Current Biology Vol 15 No 23 R946 resources for the sea urchin can the structure of the avian brain be found at Primer relates to that of the mammalian http://www.ncbi.nlm.nih.gov/geno brain, and how names have had a me/guide/sea_urchin/ and at negative influence on how birds http://hgsc.bcm.tmc.edu/projects/ Evolution of the are perceived. seaurchin/. Negativity surrounding the avian avian brain and brain began in the late nineteenth Where can I find out more? intelligence century, when Ludwig Edinger Cameron, C.B., Garey, J.R., and Swalla, B.J. provided names for the various (2000). Evolution of the chordate body parts of the vertebrate brain. His plan: New insights from phylogenetic analyses of deuterostome phyla. Proc. Nathan J. Emery and form of nomenclature was based Natl. Acad. Sci. USA 97, 4469–4474. Nicola S. Clayton on the naïve view that evolution Davidson, E.H., Rast, J.P., Oliveri, P., occurs in a linear progression, so Ransick, A., Calestani, C., Yuh, C.H., In Western society, the term ‘bird that each new species is an Minokawa, T., Amore, G., Hinman, V., brain’ is often used as a elaboration of an older species. Arenas-Mena, C., et al. (2002). A genomic regulatory network for derogatory term for a person of This scala naturae is often development. Science 295, 1669–1678. diminished intellect, partly represented as a ladder. With Davidson, E.H., and Cameron, R.A. (2002). because many people tend to respect to intelligence, Arthur Arguments for sequencing the genome think of birds as pecking Jenson, one of the key figures in of the sea urchin, Strongylocentrotus machines, responding reflexively studies of human intelligence purpuratus. A white paper submitted to the National Human Genome Research to stimuli in their environment, and argued that “single-cell Institute. partly because birds seem so protozoans, such as amoeba, rank http://www.genome.gov/Pages/Researc different from us, with their beady at the bottom of the scale, h/Sequencing/SeqProposals/SeaU- eyes and small heads. But over 40 followed in order by the rchin_Genome.pdf Duboc, V., Rottinger, E., Lapraz, F., years ago William Thorpe, who invertebrates, the lower Besnardeau, L., and Lepage, T. (2005). was the leading authority on bird vertebrates, the lower mammals... Left-right asymmetry in the sea urchin learning at that time, pointed out: and finally the primates, in order: embryo is regulated by nodal signaling “The poor development in birds of New World monkeys, Old World on the right side. Dev. Cell 9, 147–158. any brain structures clearly monkeys, the apes, and at the Ettensohn, C.A., Wessel, G.M., and Wray, G.A. eds. (2004). Development of sea corresponding to the cerebral pinnacle, humans”. urchins, ascidians and other invertebrate cortex of mammals led to the With respect to brain evolution, deuterostomes: Experimental assumption among neurologists Edinger applied this scala naturae Approaches, Volume 74 (London: not only that birds are primarily suggesting that the brains of living Elsevier Academic Press). creatures of instinct, but also that vertebrates retained ancestral Hinman, V.F., Nguyen, A.T., Cameron, R.A., and Davidson, E.H. (2003). they are very little endowed with structures, but that new brain Developmental gene regulatory network the ability to learn...this areas were added onto older architecture across 500 million years of misconceived view of brain ones, or older areas increased in echinoderm evolution. Proc. Natl. Acad. mechanisms, hindered the size and complexity to form new Sci. USA 100, 13356–13361. Peterson, K.J., Arenas-Mena, C., and development of experimental areas (Figure 1A). According to Davidson, E.H. (2000). The A/P axis in studies on bird learning”. this view, evolutionarily older echinoderm ontogeny and evolution: In the 1960s little was known brains are simple, and so produce evidence from fossils and molecules. about the cognitive capacities of simple instinctive behaviour, and Evol. Dev. 2, 93–101. birds, but recent studies lend evolutionarily newer brains are Raff, E.C., Popodi, E.M., Kauffman, J.S., Sly, B.J., Turner, F.R., Morris, V.B., and Raff, support for Thorpe’s view: we now complex, and therefore can R.A. (2003). Regulatory punctuated know that some bird species control learned and intelligent equilibrium and convergence in the make and use tools, can count, behaviour. The oldest brain evolution of developmental pathways in remember specific past events regions — those present in all direct-developing sea urchins. Evol. Dev. and reason about the mental vertebrates — were prefixed with 5, 478–493. Shu, D.-G., Conway Morris, S., Han, J., states of individuals, behaviours the term ‘paleo-‘, the next oldest Zhang, Z.-F., and Liu, J.-N. (2004). that some have considered to be brain regions were given the prefix Ancestral echinoderms from the unique to humans. Despite the ‘archi-’, whereas the new brain Chengjiang deposits of China. Nature apparent cognitive similarity regions — those present in the 430, 422–428. between humans and some birds, species closest to the top of the neuroscientists have tended to ‘ladder’ — were assigned the 1 Molecular Genetics Program, Benaroya view bird brains as interesting prefix ‘neo-’. Research Institute at Virginia Mason, 1201 Ninth Avenue, Seattle, WA 98101, curiosities with little relevance to We now know that, as with USA. 2Department of Biology, University the workings of the human brain. other parts of the body, the brains of Washington, 24 Kincaid Hall, Seattle, Recently, however, the Avian of distantly related species tend to Washington 98195, USA. 3Department Brain Nomenclature Consortium be derived from the same basic of Molecular & Cellular Biology, published a series of papers elements found in the common Sunnybrook & Women’s Research attempting to re-address the issue ancestor — they exhibit homology Institute and Medical Biophysics, University of Toronto, 2075 Bayview of the importance of the bird brain (Figure 1B). So although the Avenue, Toronto, Ontario M4N 3MS, to neuroscience by investigating common ancestor of birds and Canada. how the avian brain evolved, how mammals lived approximately 300 Magazine R947 million years ago, studies of A B extant reptiles have revealed that Humans Complex Humans the reptilian (therapsid and sauropsid) forebrain is pallial in Non-primate Mammals origin and so the common Birds mammals ancestor should also have shared Reptiles this trait. If so, then the forebrain Birds of modern birds and mammals will Amphibians also be pallial. This seems to be Reptiles the case. Fish Edinger mistakenly thought that Amphibians the majority of the avian brain was Fish derived from the striatum or basal Simple Current Biology ganglia, which tends to be involved in species-specific Figure 1. Schematic representation of two theories of brain evolution. instinctual behaviours, such as (A) The outdated ‘scala naturae’ theory, where evolution occurs in a linear, progressive feeding and sexual and parental fashion up a ladder in which ‘lower’ (simple) species evolve into ‘higher’ (complex) behaviour, as well as responses to species; going from fish and amphibians at the bottom through reptiles and birds to primates and humans at the top. With respect to brain evolution, the increasing rewards and motor coordination. complexity resulting from climbing the ladder leads to the appearance of completely In mammals, the basal ganglia has new areas which are then added onto old ones. Each colour represents a different a striated appearance due to the hypothetical brain region, either old or new. (B) The modern theory, where evolution is fibre bundles running through it. tree-like and new species evolve from older ancestral forms. With respect to brain Areas in the avian forebrain evolution, complexity is derived from refining neural structures which are already tended to resemble the present in ancestral forms, such that brain regions increase in size. There are no truly new brain areas, only elaborations of established regions. The colours represent mammalian striatum and so most different brain regions, but rather than new areas being added, evolutionarily old areas areas (paleo-, archi- or neo-) were are increased or decreased in size (or complexity). named with the root word ‘striatum’. For example, the avian matter. The analogy would be to intelligent. The names have cerebrum was originally separated compare a club sandwich changed, but not necessarily the into neostriatum, hyperstriatum, (mammalian) to a pepperoni pizza abilities associated with them. archistriatum, paleostriatum and (avian). There are over 9,000 species of ectostriatum (Figure 2). Note that The accumulation of new data birds, however many of those very few structures were thought led a consortium of avian studied by comparative to be derived from the pallium, neuroscientists to propose a new psychologists are not well and named with the root words nomenclature for the avian brain, endowed with the cognitive skills ’cortex’ or ‘pallium’. By contrast, where the forebrain was renamed associated with primates and much of the mammalian forebrain in the light of this modern dolphins. The humble pigeon, for was known to be derived from the understanding of its evolution and example, is a master at visual pallium, which resulted in a six- the relative contributions of the discrimination and memory: it can layered neocortex, the area of the striatum and pallium (Figure 2). remember hundreds of different brain which is involved in thinking, The proportion of the forebrain objects for long periods, reasoning and planning. that is known to be cortical-like discriminate between different Research in the last 30 years on (pallial) in structure has increased painting styles that would stump neural connectivity, gene significantly (Figure 2). These art history undergraduates, and expression and lesions has name changes reflect our current navigate hundreds of miles by caused a revision in our thinking understanding of how these brain following the trajectory of major about the avian forebrain and the regions evolved (Table 1), but they roads. But pigeons seem unable naming of its parts. We now know have had a wider impact on our to perform accurately on tasks that the greatest expanse of the thinking about the intellectual that require them to abstract a bird telencephalon is derived, not abilities of birds. As stated so general rule to solve a suite of from the striatum as Edinger and eloquently by William Thorpe over similar problems. For example, others previously thought, but 40 years ago, this when presented with a choice from the pallium. Indeed, the large misunderstanding about the between two colours, A and B, area of forebrain that lies above evolution of the avian brain has they cannot apply the following the basal ganglia in birds is now led to an extreme bias against the rule; ‘If pecking A is rewarded, recognised to be functionally and capabilities of birds in learning then continue to peck at A; if developmentally akin to the and cognition. Of course, we pecking A is not rewarded, peck mammalian neocortex, derived in should not be carried away with at B’. This rule is called ‘win-stay- the same way from the pallial the idea that, because the avian lose-shift’, and is easily learned by sector of the embryonic forebrain. brain is structurally more similar to crows, monkeys and apes. But rather than producing a the mammalian brain than As with all other taxonomic layered cortex as in mammals, in previously thought, all birds are groups, there are the Dumbos and birds the result was a nucleated intelligent, any more than we the Einsteins, and a species’ level structure with pockets of grey might think that all mammals are of intelligence tends to be Current Biology Vol 15 No 23 R948

Classic view Revised view

Mesopallium Archicortex Hyperstriatum Lateral Lateral Hyperpallium ventricle ventricle CDL CDL HA HA IHA HP Amygdaloid L2 Neostriatum complex L2 Nidopallium HV IHA Archistriatum E Archipallium E

Cerebellum LPO Cerebellum Striatum

Thalamus Thalamus OB OB Paleocortex Piriform cortex

Hindbrain Midbrain Paleostriatum Hindbrain Pallidum augmentum Midbrain

Paleostriatum Current Biology primitivum

Figure 2. Comparison of the classic and revised views of the avian forebrain. Left: classic view of the avian forebrain, in which the greatest expanse of the cerebrum was classified as striatal in origin (light green), compared to the smaller extent of the pallium (light blue). Right: revised view of the avian forebrain, in which the majority of the cerebrum has been re-classified as pallial in origin (light blue) compared to the smaller striatum (light green). The pallidum is coloured dark green, and the olfactory bulb is coloured yellow. Adapted from Avian Brain Nomenclature Consortium (2005). CDL, area corticoidea dorsolateralis; E, ectostriatum (classic) or entopallium (revised); HA, hyperstriatum accessorium (classic) or hyperpallium apicale (revised); HP, hippocampal complex; IHA, interstitial nucleus of the hyperpallium intercalatum; L2, field L2; LPO, parolfactory lobe; OB, olfactory bulb. Similar visual processing reflected in brain size (relative and they do not have the traditional pathways absolute). Within fish, for example, six-layered prefrontal cortex of the sharks and rays have large mammals? Although corvids and The mammalian neocortex is brains for their body size, and parrot brains are relatively the highly laminated, with six layers, although they have not been same size as those of from the superficial layers on the tested for their cognitive skills in chimpanzees, gorillas and surface to the deeper layers the laboratory, they are adaptable, orangutans, bird and mammal underneath. Each layer has its flexible and opportunistic, all brains are structured very own cell types, connectional hallmarks of intelligence. differently. We have suggested patterns and neurochemical Compare this with lampreys, that corvids and apes may composition. By contrast, the which have a very small brain for represent a case of convergent avian telencephalon is nucleated, their body size, and although mental evolution — similar with little or no laminar biologically successful in terms of cognitive processes, with the organization. There is one striking reproductive success, do not same outcome — but with exception: the Wulst or display any particularly striking divergent brains — very different hyperpallium, on the dorsal psychological adaptations. brain structures. But there are surface of the forebrain, which Similarly within the mammals: clues from modern neuroanatomy consists of three to four layers, dolphins, monkeys and apes are suggesting that avian and depending on its size. Each layer the intellectual champions, mammalian brains may have has its own connectional and compared to say, rabbits, sheep come up with similar solutions to neurochemical patterns, and visual or wild boar. The same holds true the same problems, thus information appears to be for birds. Recently, we have demonstrating both mental and processed by similar pathways to suggested that corvids (crows, neural convergent evolution. the mammalian forebrain. Similar ravens and jays) and parrots Although the gross structures of connectivity patterns have been compare favourably with the apes avian and mammalian brains are found in the somatosensory and in terms of both relative brain size radically different, there is motor systems of birds and and intelligence, but pigeons, evidence that there are mammals. It is not yet certain chickens and quail are more connectional similarities in the which aspects of these anatomical comparable to rats and mice. brains which may go some way in traits have evolved from a explaining their cognitive common ancestor and which have Avian and mammalian brains similarities. Although these evolved independently. compared similarities are found in perceptual How can corvids, parrots and systems, it is not implausible that Similar vocal learning pathways possibly other birds rival apes in similar principles may also apply The song control system of their intellectual capacities, when to cognitive systems. songbirds (oscines), such as Magazine R949

zebra finches and canaries, has Table 1. Old and new nomenclature of the avian telencephalon, with nomenclature of been the focus of neurobiological analogous structures in the mammalian telencephalon. study for almost 40 years. Song Avian Avian Mammalian birds learn their song from a tutor, old nomenclature new nomenclature nomenclature often their father. Recent studies in two other orders of birds that Ectostriatum Entopallium Neocortex (sensory) also learn their vocalizations, the Hyperstriatum Hyperpallium apicale Neocortex (sensory) parrots and hummingbirds, have accessorioum revealed similar connectivity Hyperstriatum dorsale Hyperpallium dorsocellulare Neocortex (sensory) patterns to songbirds in their vocal control pathways. In non- Hyperstriatum ventrale Mesopallium Neocortex (association) vocal learners, such as pigeons Wulst (Hyperstriatum) Wulst (Hyperpallium) Neocortex (sensory) and doves, neural activation during vocalizing is restricted to Neostriatum Nidopallium Neocortex (prefrontal) the brainstem and midbrain, Paleostriatum Lateral striatum Striatum suggesting that vocalizations are augmentatum relatively reflexive and innate. Paleostriatum Globus pallidus Globus pallidus Indeed, non-vocal learners, primitivum perceive and produce Parolfactory lobe Medial striatum Caudate and putamen vocalizations only using this neural system. By comparison, in vocal learners, neural activation traits, these birds may also have Although this is striking when perceiving calls and functionally equivalent areas evidence for functional and vocalizing occurs in the located in the telencephalon. The possibly anatomical convergence brainstem, midbrain and strongest candidate is the between the avian CDLN and additionally distinct song control caudolateral nidopallium (CDLN). primate prefrontal cortex, there nuclei in the forebrain. Very Neurobiological studies focused are a number of outstanding specific regions in the forebrain on the CDLN of pigeons have questions. For one thing, the only are involved in perceiving song or revealed similarities in tasks that have been affected by vocalizations, and separate connectivity, neurochemistry, both prefrontal cortex and CDLN regions are involved in producing neurophysiology and function to lesions are working memory song (often imitating songs the mammalian dorsolateral tasks. Other more complex tasks, produced by a tutor). Vocal prefrontal cortex. For example, such as attentional set-shifting, learning has been suggested to lesions of the CDLN affect the have not yet been tested in birds. have only evolved six times: within performance of birds on Secondly, the only avian species birds, in the oscines, parrots and traditional tasks used to gauge to be examined is the pigeon, hummingbirds; and within prefrontal cortex function in which as stated earlier is not the mammals, in the cetaceans mammals: delayed alternation, brightest pupil in the flock, and (dolphins and whales), pinnipeds reversal learning and other certainly does not demonstrate (seals and sealions) and humans. working memory tasks, such as the same forms of complex The neural pathways involved in Go/No Go. Neurons within the cognition displayed by birds with vocal learning in cetaceans and CDLN respond during the delay larger forebrains, and importantly, pinnipeds are not known. In period of Go/No Go tasks similar a larger nidopallium. Indeed, the humans, however, functionally to neurons in the primate nidopallium of crows is four times similar neural networks to birds dorsolateral prefrontal cortex. larger than that of quail, have been implicated in language There are also similarities pheasants and partridges (the learning. between the avian CDLN and only species for which there are mammalian prefrontal cortex in data). From absolute brain size, An avian ‘prefrontal cortex’? the distribution of dopamine the nidopallium of crows is One final example of fibres, and the concentration of predicted to be significantly larger convergence in the neural dopamine D1 receptors, but not than that of pigeons. It remains to systems of birds and mammals D2 receptors. Indeed, blocking D1 be seen what effect CDLN lesions relevant to the issue of receptors in the CDLN disrupts will have on corvids and parrots. intelligence is the suggestion that performance on similar tasks to Finally, many aspects of complex birds may have a functionally those affected by permanent cognition which have been equivalent structure to the lesions. Finally, the CDLN is demonstrated in corvids, such as mammalian prefrontal cortex. In connected reciprocally with episodic-like memory and theory mammals, the prefrontal cortex secondary sensory areas of all of mind, are known to be contributes to the organization, modalities, and projects to dependent on other parts of the planning and flexibility of somatomotor and limbic areas of prefrontal cortex (ventromedial behaviour based on previously the basal ganglia which allow it to sector) in humans. If these acquired information. As there is influence behavioural and abilities in corvids are functionally good evidence that some birds affective responses similar to equivalent to humans, we might display these complex cognitive primate prefrontal cortex. expect to find areas within the Current Biology Vol 15 No 23 R950 corvid brain that are structurally, attribute others with the intention Correspondences as well as functionally, analogous of pilfering, and so implement to the ventromedial prefrontal strategies to reduce this cortex of humans. This hypothesis possibility in the future. Scrub- remains to be tested. jays also protect their caches by Multidimensional reducing the amount of scaling reveals a Avian intelligence is not an information available to an oxymoron observer at the time of caching, color dimension Some birds are capable of by hiding caches behind barriers, cognitive feats which put most in the shade or as far from an unique to ‘color- mammals to shame. In the observer as possible. All this rainforests of New Caledonia and suggests that western scrub-jays deficient’ Mare, New Caledonian crows use may demonstrate another observers and construct a number of supposedly unique form of different tools which are used to human cognition: theory of mind. gain access to large grubs found Parrots, such as Alex the African J.M. Bosten1, J.D. Robinson1, in the crevices of trees. These grey, have also demonstrated G. Jordan2 and J.D. Mollon1 tools are crafted from raw intellectual abilities which rival materials (sticks and Pandanus primates, such as understanding Normal color vision depends on leaves), and there is a suggestion whether objects are the same or the relative rates at which photons that, like chimpanzees, crow tool different, their number (including are absorbed in three types of use is a form of culture. In the zero), their colour and shape. retinal cone: short-wave (S), laboratory, New Caledonian crows Our new appreciation of the middle-wave (M) and long-wave (L) are equally impressive, complexity of the avian brain is cones, maximally sensitive near demonstrating some closely tied with a new 430, 530 and 560 nm, respectively. understanding of ‘folk physics’ appreciation of the complexity of But 6% of men exhibit an X-linked (the common sense view of how the avian mind, particularly with variant form of color vision called the world works). Perhaps the respect to corvids and parrots. It deuteranomaly [1]. Their color best demonstration of this is Betty is now the job of behavioural vision is thought to depend on S the crow, who appeared to biologists, comparative cones and two forms of long-wave spontaneously bend a piece of psychologists and neuroscientists cone (L, L′) [2,3]. The two types of wire into a hook to gain access to to determine how one translates L cone contain photopigments that out-of-reach food. into the other. are maximally sensitive near Other corvids are equally 560 nm, but their spectral impressive, providing evidence of Further reading sensitivities are different enough cognitive abilities thought to be Avian Brain Nomenclature Consortium. that the ratio of their activations uniquely human. Western scrub- (2005). Avian brains and a new gives a useful chromatic signal. understanding of vertebrate brain jays, for example, are the first evolution. Nat. Rev. Neurosci. 6, Like color-normal observers, non-human animals to 151–159. deuteranomalous observers are demonstrate episodic-like Emery, N.J. (2005). Cognitive ornithology: formally trichromatic, in that they memory — the ability to The evolution of avian intelligence. Phil. need three primary lights if they are Trans. Roy. Soc. Lon. Biol. Sci., in press. remember the ‘what, where and Emery, N.J., and Clayton, N.S. (2004). The to match all possible spectral when’ of a specific past event. In mentality of crows: convergent evolution power distributions, but the these studies, jays cache of intelligence in corvids and apes. matches they make are different different types of food which Science 306, 1903–1907. from those of the normal. Here we Pepperberg, I.M. (1999). The Alex Studies: decay at different rates in Cognitive and communicative abilities of use multidimensional scaling specific locations. In order to grey parrots. Harvard University Press: (MDS) [4,5] to reveal the color recover food that is still fresh and Cambridge, MA. dimension that is private to the edible, the jays had to remember Reiner, A., Perkel, D.J., Bruce, L.L., Butler, deuteranomalous observer. ‘what’ type of food they cached, A.B., Csillag, A., Kuenzel, W., Medina, L., For both normal and anomalous Paxinos, G., Shimizu, T., Striedter, G. et ‘where’ they cached and ‘when’ al. (2004). Revised nomenclature for observers, MDS has previously they cached it. Scrub-jays are avian telencephalon and some related been used to reconstruct also extremely wary of the brainstem nuclei. J. Comp. Neurol. 473, subjective color spaces (for presence of conspecifics during 377–414. example [6,7]). The input to the Striedter, G. (2005). Principles of Brain caching. If an observer is Evolution. Sinauer Associates scaling program is a matrix of the watching when scrub-jays cache, Publishers, Inc.: Sunderland, judged similarities of all possible the storers come back later when Massachusetts. pairs in a set of stimuli; and the alone and move their caches to output is a map of the stimuli that new places that the observer minimizes the differences between does not know. Interestingly, Sub-department of Animal Behaviour the input proximities and the storers only do this if they have and Department of Experimental corresponding proximities in the Psychology,University of Cambridge, been thieves themselves in the Cambridge, UK. derived space. The length of the past. This suggests that Email: [email protected]; vector between any two stimuli in experienced scrub-jays may [email protected] the output space indicates how