortex of these species. Thedistribution of these neurochemical markers revealsspecies- and order-specific patterns that permit assess-ment of neuronal morphomolecular specialization, andcell type distribution the neocortex, as representative ofderived or ancestral features and their use in definingtaxonomic affinities among species. Independent of thediversity in morphologic and cellular organization thatoccurred during mammalian neocortical evolution, suchpatterns reveal several associations among taxa thatclosely match their phylogenetic relationships.

CONCLUSIONOne of the major objectives of comparative neuroanat-

omy is to use the range of data made available by natureto extract the higher-order commonalities across brainsthat may lead us to uncovering general higher-orderprinciples of brain and behavioral evolution. The arti-cles in this issue reflect the fact that truly comparativework can provide the potential to uncover those princi-ples. Eventually we may possess a deeper understand-ing of the relationship between brains, behavior, andenvironment.

ACKNOWLEDGMENTSThe authors thank the participants of the symposium

on the evolution of neurobiological specializations in mam-mals held at the American Association of Anatomists an-nual meeting in San Diego in April 2005. They also ac-knowledge Editor Roger R. Markwald and ManagingEditor David Bernanke. Special thanks to Associate Edi-tor Jeffrey Laitman for his enduring support for this sym-posium and special issue and his valuable advice andassistance in bringing the issue to fruition.

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