The evolution of cerebrotypes in birds

Multivariate analyses of brain composition in mammals, amphibians and fish have revealed the evolution of 'cerebrotypes' that reflect specific niches and/or clades. Here, we present the first demonstration of similar cerebrotypes in birds. Using principal component analysis and hierarchical clustering methods to analyze a data set of 67 species, we demonstrate that five main cerebrotypes can be recognized. One type is dominated by galliforms and pigeons, among other species, that all share relatively large brainstems, but can be further differentiated by the proportional size of the cerebellum and telencephalic regions. The second cerebrotype contains a range of species that all share relatively large cerebellar and small nidopallial volumes. A third type is composed of two species, the tawny frogmouth (Podargus strigoides) and an owl, both of which share extremely large Wulst volumes. Parrots and passerines, the principal members of the fourth group, possess much larger nidopallial, mesopallial and striatopallidal proportions than the other groups. The fifth cerebrotype contains species such as raptors and waterfowl that are not found at the extremes for any of the brain regions and could therefore be classified as 'generalist' brains. Overall, the clustering of species does not directly reflect the phylogenetic relationships among species, but there is a tendency for species within an order to clump together. There may also be a weak relationship between cerebrotype and developmental differences, but two of the main clusters contained species with both altricial and precocial developmental patterns. As a whole, the groupings do agree with behavioral and ecological similarities among species. Most notably, species that share similarities in locomotor behavior, mode of prey capture or cognitive ability are clustered together. The relationship between cerebrotype and behavior/ecology in birds suggests that future comparative studies of brain-behavior relationships will benefit from adopting a multivariate approach.     

Maternal effects and the evolution of brain size in birds: overlooked developmental constraints

A central dogma for the evolution of brain size posits that the maintenance of large brains incurs developmental costs, because they need prolonged periods to grow during the early ontogeny. Such constraints are supported by the interspecific relationship between ontological differences and relative brain size in birds and mammals. Given that mothers can strongly influence the development of the offspring via maternal effects that potentially involve substances essential for growing brains, we argue that such effects may represent an important but overlooked component of developmental constraints on brain size. To demonstrate the importance of maternal effect on the evolution of brains, we investigated the interspecific relationship between relative brain size and maternal effects, as reflected by yolk testosterone, carotenoids, and vitamins A and E in a phylogenetic study of birds. Females of species with relatively large brains invested more in eggs in terms of testosterone and vitamin E than females of species with small brains. The effects of carotenoid and vitamin A levels on the evolution of relative brain size were weaker and non-significant. The association between relative brain size and yolk testosterone was curvilinear, suggesting that very high testosterone levels can be suppressive. However, at least in moderate physiological ranges, the positive relationship between components of maternal effects and relative brain size may imply one aspect of developmental costs of large brains. The relationship between vitamin E and relative brain size was weakened when we controlled for developmental mode, and thus the effect of this antioxidant may be indirect. Testosterone-enhanced neurogenesis and vitamin E-mediated defence against oxidative stress may have key functions when the brain of the embryo develops, with evolutionary consequences for relative brain size.     

Evolution of brain size in the Palaeognath lineage, with an emphasis on new zealand ratites

Brain size in vertebrates varies principally with body size. Although many studies have examined the variation of brain size in birds, there is little information on Palaeognaths, which include the ratite lineage of kiwi, emu, ostrich and extinct moa, as well as the tinamous. Therefore, we set out to determine to what extent the evolution of brain size in Palaeognaths parallels that of other birds, i.e., Neognaths, by analyzing the variation in the relative sizes of the brain and cerebral hemispheres of several species of ratites and tinamous. Our results indicate that the Palaeognaths possess relatively smaller brains and cerebral hemispheres than the Neognaths, with the exception of the kiwi radiation (Apteryx spp.). The external morphology and relatively large size of the brain of Apteryx, as well as the relatively large size of its telencephalon, contrast with other Palaeognaths, including two species of historically sympatric moa, suggesting that unique selective pressures towards increasing brain size accompanied the evolution of kiwi. Indeed, the size of the cerebral hemispheres with respect to total brain size of kiwi is rivaled only by a handful of parrots and songbirds, despite a lack of evidence of any advanced behavioral/cognitive abilities such as those reported for parrots and crows. In addition, the enlargement in brain and telencephalon size of the kiwi occurs despite the fact that this is a precocial bird. These findings form an exception to, and hence challenge, the current rules that govern changes in relative brain size in birds.     

Behavioral flexibility positively correlated with relative brain volume in predatory bats

We investigated the potential relationships between foraging strategies and relative brain and brain region volumes in predatory (animal-eating) echolocating bats. The species we considered represent the ancestral state for the order and approximately 70% of living bat species. The two dominant foraging strategies used by echolocating predatory bats are substrate-gleaning (taking prey from surfaces) and aerial hawking (taking airborne prey). We used species-specific behavioral, morphological, and ecological data to classify each of 59 predatory species as one of the following: (1) ground gleaning, (2) behaviorally flexible (i.e., known to both glean and hawk prey), (3) clutter tolerant aerial hawking, or (4) open-space aerial hawking. In analyses using both species level data and phylogenetically independent contrasts, relative brain size was larger in behaviorally flexible species. Further, relative neocortex volume was significantly reduced in bats that aerially hawk prey primarily in open spaces. Conversely, our foraging behavior index did not account for variability in hippocampus and inferior colliculus volume and we discuss these results in the context of past research.     

Brain organization and specialization in deep-sea chondrichthyans

Chondrichthyans occupy a basal place in vertebrate evolution and offer a relatively unexplored opportunity to study the evolution of vertebrate brains. This study examines the brain morphology of 22 species of deep-sea sharks and holocephalans, in relation to both phylogeny and ecology. Both relative brain size (expressed as residuals) and the relative development of the five major brain areas (telencephalon, diencephalon, mesencephalon, cerebellum, and medulla) were assessed. The cerebellar-like structures, which receive projections from the electroreceptive and lateral line organs, were also examined as a discrete part of the medulla. Although the species examined spanned three major chondrichthyan groupings (Squalomorphii, Galeomorphii, Holocephali), brain size and the relative development of the major brain areas did not track phylogenetic groupings. Rather, a hierarchical cluster analysis performed on the deep-sea sharks and holocephalans shows that these species all share the common characteristics of a relatively reduced telencephalon and smooth cerebellar corpus, as well as extreme relative enlargement of the medulla, specifically the cerebellar-like lobes. Although this study was not a functional analysis, it provides evidence that brain variation in deep-sea chondichthyans shows adaptive patterns in addition to underlying phylogenetic patterns, and that particular brain patterns might be interpreted as 'cerebrotypes'.     

Not all brains are made the same: new views on brain scaling in evolution

Evolution has generated mammalian brains that vary by a factor of over 100,000 in mass. Despite such tremendous diversity, brain scaling in mammalian evolution has tacitly been considered a homogeneous phenomenon in terms of numbers of neurons, neuronal density, and the ratio between glial and neuronal cells, with brains of different sizes viewed as similarly scaled-up or scaled-down versions of a shared basic plan. According to this traditional view, larger brains would have more neurons, smaller neuronal densities (and, hence, larger neurons), and larger glia/neuron ratios than smaller brains. Larger brains would also have a cerebellum that maintains its relative size constant and a cerebral cortex that becomes relatively larger to the point that brain evolution is often equated with cerebral cortical expansion. Here I review our recent data on the numbers of neuronal and nonneuronal cells that compose the brains of 28 mammalian species belonging to 3 large clades (Eulipotyphla, Glires, and Primata, plus the related Scandentia) and show that, contrary to the traditional notion of shared brain scaling, both the cerebral cortex and the cerebellum scale in size as clade-specific functions of their numbers of neurons. As a consequence, neuronal density and the glia/neuron ratio do not scale universally with structure mass and, most importantly, mammalian brains of a similar size can hold very different numbers of neurons. Remarkably, the increased relative size of the cerebral cortex in larger brains does not reflect an increased relative concentration of neurons in the structure. Instead, the cerebral cortex and cerebellum appear to gain neurons coordinately across mammalian species. Brain scaling in evolution, hence, should no longer be equated with an increasing dominance of the cerebral cortex but rather with the concerted addition of neurons to both the cerebral cortex and the cerebellum. Strikingly, all brains appear to gain nonneuronal cells in a similar fashion, with relatively constant nonneuronal cell densities. As a result, while brain size can no longer be considered a proxy for the number of brain neurons across mammalian brains in general, it is actually a very good proxy for the number of nonneuronal cells in the brain. Together, these data point to developmental mechanisms that underlie evolutionary changes in brain size in mammals: while the rules that determine how neurons are added to the brain during development have been largely free to vary in mammalian evolution across clades, the rules that determine how other cells are added in development have been mostly constrained and to this day remain largely similar both across brain structures and across mammalian groups.     

Interspecific allometry of the brain and brain regions in parrots (psittaciformes): comparisons with other birds and primates

Despite significant progress in understanding the evolution of the mammalian brain, relatively little is known of the patterns of evolutionary change in the avian brain. In particular, statements regarding which avian taxa have relatively larger brains and brain regions are based on small sample sizes and statistical analyses are generally lacking. We tested whether psittaciforms (parrots, cockatoos and lorikeets) have larger brains and forebrains than other birds using both conventional and phylogenetically based methods. In addition, we compared the psittaciforms to primates to determine if cognitive similarities between the two groups were reflected by similarities in brain and telencephalic volumes. Overall, psittaciforms have relatively larger brains and telencephala than most other non-passerine orders. No significant difference in relative brain or telencephalic volume was detected between psittaciforms and passerines. Comparisons of other brain region sizes between psittaciforms and other birds, however, exhibited conflicting results depending upon whether body mass or a brain volume remainder (total brain volume - brain region volume) was used as a scaling variable. When compared to primates, psittaciforms possessed similar relative brain and telencephalic volumes. The only exception to this was that in some analyses psittaciforms had significantly larger telencephala than primates of similar brain volume. The results therefore provide empirical evidence for previous claims that psittaciforms possess relatively large brains and telencephala. Despite the variability in the results, it is clear that psittaciforms tend to possess large brains and telencephala relative to non-passerines and are similar to primates in this regard. Although it could be suggested that this reflects the advanced cognitive abilities of psittaciforms, similar studies performed in corvids and other avian taxa will be required before this claim can be made with any certainty.     

Microchiropterans have a diminutive cerebral cortex,not an enlarged cerebellum,compared to megachiropterans and other mammals

Small echolocating bats are set apart from most other mammals by their relatively large cerebellum, a feature that has been associated to echolocation, as it is presumed to indicate a relatively enlarged number of neurons in the cerebellum in comparison to other brain structures. Here we quantify the neuronal composition of the cerebral cortex, cerebellum and remaining brain structures of seven species of large Pteropodid bats (formerly classified as megachiropterans), one of which echolocates, and six species of small bats (formerly classified as microchiropterans), all of which echolocate. This chiropteran data is compared to 60 mammalian species in our dataset to determine whether the relatively large cerebellum of the small echolocating bats, and possibly that of the echolocating Pteropodid, contains a relatively enlarged number of neurons. We find no evidence that the distribution of neurons differs between microchiropterans and megachiropterans, but our data indicate that microchiropterans, like the smallest shrew in our dataset, have diminutive cerebral cortices, which makes the cerebellum appear relatively large. We propose that, in agreement with the diminutive brain size of the earliest fossil mammals, this is a plesiomorphic, not a derived, feature of microchiropteran brains. The results of this study also reveal important neural characteristics related to the phylogenetic affinities and relationships of the chiropterans.     

Brain composition in Heliconius butterflies,posteclosion growth and experience‐dependent neuropil plasticity

Behavioral and sensory adaptations are often reflected in the differential expansion of brain components. These volumetric differences represent changes in cell number, size, and/or connectivity, which may denote changes in the functional and evolutionary relationships between different brain regions, and between brain composition and behavioral ecology. Here we describe the brain composition of two species of Heliconius butterflies, a long‐standing study system for investigating ecological adaptation and speciation. We confirm a previous report of a striking volumetric expansion of the mushroom body, and explore patterns of differential posteclosion and experience‐dependent plasticity between different brain regions. This analysis uncovers age‐ and experience‐dependent posteclosion mushroom body growth comparable to that in foraging Hymenoptera, but also identifies plasticity in several other neuropils. An interspecific analysis indicates that Heliconius display a remarkably large investment in mushroom bodies for a lepidopteran, and indeed rank highly compared to other insects. Our analyses lay the foundation for future comparative and experimental analyses that will establish Heliconius as a valuable case study in evolutionary neurobiology. J. Comp. Neurol. 524:1747–1769, 2016. © 2016 Wiley Periodicals, Inc.     

Comparative analysis of cortical layering and supragranular layer enlargement in rodent carnivore and primate species

The mammalian cerebral cortex is composed of individual layers characterized by the cell types they contain and their afferent and efferent connections. The current study examined the raw, and size-normalized, laminar thicknesses in three cortical regions (somatosensory, motor, and premotor) of fourteen species from three orders of mammals: primates, carnivores, and rodents. The proportional size of the pyramidal cell layers (supra- and infragranular) varied between orders but was similar within orders despite wide variance in absolute cortical thickness. Further, supragranular layer thickness was largest in primates (46 +/- 3 percent), followed by carnivores (36 +/- 3 percent), and then rodents (19 +/- 4 percent), suggesting a distinct difference in the proportion of cortex devoted to corticocortical connectivity across these orders. Although measures of supragranular layer thickness are highly correlated with measures of overall brain size, such associations are not present when independent contrasts are used to control for phylogenetic inertia. Interestingly, neurogenesis time span remains strongly associated with supragranular layer thickness despite size normalization and controlling for phylogenetic inertia. Such layering differences between orders, and similarities amongst species within an order, suggest that supragranular layer expansion may have occurred early in mammalian evolution and may be related to ontogenetic variables such as neurogenesis time span rather than measures of overall size.     

Phenotypic diversity is the cornerstone of evolution: variation in cortical field size within short-tailed opossums

Natural selection operates on phenotypic variation that exists within a population. Variable aspects of cortical organization, such as the size and connections of a cortical field, can generate differences in behavior, which is a target of natural selection. Yet studies pertaining to within-species variability in cortical organization are limited. In the present investigation, we examined variation in brain size, cortical sheet size, and primary sensory cortical field sizes in the adult short-tailed opossum (Monodelphis domestica). Within individuals, we found no significant difference between the right and left hemispheres in the overall size of the dorsolateral cortex or in primary cortical field sizes. Between individuals, we found relatively little intraspecies variation in brain weight, brain volume, and cortical sheet area for the dorsolateral neocortex and pyriform cortex; however, we observed a large degree of variability in body weight and primary sensory cortical field size, as defined by myeloarchitecture. Further, we found that the size of each cortical field correlated with the size of the other cortical fields as well as with the total size of the dorsolateral cortex. Here we discuss the possible sources of variation and examine the relationship between cortical field size and sensory processing abilities and behaviors across species. Since behavior is the target of natural selection, variation in cortical field size across individuals may supply the raw material necessary for cortical field evolution.     

Brains, bodies and metabolism

The interrelationship of brain and body sizes has been the subject of investigations for over a hundred years. These studies have demonstrated that variation in brain weights is much smaller than that in body weights; consequently, scaling studies are ones of negative allometry. Furthermore, the variability in brain weight is greater when comparisons are between species rather than among individuals of the same species, and the degree of variability in brain size differs among orders. The largest shifts in brain sizes relative to changes in body weights are found when comparing different ontogenetic stages. Debate continues as to the importance of metabolism in determining the interrelationship of brain-body weights for interpreting differences in relative brain size. Although past advances in the study of brain-body size associations have come by increasing the size of the data bases and by improved statistical analyses, the recent utilization of transgenic animals may provide new insights into the mechanism of this association.     

Evolutionary convergence in nervous systems: insights from comparative phylogenetic studies

Over the past 20 years, cladistic analyses have revolutionized our understanding of brain evolution by demonstrating that many structures, some of which had previously been assumed to be homologous, have evolved many times independently. These and other studies demonstrate that evolutionary convergence in brain anatomy and function is widespread. Although there are relatively few neuroethological studies in which brain and behavior have be studied within an evolutionary framework, three relatively well studied cases are reviewed here: electric communication among gymnotiform and mormyriform fishes, prey capture among frogs, and sound localization among owls. These three examples reveal similar patterns of brain evolution. First, it is clear that novel abilities have evolved many times independently in taxa whose common ancestors lack these abilities. Second, it is apparent that small changes in neural pathways can lead to dramatic changes in an organism's abilities. Brain evolution at this small scale is quite common. The behavioral importance of small scale changes on one hand, and the pervasiveness of convergent evolution on the other, have several implications for understanding brain evolution. First, similar abilities may be conferred by convergent rather than homologous circuits, even among closely related species. Furthermore, closely related species may use the same information in different ways, or they may use different means to obtain the same information. One reason that convergence is so common in the biological world may be that the evolutionary appearance of novel functions is associated with constraints, for example in the algorithms used for a given neural computation. Convergence in functional organization may thus reveal basic design features of neural circuits in species that possess unique evolutionary histories but use similar algorithms to solve basic computational problems.     

Relative eye size in elasmobranchs

Variation in relative eye size was investigated in a sample of 46 species of elasmobranch, 32 species of sharks and 14 species of batoids (skates and rays). To get a measure of eye size relative to body size, eye axial diameter was scaled with body mass using least-squares linear regression, using both raw species data, where species are treated as independent data points, and phylogenetically independent contrasts. Residual values calculated for each species, using the regression equations describing these scaling relationships, were then used as a measure of relative eye size. Relative and absolute eye size varies considerably in elasmobranchs, although sharks have significantly relatively larger eyes than batoids. The sharks with the relatively largest eyes are oceanic species; either pelagic sharks that move between the epipelagic (0-200 m) and 'upper' mesopelagic (200-600 m) zones, or benthic and benthopelagic species that live in the mesopelagic (200-1,000 m) and, to a lesser extent, bathypelagic (1,000-4,000 m) zones. The elasmobranchs with the relatively smallest eyes tend to be coastal, often benthic, batoids and sharks. Active benthopelagic and pelagic species, which prey on active, mobile prey also have relatively larger eyes than more sluggish, benthic elasmobranchs that feed on more sedentary prey such as benthic invertebrates. A significant positive correlation was found between absolute eye size and relative eye size, but some very large sharks, such as Carcharodon carcharias have absolutely large eyes, but have relatively small eyes in relation to body mass.     

Is brain size an ecological variable?

Brain size increases with body weight -but the relationship between the two variables is not a simple one. Even when body size is taken into account, some species (for example, man) have relatively large brains, whilst for others brain sizes are smaller than expected. In this article Georgina Mace and colleagues show that ecological niche, especially diet, can account for much of this residual variation.     

Anseriform brain and its parts versus taxonomic and ecological categories

The size of the brain and its macro-anatomical parts in 206 birds representing 19 anseriform species and 4 tribes (Anserini, Anatini, Aythyini and Mergini) was the subject of a comparative analysis. The comparisons involved two aspects: taxonomic (differences among species within tribes and differences among tribes) and ecological (diet composition: vegetation, invertebrates, or fish and the foraging mode: browsing, dabbling, shallow diving, and deep diving). The relative size of the encephalon (E) and its parts (optic tectum, OT; cerebellum, C; brain stem, BS; hemispheres, H) were described using appropriate indices. Five of them, called the cerebral-body indices (E/BW, OT/BW, C/BW, BS/BW, H/BW), involved a ratio between the weight of E or its parts and that of the body (BW). Four intracerebral indices (OT/E, C/E, BS/E, H/E) and allometric equations were used as well. Almost all the indices showed a high intraspecific variability within the Anserini and Mergini; on the other hand, the intracerebral indices did not differ between the species of the Anatini and Aythyini (except for OT/E in the Aythyini). Between-tribe differences were reflected in all 9 indices. The birds feeding on different diets were found to differ in their OT/E and H/E. The herbivorous anserifom OT/E was clearly lower than that of those birds feeding on invertebrates and fish. The highest OT/E was that of the piscivorous birds. In terms of foraging mode, significant differences were revealed in 7 out of the 9 indices used (differences in OT/BW and C/BW proved non-significant). OT/E of the browsing birds was clearly lower than that of the deep diving ducks; BS/E of the browsers was much lower than that of the dabbling and shallow diving ducks. Geese and swans (browsers) showed much higher H/E compared to the deep diving sea ducks. The latter revealed the highest C/E, but significant differences were detected only in comparison with C/E of the shallow diving ducks. The taxonomic (among tribes) and ecological comparisons showed more differences in the intracerebral indices than in the cerebral-body indices.     

Brain size and social complexity: a computed tomography study in Hyaenidae

The social brain hypothesis posits that the demands of living in complex social groups require increased neural processing, and that this underlies the expansion of brain areas involved in mediation of complex social behavior. However, much of the support for the social brain hypothesis is derived from comparative studies in primates. If large brains evolved as a result of selection pressures imposed by life within complex societies, as the social brain hypothesis predicts, then gregarious nonprimate species should possess large brains and exhibit comparable expansion of brain areas mediating social behavior. Our purpose here was to test a prediction of the social brain hypothesis-- that increased brain size is related to social complexity --by examining species in the carnivore family Hyaenidae. Hyaenidae contains 4 extant species that span a spectrum of social complexity: the aardwolf (Proteles cristata) is solitary during the nonbreeding season, and forms monogamous pairs during the breeding season; the striped hyena (Hyaena hyaena) lives solitarily or in small groups; the brown hyena (Parahyaena brunnea) lives in groups of up to 14 individuals; and the spotted hyena (Crocuta crocuta) lives in complex hierarchically organized groups containing up to 90 animals. Computed tomography was used to create three-dimensional endocasts based on serial analysis of coronal sections of the adult endocranium. The largest brain volume, relative to body size, is found in the spotted hyena. We found no significant variation in relative brain volume among striped hyenas, brown hyenas, and aardwolves. The spotted hyena also possesses a larger anterior cerebrum volume relative to total brain volume than is found in the other hyena species; this region is composed primarily of frontal cortex. These data are consistent with the idea that expansion of the frontal cortex is driven by the demands of processing cognitive information associated with complex social lives, but other factors may drive the evolution of large brains in hyaenids.     

An allometric analysis of the frequency of hippocampal theta: the significance of brain metabolic rate

The dominant frequency of hippocampal rhythmic slow activity (RSA) is known to differ among species, even under similar experimental conditions. The cause of these species differences has not yet been identified. In this paper it is shown that RSA frequency is allometrically related to brain size for the 9 mammalian species for which data are available. It is further shown that the relationship between brain size and RSA frequency is similar to the relationship between brain size and specific brain metabolic rate. Based on these and other relationships, it is suggested that differences in the firing frequencies of the neuronal pacemakers underlying the generation of RSA reflect differences in specific brain metabolic rate, both within and among species.     

Weak correlations between body height and several brain metrics in healthy elderly subjects

The question whether body height is related to different brain size measures has recently gained renewed interest as some studies have reported that body height correlates with intelligence and several brain size measures. In this study, we re‐evaluated this question by examining the relationship between body height and different brain size measures including intracranial volume, total brain volume, total cortical surface area, total cortical volume, volume of normal‐appearing white matter, white matter hyperintensity, cortical surface area, cortical thickness, subcortical grey matter volume, cerebellar cortex and cerebellar white matter in a relatively large sample (n = 216) of physically and cognitively healthy elderly subjects (mean age 71 years, age range 65–85 years). We identified small correlations (r = .11–.19) between body height and seven out of 10 brain metrics (total brain volume, cortical surface area, cortical volume, subcortical volume, normal‐appearing white matter volume and cerebellar grey as well as white matter volumes) when controlling for sex and age. Based on these small relationships between body height and various brain size measures, we discuss the possible reasons and theoretical problems for these small relationships.     

Relative medial and dorsal cortex volume in relation to foraging ecology in congeneric lizards

The need to locate distributed resources such as mates, food, and nests is correlated with an enlarged hippocampus in many mammalian and avian species. This correlation is believed to be a consequence of selection for spatial ability. Little is known about how such ecological needs affect non-mammalian, non-avian species. In lizards, the putative hippocampal homologues are the dorsal cortex (DC) and medial cortex (MC). We examined the relationship between foraging ecology and the size of the DC and MC in congeneric male lizards. We predicted based on the mammalian and avian literature that Acanthodactylus boskianus, an active forager that captures clumped, immobile prey would have a larger MC and DC than A. scutellatus, a sit-and-wait predator, that captures mobile prey. Our previous behavioral studies showed that A. boskianus did not differ from A. scutellatus on a spatial task but that A. boskianus was significantly better at the reversal of a visual discrimination, another task that is hippocampally dependent in mammals. In the current study, we found that, relative to telencephalon volume, the MC and DC were larger in the active forager whereas a control region, the lateral, olfactory, cortex, was similar in size between species. The current anatomical results suggest that MC and DC size is related to active foraging in lizards and, along with our previous behavioral studies, show that it is possible for this relationship to occur in the absence of evidence for species differences in spatial memory. Copyright (R) 2000 S.Karger AG, Basel