Mammalian and avian neuroanatomy and the question of consciousness in birds

Some birds display behavior reminiscent of the sophisticated cognition and higher levels of consciousness usually associated with mammals, including the ability to fashion tools and to learn vocal sequences. It is thus important to ask what neuroanatomical attributes these taxonomic classes have in common and whether there are nevertheless significant differences. While the underlying brain structures of birds and mammals are remarkably similar in many respects, including high brain-body ratios and many aspects of brain circuitry, the architectural arrangements of neurons, particularly in the pallium, show marked dissimilarity. The neural substrate for complex cognitive functions that are associated with higher-level consciousness in mammals and birds alike may thus be based on patterns of circuitry rather than on local architectural constraints. In contrast, the corresponding circuits in reptiles are substantially less elaborated, with some components actually lacking, and in amphibian brains, the major thalamopallial circuits involving sensory relay nuclei are conspicuously absent. On the basis of these criteria, the potential for higher-level consciousness in these taxa appears to be lower than in birds and mammals.     

Reptilian Cognition: A More Complex Picture via Integration of Neurological Mechanisms,Behavioral Constraints,and Evolutionary Context

Unlike birds and mammals, reptiles are commonly thought to possess only the most rudimentary means of interacting with their environments, reflexively responding to sensory information to the near exclusion of higher cognitive function. However, reptilian brains, though structurally somewhat different from those of mammals and birds, use many of the same cellular and molecular processes to support complex behaviors in homologous brain regions. Here, the neurological mechanisms supporting reptilian cognition are reviewed, focusing specifically on spatial cognition and the hippocampus. These processes are compared to those seen in mammals and birds within an ecologically and evolutionarily relevant context. By viewing reptilian cognition through an integrative framework, a more robust understanding of reptile cognition is gleaned. Doing so yields a broader view of the evolutionarily conserved molecular and cellular mechanisms that underlie cognitive function and a better understanding of the factors that led to the evolution of complex cognition.     

New data on the brain and cognitive abilities of birds

New evidence of functional analogies and homologies of avian and mammalian brains is presented, as is a revised nomenclature of the most important brain structures. Comparative characteristics of the avian brain and criteria for its progressive development in the phylogeny have been considered. We studied the possibility to use Portmann??s index as one of the indicators of brain development in different avian species. We substantiated the necessity to chose for investigation new sets of avian species with medium (Parus caeruleus and Loxia curvirostra) and low (Larus glaucescens) levels of brain complexity to maintain fully valuable grounds for comparing the cognitive abilities in birds. The main experimentally supported proofs of the existence of elementary thinking and some other cognitive functions in the higher birds have been reviewed. The high levels of cognitive processes that underlie the tool using ability in birds, as well as the similarity to those processes in apes, have been demonstrated from the results obtained in the first decade of the 21st century. Comparative studies on proto-instrumental activity confirmed the ability of hooded crows and ravens to find urgent solution of tool-using tasks. Although birds with a medium level of brain complexity display seemingly rational behavior, it is plausible that they use simpler rules being unable to understand the task logic. It was shown that birds of different orders with a high level of brain complexity demonstrate similar dynamics in the development of abstract concepts. Crossbills, which have a medium level of brain complexity, were able to develop the same concepts at a lower level than the corvids; whereas the seagulls and pigeons, which possess a low level of cognitive abilities, were not able to operate any abstractions and were incapable of solving other cognitive tests. The fact that corvids, parrots, and apes have similar abilities to solve some cognitive tasks supports the hypothesis of the convergent evolution of the brain and cognition in birds and primates.     

Estrogen synthetase (aromatase) immunohistochemistry reveals concordance between avian and rodent limbic systems and hypothalami

During amniote evolution, an early divergence occurred about 300 million years ago between the reptilian lines leading to the appearance of birds (anapsids) and mammals (synapsids). The different functional requirements of these vertebrate groups have involved divergent evolution of their brains. Even superficial examination reveals major anatomical differences between mammalian and avian brains, such as extensive development of the optic lobes and cerebellum in birds and a highly developed cortex in mammals. It has been nearly impossible to identify avian homologs of some mammalian brain regions by standard morphological criteria. This has long frustrated efforts at clarifying hypotheses regarding the anatomical location, field size, and regulation of brain functions shared between these two classes, despite the certainty that the principles of neurobiology apply equally at the cellular level in both groups. In an effort to remove this barrier, we have sought markers of common function that despite apparent anatomical dissimilarity, can allow recognition of homologous brain structures. We illustrate here how comparative analysis of the distribution of the steroid-metabolizing enzyme estrogen synthetase (aromatase) may help to understand the differences and similarities in the limbic system and hypothalamus of birds and mammals.     

Is Cooperative Breeding Associated With Bigger Brains? A Comparative Test in the Corvida (Passeriformes)

The cognitive demands of a social existence favour the evolution of relatively large brains and neocortices in primates. Comparable tests of sociality and brain size/structure in birds have not been performed, despite marked similarities in the social systems of birds and mammals. Here, we test whether one aspect of avian sociality, cooperative breeding, is associated with an increase in brain size across 155 species of the passeriform parvorder Corvida. Using conventional and phylogeny‐corrected statistics, we examined the correlated evolution of relative brain size and: the presence/absence of cooperative breeding, percentage of nests that are cooperative and cooperatively breeding group size. Most of the comparisons yielded non‐significant results, which suggests that cooperative breeding is not related to relative brain size in this parvorder. There are a number of potential explanations for our findings. First, changes in brain region size may be correlated with cooperative breeding without affecting overall brain size. Secondly, cooperatively breeding birds might not possess more complex social behaviour than non‐cooperatively breeding birds. Thirdly, relatively large brains might be ancestral in this parvorder. This may predispose them to evolve the range of complex behaviours found in this group, including extreme sociality. Finally, ecological and/or developmental factors might play a more significant role than social behaviour in the diversification of avian brain size. Assessing these alternatives requires more information on the neural and cognitive differences between bird species.     

Cognitive ornithology: the evolution of avian intelligence

Comparative psychologists interested in the evolution of intelligence have focused their attention on social primates, whereas birds tend to be used as models of associative learning. However, corvids and parrots, which have forebrains relatively the same size as apes, live in complex social groups and have a long developmental period before becoming independent, have demonstrated ape-like intelligence. Although, ornithologists have documented thousands of hours observing birds in their natural habitat, they have focused their attention on avian behaviour and ecology, rather than intelligence. This review discusses recent studies of avian cognition contrasting two different approaches; the anthropocentric approach and the adaptive specialization approach. It is argued that the most productive method is to combine the two approaches. This is discussed with respects to recent investigations of two supposedly unique aspects of human cognition; episodic memory and theory of mind. In reviewing the evidence for avian intelligence, corvids and parrots appear to be cognitively superior to other birds and in many cases even apes. This suggests that complex cognition has evolved in species with very different brains through a process of convergent evolution rather than shared ancestry, although the notion that birds and mammals may share common neural connectivity patterns is discussed.     

Hippocampal memory consolidation during sleep: a comparison of mammals and birds

The transition from wakefulness to sleep is marked by pronounced changes in brain activity. The brain rhythms that characterize the two main types of mammalian sleep, slow‐wave sleep (SWS) and rapid eye movement (REM) sleep, are thought to be involved in the functions of sleep. In particular, recent theories suggest that the synchronous slow‐oscillation of neocortical neuronal membrane potentials, the defining feature of SWS, is involved in processing information acquired during wakefulness. According to the Standard Model of memory consolidation, during wakefulness the hippocampus receives input from neocortical regions involved in the initial encoding of an experience and binds this information into a coherent memory trace that is then transferred to the neocortex during SWS where it is stored and integrated within preexisting memory traces. Evidence suggests that this process selectively involves direct connections from the hippocampus to the prefrontal cortex (PFC), a multimodal, high‐order association region implicated in coordinating the storage and recall of remote memories in the neocortex. The slow‐oscillation is thought to orchestrate the transfer of information from the hippocampus by temporally coupling hippocampal sharp‐wave/ripples (SWRs) and thalamocortical spindles. SWRs are synchronous bursts of hippocampal activity, during which waking neuronal firing patterns are reactivated in the hippocampus and neocortex in a coordinated manner. Thalamocortical spindles are brief 7–14 Hz oscillations that may facilitate the encoding of information reactivated during SWRs. By temporally coupling the readout of information from the hippocampus with conditions conducive to encoding in the neocortex, the slow‐oscillation is thought to mediate the transfer of information from the hippocampus to the neocortex. Although several lines of evidence are consistent with this function for mammalian SWS, it is unclear whether SWS serves a similar function in birds, the only taxonomic group other than mammals to exhibit SWS and REM sleep. Based on our review of research on avian sleep, neuroanatomy, and memory, although involved in some forms of memory consolidation, avian sleep does not appear to be involved in transferring hippocampal memories to other brain regions. Despite exhibiting the slow‐oscillation, SWRs and spindles have not been found in birds. Moreover, although birds independently evolved a brain region—the caudolateral nidopallium (NCL)—involved in performing high‐order cognitive functions similar to those performed by the PFC, direct connections between the NCL and hippocampus have not been found in birds, and evidence for the transfer of information from the hippocampus to the NCL or other extra‐hippocampal regions is lacking. Although based on the absence of evidence for various traits, collectively, these findings suggest that unlike mammalian SWS, avian SWS may not be involved in transferring memories from the hippocampus. Furthermore, it suggests that the slow‐oscillation, the defining feature of mammalian and avian SWS, may serve a more general function independent of that related to coordinating the transfer of information from the hippocampus to the PFC in mammals. Given that SWS is homeostatically regulated (a process intimately related to the slow‐oscillation) in mammals and birds, functional hypotheses linked to this process may apply to both taxonomic groups.     

The avian 'prefrontal cortex' and cognition

Both mammals and birds can flexibly organize their behavior over time. In mammals, the mental operations generating this ability are called executive functions and are associated with the prefrontal cortex. The corresponding structure in birds is the nidopallium caudolaterale. Anatomical, neurochemical, electrophysiological and behavioral studies show these structures to be highly similar. The avian forebrain displays no lamination that corresponds to the mammalian neocortex, hence lamination does not seem to be a requirement for higher cognitive functions. Because all other aspects of the neural architecture of the mammalian and the avian prefrontal areas are extremely comparable, the freedom to create different neural architectures that generate prefrontal functions seems to be very limited.     

Avian brain evolution: new data from Palaeogene birds (Lower Eocene) from England

Investigation of how the avian brain evolved to its present state is informative for studies of the theropod–bird transition, and as a parallel to mammalian brain evolution. Neurological anatomy in fossil bird species can be inferred from endocranial casts, but such endocasts are rare. Here, we use computed tomographic analysis to determine the state of brain anatomy in two marine birds from the Lower Eocene London Clay Formation of England. The brains of Odontopteryx (Odontopterygiformes) and Prophaethon (Pelecaniformes) are remarkably similar to those of extant seabirds, and probably possessed similar somatosensory and motor capabilities. Each virtual endocast exhibits a degree of telencephalic expansion comparable to living avian species. However, the eminentia sagittalis (wulst), a feature characteristic of all living birds, is poorly developed. Our findings support the conclusion that much of the telencephalic expansion of modern birds was complete by the end of the Mesozoic, but that overall telencephalic volume has increased throughout the Cenozoic through dorsal expansion of the eminentia sagittalis. We suggest that improvements in cognition relating to telencephalic expansion may have provided neornithine avian clades with an advantage over archaic lineages at the Cretaceous–Tertiary boundary, explaining their survival and rapid diversification in the Cenozoic. © 2009 The Natural History Museum. Journal compilation © 2009 The Linnean Society of London, Zoological Journal of the Linnean Society, 2009, 155 , 198–219.     

Longevity is associated with relative brain size in birds

Brain size of vertebrates has long been recognized to evolve in close association with basic life‐history traits, including lifespan. According to the cognitive buffer hypothesis, large brains facilitate the construction of behavioral responses against novel socioecological challenges through general cognitive processes, which should reduce mortality and increase lifespan. While the occurrence of brain size–lifespan correlation has been well documented in mammals, much less evidence exists for a robust link between brain size and longevity in birds. The aim of this study was to use phylogenetically controlled comparative approach to test for the relationship between brain size and longevity among 384 avian species from 23 orders. We used maximum lifespan and maximum reproductive lifespan as the measures of longevity and accounted for a set of possible confounding effects, such as allometry, sampling effort, geographic patterns, and life‐history components (clutch size, incubation length, and mode of development). We found that both measures of longevity positively correlated with relative (residual) brain size. We also showed that major diversification of brain size preceded diversification of longevity in avian evolution. In contrast to previous findings, the effect of brain size on longevity was consistent across lineages with different development patterns, although the relatively low strength of this correlation could likely be attributed to the ubiquity of allomaternal care associated with the altricial mode of development. Our study indicates that the positive relationship between brain size and longevity in birds may be more general than previously thought.     

The allometric approach to species differences in brain size

Allometric methods can be used to test quantitative theories of the relationship between brain size and body size across species, and to search for ecological, behavioural, life history, and ontogenetic correlates of brain size. Brain size scales with an allometric exponent of around 0.75 against body size across mammals, but is closer to 0.56 for birds and for reptiles. The slope of the allometric line often varies depending upon the taxonomic level of analysis. However, this phenomenon, at least in mammals, may be a statistical artifact. Brain size for a given body size (relative brain size) varies among orders in birds and mammals, and some dietary associations with relative brain size have been found in particular taxa. Developmental status at birth is the most consistent correlate of relative brain size: precocial neonates have larger brains for a given maternal size than altricial neonates in both birds and mammals. Altricial neonates, however, have more brain growth following birth, and in birds also have larger relative adult brain sizes. Energetic explanations for differences in neonatal brain growth, although attractive on theoretical grounds, have largely failed to stand up to empirical tests.     

Assessing arboreal adaptations of bird antecedents: testing the ecological setting of the origin of the avian flight stroke

The origin of avian flight is a classic macroevolutionary transition with research spanning over a century. Two competing models explaining this locomotory transition have been discussed for decades: ground up versus trees down. Although it is impossible to directly test either of these theories, it is possible to test one of the requirements for the trees-down model, that of an arboreal paravian. We test for arboreality in non-avian theropods and early birds with comparisons to extant avian, mammalian, and reptilian scansors and climbers using a comprehensive set of morphological characters. Non-avian theropods, including the small, feathered deinonychosaurs, and Archaeopteryx, consistently and significantly cluster with fully terrestrial extant mammals and ground-based birds, such as ratites. Basal birds, more advanced than Archaeopteryx, cluster with extant perching ground-foraging birds. Evolutionary trends immediately prior to the origin of birds indicate skeletal adaptations opposite that expected for arboreal climbers. Results reject an arboreal capacity for the avian stem lineage, thus lending no support for the trees-down model. Support for a fully terrestrial ecology and origin of the avian flight stroke has broad implications for the origin of powered flight for this clade. A terrestrial origin for the avian flight stroke challenges the need for an intermediate gliding phase, presents the best resolved series of the evolution of vertebrate powered flight, and may differ fundamentally from the origin of bat and pterosaur flight, whose antecedents have been postulated to have been arboreal and gliding.     

Evolutionary relationships among the Schistosomatidae (Platyhelminthes:Digenea) and an Asian origin for Schistosoma

Schistosome blood flukes parasitize birds, mammals, and crocodilians and are responsible for causing one of the great neglected diseases of humanity, schistosomiasis. A phylogenetic study of 10 schistosome genera using approximately 1,100 bases of the large subunit of the nuclear ribosomal gene complex revealed 2 major clades. One clade is entirely mammalian and includes the genera Schistosoma and Orientobilharzia. A close examination of relationships in this group suggests that the medically important Schistosoma arose in Asia and not in Africa as generally presumed and is paraphyletic. The second clade is primarily avian, consisting of 6 genera of exclusively avian parasites and 2 genera of North American mammal flukes. These results indicate a secondary host capture of mammals on the North American continent. This study provides little evidence concerning the ancestral molluscan or vertebrate schistosome host but does demonstrate that host switching has been an important feature of schistosome evolution. Evidence also indicates that the reduced sexual dimorphism characteristic of some avian schistosomes is derived evolutionarily.     

Cytochrome b evolution in birds and mammals: an evaluation of the avian constraint hypothesis.

Patterns of molecular evolution in birds have long been considered anomalous. Compared with other vertebrates, birds have reduced levels of genetic divergence between groups of similar taxonomic ranks for a variety of nuclear and mitochondrial markers. This observation led to the avian constraint hypothesis, which identifies increased functional constraint on avian proteins as the cause for the reduction in genetic divergence. Subsequent investigations provided additional support for the avian constraint hypothesis when rates of molecular evolution were found to be slower in birds than in mammals in a variety of independent calibrations. It is possible to test the avian constraint hypothesis as an explanation for this avian slowdown by comparing DNA sequence data from protein-coding regions in birds and homologous regions in mammals. The increased selective constraints should lead to a reduction in the proportion of amino acid replacement substitutions. To test for such a decrease, we calculated the numbers of amino acid replacement substitutions per replacement site (dN) and silent substitutions per silent site (dS) for the complete mitochondrial cytochrome b gene using 38 avian and 43 mammalian comparisons that were phylogenetically independent. We find that dN/dS is significantly smaller in birds than in mammals. This difference cannot be explained by differences in codon bias affecting dS values. We suggest that the avian slowdown can be explained, at least in part, by a decreased tolerance for amino acid substitutions in avian species relative to mammalian species.     

The compositional patterns of the avian genomes and their evolutionary implications

The compositional distributions of large (main-band) DNA fragments from eight birds belonging to eight different orders (including both paleognathous and neognathous species) are very broad and extremely close to each other. These findings, which are paralleled by the compositional similarity of homologous coding sequences and their codon positions, support the idea that birds are a monophyletic group.The compositional distribution of third-codon positions of genes from chicken, the only avian species for which a relatively large number of coding sequences is known, is very broad and bimodal, the minor GC-richer peak reaching 100% GC. The very high compositional heterogeneity of avian genomes is accompanied (as in the case of mammalian genomes) by a very high speciation rate compared to cold-blooded vertebrates which are characterized by genomes that are much less heterogeneous. The higher GC levels attained by avian compared to mammalian genomes might be correlated with the higher body temperature (41–43°C) of birds compared to mammals (37°C).A comparison of GC levels of coding sequences and codon positions from man and chicken revealed very close average GC levels and standard deviations. Homologous coding sequences and codon positions from man and chicken showed a surprisingly high degree of compositional similarity which was, however, higher for GC-poor than for GC-rich sequences. This indicates that GC-poor isochores of warm-blooded vertebrates reflect the composition of the isochores of the genome of the common reptilian ancestor of mammals and birds, which underwent only a small compositional change at the transition from cold- to warm-blooded vertebrates. In contrast, the GC-rich isochores of birds and mammals are the result of large compositional changes at the same evolutionary transition, where were in part different in the two classes of warm-blooded vertebrates.Correspondence to: G. Bernaadi     

Avian evolution: from Darwin's finches to a new way of thinking about avian forebrain organization and behavioural capabilities

The study of birds, especially the Galapagos finches, was important to Darwin in the development of the theory of evolution by natural selection. Birds have also been at the centre of a recent reformulation in understanding cerebral evolution and the substrates for higher cognition. While it was once thought that birds possess a simple cerebrum and were thus limited to instinctive behaviours, it is now clear that birds possess a well-developed cerebrum that looks very different from the mammalian cerebrum but can support a cognitive ability that for some avian species rivals that in primates.     

Avian brains and a new understanding of vertebrate brain evolution

We believe that names have a powerful influence on the experiments we do and the way in which we think. For this reason, and in the light of new evidence about the function and evolution of the vertebrate brain, an international consortium of neuroscientists has reconsidered the traditional, 100-year-old terminology that is used to describe the avian cerebrum. Our current understanding of the avian brain - in particular the neocortex-like cognitive functions of the avian pallium - requires a new terminology that better reflects these functions and the homologies between avian and mammalian brains.