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The selection of model species tends to involve two typically unstated assumptions, namely: (1) that the similarity between species decreases steadily with phylogenetic distance, and (2) that similarities are greater at lower levels of biological organization. The first assumption holds on average, but species similarities tend to decrease with the square root of divergence time, rather than linearly, and lineages with short generation times (which includes most model species) tend to diverge faster than average, making the decrease in similarity non-monotonic. The second assumption is more difficult to test. Comparative molecular research has traditionally emphasized species similarities over differences, whereas comparative research at higher levels of organization frequently highlights the species differences. However, advances in comparative genomics have brought to light a great variety of species differences, not just in gene regulation but also in protein coding genes. Particularly relevant are cases in which homologous high-level characters are based on non-homologous genes. This phenomenon of non-orthologous gene displacement, or “deep non-homology,” indicates that species differences at the molecular level can be surprisingly large. Given these observations, it is not surprising that some findings obtained in model species do not generalize across species as well as researchers had hoped, even if the research is molecular.

Comparative neurobiologists have long wondered when and how the dorsal pallium (e.g., mammalian neocortex) evolved. For the last 50 years, the most widely accepted answer has been that this structure was already present in the earliest vertebrates and, therefore, homologous between the major vertebrate lineages. One challenge for this hypothesis is that the olfactory bulbs project throughout most of the pallium in the most basal vertebrate lineages (notably lampreys, hagfishes, and lungfishes) but do not project to the putative dorsal pallia in teleosts, cartilaginous fishes, and amniotes (i.e., reptiles, birds, and mammals). To make sense of these data, one may hypothesize that a dorsal pallium existed in the earliest vertebrates and received extensive olfactory input, which was subsequently lost in several lineages. However, the dorsal pallium is notoriously difficult to delineate in many vertebrates, and its homology between the various lineages is often based on little more than its topology. Therefore, we suspect that dorsal pallia evolved independently in teleosts, cartilaginous fishes, and amniotes. We further hypothesize that the emergence of these dorsal pallia was accompanied by the phylogenetic restriction of olfactory projections to the pallium and the expansion of inputs from other sensory modalities. We do not deny that the earliest vertebrates may have possessed nonolfactory sensory inputs to some parts of the pallium, but such projections alone do not define a dorsal pallium.

Basal stem tetrapods were fully aquatic but spent time at the water surface breathing air, which was useful at the end of the Devonian, when aquatic oxygen levels were low. After the Devonian, early tetrapods became fully terrestrial, at least as adults. This transition involved major changes in the musculoskeletal system for locomotion and the evolution of new modes of feeding. Aerial vision required changes in the eye but then allowed for high-resolution vision over long distances. In contrast, the lateral line systems are useless in air and were lost in fully terrestrial tetrapods. The brains of early tetrapods were relatively simple, possibly simplified through a process called paedomorphosis. The telencephalon’s main function in early tetrapods was to inhibit or disinhibit the lower brain regions. Later tetrapods diverged into extant amphibians and amniotes. Within the amphibian lineage, anurans evolved a tympanic ear, which increased their ability to hear airborne sounds.

After summarizing the earlier chapters, which focused on the evolution of specific lineages, this chapter examines general patterns in the evolution of vertebrate nervous systems. Most conspicuous is that relative brain size and complexity increased independently in many lineages. The proportional size of individual brain regions tends to change predictably with absolute brain size (and neurogenesis timing), but the scaling rules vary across lineages. Attempts to link variation in the size of individual brain areas (or entire brains) to behavior are complicated in part because the connections, internal organization, and functions of individual brain regions also vary across phylogeny. In addition, major changes in the functional organization of vertebrate brains were caused by the emergence of novel brain regions (e.g., neocortex in mammals and area dorsalis centralis in teleosts) and novel circuits. These innovations significantly modified the “vertebrate brain Bauplan,” but their mechanistic origins and implications require further investigation.

Between 450 and 500 million years ago, some vertebrates evolved paired fins and jaws, which made them more efficient swimmers and fiercer predators. These jawed vertebrates (i.e., gnathostomes) diversified in the Devonian period, but most died out during the end-Devonian mass extinction. The surviving gnathostomes had a more complex vestibular apparatus than their jawless ancestors, an expanded set of olfactory receptor genes, and vomeronasal receptors. A major innovation in the brains of gnathostomes was the emergence of a cerebellum that is distinct from the cerebellum-like areas found in all vertebrates. The telencephalon of early vertebrates processed primarily olfactory information, but this olfactory dominance was independently reduced in three later lineages, namely in cartilaginous fishes, ray-finned fishes, and tetrapods. In concert with the reduction in olfactory dominance, these lineages enlarged their telencephalon, relative to other brain regions, and evolved a telencephalic “dorsal pallium” that receives non-olfactory sensory information from the diencephalon.

Much is conserved in vertebrate evolution, but significant changes in the nervous system occurred at the origin of vertebrates and in most of the major vertebrate lineages. This book examines these innovations and relates them to evolutionary changes in other organ systems, animal behavior, and ecological conditions at the time. The resulting perspective clarifies what makes the major vertebrate lineages unique and helps explain their varying degrees of ecological success. One of the book’s major conclusions is that vertebrate nervous systems are more diverse than commonly assumed, at least among neurobiologists. Examples of important innovations include not only the emergence of novel brain regions, such as the cerebellum and neocortex, but also major changes in neuronal circuitry and functional organization. A second major conclusion is that many of the apparent similarities in vertebrate nervous systems resulted from convergent evolution, rather than inheritance from a common ancestor. For example, brain size and complexity increased numerous times, in many vertebrate lineages. In conjunction with these changes, olfactory inputs to the telencephalic pallium were reduced in several different lineages, and this reduction was associated with the emergence of pallial regions that process non-olfactory sensory inputs. These conclusions cast doubt on the widely held assumption that all vertebrate nervous systems are built according to a single, common plan. Instead, the book encourages readers to view both species similarities and differences as fundamental to a comprehensive understanding of nervous systems.

This introductory chapter describes the book’s general approach and underlying philosophy. The authors adopt a definition of biological homology that recognizes the hierarchical nature of biological organization and allows for any aspects of a character to change over the course of evolution. The only essential homology criterion is that the characters in question must have been retained from a common ancestor, rather than having evolved independently in multiple lineages. These fundamental ideas are discussed in the context of related concepts, notably “field homology” and the homology of cell types and developmental pathways. Although it is easy to get tangled up in questions about the homology or non-homology of individual characters, the book’s main concern is the evolution and natural history of entire organisms and the lineages to which they belong.

Mammals and birds exhibit many examples of convergent evolution, including endothermy and related traits that helped them survive the end-Cretaceous mass extinction. The subsequent diversification of both lineages was accompanied by multiple expansions in relative and (often) absolute brain size. Examples of convergent evolution in the brain include complex folding of the cerebellar cortex, complex auditory circuits, and highly laminar areas within the telencephalon. Of course, birds and mammals also diverged in numerous respects. In particular, early mammals (but not birds!) shifted into a nocturnal niche, which was accompanied by an expansion of the olfactory system and the evolution of highly light-sensitive eyes. In the process, early mammals became “color-blind,” but excellent color vision re-evolved in some diurnal lineages, notably platyrrhine primates. Mammalian brains are also unusual for having strong reciprocal connections between thalamus and dorsal pallium (i.e., neocortex) and extensive commissural connections between the left and right neocortex.

Some time in the Ediacaran or early Cambrian period, the first vertebrates emerged. Compared to the invertebrate chordates, early vertebrates were active predators, rather than suspension feeders. This change in behavior was facilitated by several major morphological innovations, including pharyngeal muscles that pump water through the pharynx, vascularized gills, paired image-forming eyes, a complex vestibular apparatus, lateral line receptors, taste buds, and a well-developed olfactory system. Early vertebrates also evolved several new brain regions, notably the telencephalon and the midbrain. Developmentally, most of these innovations were linked to the emergence of two novel embryonic tissues, namely placodes and neural crest. Although these tissues and their adult derivatives did not evolve “out of nothing,” they represent genuine innovations that contributed substantially to the evolutionary success of the vertebrate lineage.

Early amniotes evolved water-resistant skin and eggs, which allowed them to live and reproduce entirely on land. Roughly 300 million years ago, amniotes split into synapsids (including mammals) and sauropsids (“reptiles” and birds). The sauropsid lineage includes squamates (lizards and snakes), turtles, and archosaurs (crocodilians and dinosaurs, including birds). Tympanic ears and more complex auditory systems evolved at least twice within the various amniote lineages. Amniotes also evolved a separate vomeronasal epithelium and more diverse modes of locomotion and feeding. Brain size relative to body size increased in early amniotes and then increased further in several amniote lineages, notably mammals and birds. The most enlarged regions were the cerebellum and the telencephalon. Within the telencephalon, sauropsids enlarged mainly the ventral pallium, whereas mammals enlarged the dorsal pallium (aka neocortex). Although these regions are not homologous to one another, they both receive unimodal auditory, visual, and somatosensory input from the thalamus.

Testing this Darwinian hypothesis is a tough nut to crack

Why the cerebral cortex folds in some mammals but not in others has long fascinated and mystified neurobiologists. Over the past century—especially the past decade—researchers have used theory and experiment to support different folding mechanisms such as tissue buckling from mechanical stress, axon tethering, localized proliferation, and external constraints. In this review, we synthesize these mechanisms into a unifying framework and introduce a hitherto unappreciated mechanism, the radial intercalation of new neurons at the top of the cortical plate, as a likely proximate force for tangential expansion that then leads to cortical folding. The interplay between radial intercalation and various biasing factors, such as local variations in proliferation rate and connectivity, can explain the formation of both random and stereotypically positioned folds.

Although the hippocampus is structurally quite different among reptiles, birds, and mammals, its function in spatial memory is said to be highly conserved. This is surprising, given that structural differences generally reflect functional differences. Here I review this enigma in some detail, identifying several evolutionary changes in hippocampal cytoarchitecture and connectivity. I recognize a lepidosaurid pattern of hippocampal organization (in lizards, snakes, and the tuatara Sphenodon) that differs substantially from the pattern of organization observed in the turtle/archosaur lineage, which includes crocodilians and birds. Although individual subdivisions of the hippocampus are difficult to homologize between these two patterns, both lack a clear homolog of the mammalian dentate gyrus. The strictly trilaminar organization of the ancestral amniote hippocampus was gradually lost in the lineage leading to birds, and birds expanded the system of intrahippocampal axon collaterals, relative to turtles and lizards. These expanded collateral axon branches resemble the extensive collaterals in CA3 of the mammalian hippocampus but probably evolved independently of them. Additional examples of convergent evolution between birds and mammals are the loss of direct inputs to the hippocampus from the primary olfactory cortex and the general expansion of telencephalic regions that communicate reciprocally with the hippocampus. Given this structural convergence, it seems likely that some similarities in the function of the hippocampus between birds and mammals, notably its role in the ability to remember many different locations without extensive training, likewise evolved convergently. The currently available data do not allow for a strong test of this hypothesis, but the hypothesis itself suggests some promising new research directions.

Efforts to understand nervous system structure and function have received new impetus from the federal Brain Research through Advancing Innovative Neurotechnologies (BRAIN) Initiative. Comparative analyses can contribute to this effort by leading to the discovery of general principles of neural circuit design, information processing, and gene-structure-function relationships that are not apparent from studies on single species. We here propose to extend the comparative approach to nervous system ‘maps' comprising molecular, anatomical, and physiological data. This research will identify which neural features are likely to generalize across species, and which are unlikely to be broadly conserved. It will also suggest causal relationships between genes, development, adult anatomy, physiology, and, ultimately, behavior. These causal hypotheses can then be tested experimentally. Finally, insights from comparative research can inspire and guide technological development. To promote this research agenda, we recommend that teams of investigators coalesce around specific research questions and select a set of ‘reference species' to anchor their comparative analyses. These reference species should be chosen not just for practical advantages, but also with regard for their phylogenetic position, behavioral repertoire, well-annotated genome, or other strategic reasons. We envision that the nervous systems of these reference species will be mapped in more detail than those of other species. The collected data may range from the molecular to the behavioral, depending on the research question. To integrate across levels of analysis and across species, standards for data collection, annotation, archiving, and distribution must be developed and respected. To that end, it will help to form networks or consortia of researchers and centers for science, technology, and education that focus on organized data collection, distribution, and training. These activities could be supported, at least in part, through existing mechanisms at NSF, NIH, and other agencies. It will also be important to develop new integrated software and database systems for cross-species data analyses. Multidisciplinary efforts to develop such analytical tools should be supported financially. Finally, training opportunities should be created to stimulate multidisciplinary, integrative research into brain structure, function, and evolution. J. Comp. Neurol. 522:1445–1453, 2014. © 2014 Wiley Periodicals, Inc.

Efforts to understand nervous system structure and function have received new impetus from the federal Brain Research through Advancing Innovative Neurotechnologies (BRAIN) Initiative. Comparative analyses can contribute to this effort by leading to the discovery of general principles of neural circuit design, information processing, and gene-structure-function relationships that are not apparent from studies on single species. We here propose to extend the comparative approach to nervous system ‘maps' comprising molecular, anatomical, and physiological data. This research will identify which neural features are likely to generalize across species, and which are unlikely to be broadly conserved. It will also suggest causal relationships between genes, development, adult anatomy, physiology, and, ultimately, behavior. These causal hypotheses can then be tested experimentally. Finally, insights from comparative research can inspire and guide technological development. To promote this research agenda, we recommend that teams of investigators coalesce around specific research questions and select a set of ‘reference species' to anchor their comparative analyses. These reference species should be chosen not just for practical advantages, but also with regard for their phylogenetic position, behavioral repertoire, well-annotated genome, or other strategic reasons. We envision that the nervous systems of these reference species will be mapped in more detail than those of other species. The collected data may range from the molecular to the behavioral, depending on the research question. To integrate across levels of analysis and across species, standards for data collection, annotation, archiving, and distribution must be developed and respected. To that end, it will help to form networks or consortia of researchers and centers for science, technology, and education that focus on organized data collection, distribution, and training. These activities could be supported, at least in part, through existing mechanisms at NSF, NIH, and other agencies. It will also be important to develop new integrated software and database systems for cross-species data analyses. Multidisciplinary efforts to develop such analytical tools should be supported financially. Finally, training opportunities should be created to stimulate multidisciplinary, integrative research into brain structure, function, and evolution.

Evo-devo biology involves cross-species comparisons of entire developmental trajectories, not just of adult forms. This approach has proven very successful in general morphology, but its application to neurobiological problems is still relatively new. To date, the most successful area of evo-devo neurobiology has been the use of comparative developmental data to clarify adult homologies. The most exciting future prospect is the use of comparative developmental data to understand the formation of species differences in adult structure and function. An interesting «model system» for this kind of research is the quest to understand why the neocortex folds in some species but not others.

Some contemporary scientists are using comparative neurobiological data to argue that non-mammalian vertebrates have feelings, most notably of pain (e.g., Braithwaite, 2010; Mashour and Alkire, 2012), while Key (2016) uses the same general data to reach the opposite conclusion. In a nutshell, he argues that fish cannot feel pain because fish don’t have a neocortex, which humans need to consciously experience pain. I don’t know how these scientists can look at essentially the same data and reach such disparate conclusions, but I suspect that some of them have strong a priori beliefs and, therefore, view the data through differently tinted spectacles. In any case, I think that both sides have overplayed their hands; the debate cannot be settled yet. Georg F. Striedter gstriedt@uci.edu is Professor in the School of Biological Sciences, University of California, Irvine. Editor-in-Chief of Brain, Behavior, and Evolution, his research is on the evolution of vertebrate brains and behavior, including what makes specific taxonomic groups (e.g., humans, primates, birds) behaviorally and neurobiologically unique, with a special interest in synthesizing experimental data that are already published. http://www.cnlm.uci.edu/fellows/georg-striedter As Key (2016) notes in his review, teleost fish have brains that differ radically from those of mammals, especially in the forebrain. Teleost fish do have homologs of the main telencephalic divisions that all vertebrates share, but teleosts and other non-mammalian vertebrates don’t have the kind of laminated neocortex that mammals possess. Key also claims that humans with extensive damage to the neocortex lack consciousness, including feelings of pain. I am less certain of this claim, in part because the neocortex is such a prominent component of human brains that its destruction is likely to throw most of the remaining central nervous system into paralytic disarray (see Merker, 2007, for additional criticisms of the “consciousness is in the neocortex” argument and Langsjo et al., 2012, for some relevant data). However, for the purposes of argument, I am willing to grant that humans with total neocortical lesions tend not to feel pain. But do these stipulated facts allow us to conclude that fish cannot be conscious or feel pain? I do not think so, because fish might have evolved an altogether different set of neural circuits that is just as capable as the mammalian neocortex of generating consciousness. After all, the independent evolution of similar neural features and behavioral capacities is a well-known aspect of evolution. It is pretty clear, for example, that the capacity for complex cognition (e.g., tool manufacture and use) evolved independently in birds and mammals (see Striedter, 2013), even though the avian telencephalon is very different from its mammalian Animal Sentience 2016.021: Commentary on Key on Fish Pain 2 counterpart. (Birds do have a neocortex homolog, but most of it differs in numerous respects from the mammalian neocortex.) Hence we cannot conclude that birds are incapable of complex cognition just because they lack a typical mammalian neocortex. Similarly, we cannot conclude that fish are red-green color blind just because they lack one of the photosensitive pigments that primates need to make this discrimination; fish simply accomplish this task using a different set of molecules (e.g., Bowmaker, 1998). In short, the fact that different species can (and did) evolve different neural mechanisms to achieve similar behaviors makes me wary of concluding that fish cannot feel pain simply because they lack mammalian neocortex. Key goes on to make a more specific and interesting argument: He claims that having a neocortex is the only way to achieve consciousness, because only a neocortex can provide the kind of “signal amplification” and “global integration” that is needed for consciousness. This is a laudable attempt to specify the kinds of “computations” that might be capable of generating consciousness. However, the criteria he lists seem vague to me and heavily dependent on the assumption that only a mammalian neocortex can generate consciousness, which would make the argument circular. Moreover, it is far from clear that fish brains cannot meet Key’s criteria, because some teleosts have a very well developed telencephalon (Nieuwenhuys, 2009), including lamination in some areas, and all teleosts have a large and highly laminated midbrain tectum, which is generally acknowledged to mediate multisensory and sensorimotor integration (Northmore, 2011), as well as attention (at least in mammals). So, who is to say that a fish brain cannot achieve the kind of signal amplification and global integration that is supposedly sufficient for generating conscious experiences? Key might counter that possession of a large midbrain is not relevant to the debate, because we already know (or have at least stipulated) that when the neocortex is lesioned in humans the remaining subcortical regions cannot support consciousness. However, ever since Richard Owen introduced the concept of homology into biology, it has been clear that homologous structures may change their functions during the course of evolution (e.g., Striedter and Northcutt, 1991). It is particularly relevant that non-mammals with lesions of the “cerebral hemispheres” have long been known to be capable of broadly conserved behaviors that primates with equivalent lesions cannot perform. For example, fish and frogs are capable of locomotion even after their telencephalon is ablated, whereas primates with lesions of the motor cortex are generally paralyzed (Ch. 2 of James, 1890). Given such species differences in lesion effects, I ask: if fish with without cerebral hemispheres can swim, why shouldn’t they be able to feel pain? It is at least a possibility. I am also concerned with Key’s claim that non-mammalian vertebrates “do not perform behaviours to be rewarded with pleasurable feelings or alternatively to escape painful feelings.” This claim seems to imply that non-mammals can only generate hard-wired defensive responses to noxious stimuli (nocifensive behaviors), and that they are incapable of behavior that is driven by expected rewards or punishments. Yet it is abundantly clear that both classical and instrumental conditioning are broadly conserved among the vertebrates (MacPhail, 1982). It is interesting to note, for example, that goldfish learn to avoid food that made them nauseous and that this conditioned taste aversion is impaired after telencephalic lesions, just as it is in Animal Sentience 2016.021: Commentary on Key on Fish Pain 3 mammals and birds. Based on his target article, I suspect that Key might respond by saying that such forms of learning have “survival value” and are, therefore, distinct from conscious feelings. However, I am not convinced that conscious feelings must lack survival value to be considered genuine. Indeed, I would argue that a generalized “feeling of pain” might be just as useful to animals as a highly localized sensation of pain; the latter helps the animal deal with present pain, the former helps it learn how to avoid future pain. For me, there are two key unanswered questions: First, how does neural circuitry generate consciousness? If we could answer this question, then we could perhaps determine which species have the requisite mechanisms, be they in the neocortex or elsewhere. Alas, I remain unconvinced of any answers that have thus far been proposed. Second, I would like to know what “selective pressures” might give rise to feelings and consciousness, and whether those pressures might differ across species? Again, I do not have a clear answer, but it seems clear to me that pain may have a variety of functions in addition to simply triggering an escape from noxious stimuli. Feelings and memories of pain might, for example, prompt an injured animal to rest and heal, long after the noxious stimulus has passed. Importantly, I’m happy to concede that these functions may vary across species. I am intrigued, for example, by the recent suggestion that humans might feel and express pain differently from other animals, because humans stand to benefit (much more than other animals) when their conspecifics help them recuperate (Finlay and Syal, 2014). However, allowing for this species difference need not imply that non-humans do not feel pain; it simply means that they might feel it differently and, just as importantly, express those feelings differently. In short, I think that it is possible to analyze feelings of pain (perhaps even consciousness in general) from a comparative perspective, but drawing firm conclusions now seems premature. Hopefully some data from comparative neurobiology can help inform this quest, but I am not yet sure how this might best be done. For now, I remain an optimistic agnostic.

Primates have evolved an expanded isocortex relative to many other mammals. Parrots and songbirds have evolved an expanded telencephalon relative to many other birds. Previous work suggests that the expansion of the telencephalon in parrots and songbirds as well as the isocortex in primates is achieved, at least in part, by selectively delaying neurogenesis, expanding the subventricular zone (SVZ) and delaying maturation. The finding that similar developmental alterations in the spatial and temporal pattern of neurogenesis evolved together in these two distant lineages suggests that a single change in developmental mechanism might account for the expansion of the isocortex or telencephalon. We here review how uniformly lengthening developmental schedules may result in delays of neurogenesis, the expansion of the SVZ and delayed maturation. We propose that delays in neurogenesis may cause ventricular zone (VZ) cells to proliferate faster than the VZ can expand, which may force many proliferating cells to leave the VZ and form an expanded SVZ. Prolonged proliferation in the VZ and SVZ causes delays in neuronal maturation, which in turn may promote learning from conspecifics. Thus, we suggest that a single heterochronic change in developmental timing may orchestrate a variety of changes in the spatial and temporal pattern of proliferation, which has important behavioral consequences in adulthood.

The telencephalon is proportionately larger in parrots than in galliformes (chicken-like birds), whereas the midbrain tectum is proportionately smaller. We here test the hypothesis that the adult species difference in midbrain proportion is due to an evolutionary change in early brain patterning. In particular, we compare the size of the early embryonic midbrain between parakeets (Melopsittacus undulatus) and bobwhite quail (Colinus virgianus) by examining the expression domains of transcription factors Pax6 and Gbx2, which are expressed in the forebrain and hindbrain, respectively. Because these expression domains form rostral and caudal borders with the presumptive midbrain when this region is specified (Hamburger-Hamilton stages 9-11), they allow us to measure and compare the sizes of a molecularly defined presumptive midbrain in the two species. Based on published data from older embryos, we predicted that the molecularly defined midbrain territory is significantly larger in quail than parakeets. Indeed, our data show that normalized midbrain length is 33% greater in quail and that the midbrain to forebrain ratio is 28% greater. This is strong evidence of a significant species difference in early brain patterning.

Parrots comprise one of the several taxa in which life-long learning of new vocal signals used in intraspecific communication is known to occur routinely. The functions and evolutionary bases of this ability are largely unknown. In the budgerigar (Melopsittacus undulatus), males typically imitate their partner’s contact call type during pair formation. However, a female’s initial choice among unfamiliar males is not based on their production of her call type, because birds without prior social contact rarely produce the same call type. Here, we demonstrate that female budgerigars prefer unfamiliar males with calls that are similar to their own, as measured by spectrogram cross-correlation, but which are not imitations. This was shown by training females via operant conditioning to control access to movies of courting males and by systematically varying the audio tracks of these movies. Females learned this task easily and interacted with virtual males as if they were real. This methodology will be useful for exploring functions and mechanisms of social communication, because it eliminates the confounding impact of short-term changes in a stimulus individual’s behavior on a test individual’s response. Our results suggest that the neuroplastic vocal abilities of budgerigars, and perhaps other parrots, have been shaped by sexual selection.

Adult galliform birds (e.g. chickens) exhibit a relatively small telencephalon and a proportionately large optic tectum compared with parrots and songbirds. We previously examined the embryonic origins of these adult species differences and found that the optic tectum is larger in quail than in parakeets and songbirds at early stages of development, prior to tectal neurogenesis onset. The aim of this study was to determine whether a proportionately large presumptive tectum is a primitive condition within birds or a derived feature of quail and other galliform birds. To this end, we examined embryonic brains of several avian species (emus, parrots, songbirds, waterfowl, galliform birds), reptiles (3 lizard species, alligators, turtles) and a monotreme (platypuses). Brain region volumes were estimated from serial Nissl-stained sections. We found that the embryos of galliform birds and lizards exhibit a proportionally larger presumptive tectum than all the other examined species. The presumptive tectum of the platypus is unusually small. The most parsimonious interpretation of these data is that the expanded embryonic tectum of lizards and galliform birds is a derived feature in both of these taxonomic groups.

The telencephalon of birds and placental mammals harbors a proliferative subventricular zone (SVZ) in the subpallium as well as the pallium. Turtles, which are phylogenetically intermediate between bird, and mammals, exhibit at best a rudimentary SVZ. This suggests that SVZs evolved independently in mammals and birds, but it is not clear whether subpallial and pallial SVZs evolved with the origin of birds or in some earlier, non-avian sauropsid ancestor. To answer this question, we examined the brains of embryonic alligators (Ferguson stages 15–22) because crocodilians are the closest extant sister group to birds. To visualize the SVZ we labeled mitotic cells with antibodies against phosphorylated histone-3 (pH3) and proliferating cells with antibodies against proliferating cell nuclear antigen (PCNA). We found that the telencephalon of alligators contains an SVZ only in the subpallium. Because turtles, lizards and amphibians seem to lack SVZs, our finding suggests that a subpallial SVZ evolved in the last common ancestor of birds and crocodilians. Given that placental mammals and birds, but not marsupial mammals or reptiles, possess an SVZ within their pallium, we conclude that a pallial SVZ probably evolved independently in birds and placental mammals.

Parrots, including parakeets, evolved significantly larger brains than other birds, relative to their body size, and they possess a proportionately larger telencephalon. For example, the telencephalon occupies approximately 68% of the brain in parakeets but only 52% in bobwhite quail. The present study was designed to determine when and how this difference in brain region proportions arises during development. To that end, we present volumetric data on the major brain regions in parakeets and bobwhite quail at several stages of embryogenesis, at hatching and, for the parakeets, 1 week after hatching. We also report on the proportional sizes of each region's proliferative and postproliferative zones. One major finding is that parakeets develop a proportionately larger telencephalon relatively late in development and that this late increase correlates with a delay in telencephalic neurogenesis. The most prominent aspect of this delayed telencephalic development is a tremendous expansion of the proliferative subventricular zone in the telencephalon of late embryonic and posthatching parakeets. The second major finding is that the tectum is much smaller in parakeets than in quail at all developmental stages examined, suggesting that the tectum's reduced size is due to an evolutionary change in how much tissue was allocated to become tectum at the time of brain regionalization. Collectively these findings indicate that evolutionary changes in brain region proportions are caused not by a single type of change but by several distinct developmental mechanisms, including changes in brain regionalization and neurogenesis timing.

Adult brains differ among species in the proportional sizes of their major subdivisions. For example, the telencephalon occupies 71% of the entire brain in parakeets (Melopsittacus undulatus) but only 54% in quail (Colinus virginianus). In contrast, the tectum is smaller in parakeets than in quail. To determine whether these differences in brain region size arise because of species differences in cell cycle rates, parakeet and quail embryos were collected at various stages of development (HH24–HH37) and stained with antibodies against proliferating cell nuclear antigen (PCNA), which labels all dividing cells, and phosphorylated histone-3 (pH3), which labels M-phase cells. Analysis of pH3+ cell densities and pH3+/PCNA+ cell ratios were used to compare cell cycle rates across stages and species. Cumulative labeling with bromodeoxyuridine (BrdU) was also used to compare cell cycle rates at stages 24 and 28 in quail. We found that telencephalic cell cycle rates lengthen with age in both species, but that they lengthen significantly later in parakeets than in quail. This species difference in cell cycle rates explains, at least partly, why adult parakeets have a proportionately larger telencephalon. Tectal cell cycle rates also remain elevated for a prolonged period of time in parakeets compared to quail. This seems paradoxical at first, given that the parakeet’s adult tectum is relatively small. However, the tectum is initially much smaller but then grows more extensively in parakeets than in quail. Thus, species differences in adult brain proportions can be traced back to species differences in cell cycle kinetics.

A trait typical of parrots, but rare in other groups of birds, is the acquisition of new learned calls (acquired by copying conspecifics) throughout an individual's lifetime. The significance of this distinctive psittacid trait is not understood. In budgerigars, females preferentially affiliate with unfamiliar males whose contact calls resemble their own during brief dyadic choice trials; also, in forced-pair situations, contact call similarity of members of pairs increases as a result of a male tendency to imitate his mate's call type. The functions of budgerigar call imitation and preference for pre-pairing similarity are currently unknown. Moreover, as budgerigar pair formation occurs over a span of days or weeks, it is important to determine whether birds in breeding colonies assort and proceed to breed on the basis of pre-pairing contact call similarity, and whether high levels of call similarity are maintained after pair formation is complete. To explore these questions, we recorded contact calls of male and female budgerigars before and after they were placed into an aviary equipped for breeding. As predicted, birds paired assortatively based on pre-pairing call similarity. Once birds had paired, their calls converged further in acoustic structure, as previous work had led us to expect. However, after eggs were laid and the males began to feed their mates, the calls of mated birds diverged, suggesting that there might be some cost to maintenance of shared calls. Male care-giving correlated with the degree to which his pre-pairing calls resembled those of his mate, but not with the similarity achieved through convergence. These results suggest that female budgerigars may use a male's pre-pairing call similarity as a predictor of paternal investment. The questions of why such similarity predicts male care-giving, and why calls converge following initial pairing activities, require further work.

Brain evolution is a complex weave of species similarities and differences, bound by diverse rules and principles. This book is a detailed examination of these principles, using data from a wide array of vertebrates but minimizing technical details and terminology. It is written for advanced undergraduates, graduate students, and more senior scientists who already know something about “the brain,” but want a deeper understanding of how diverse brains evolved. The book’s central theme is that evolutionary changes in absolute brain size tend to correlate with many other aspects of brain structure and function, including the proportional size of individual brain regions, their complexity, and their neuronal connections. To explain these correlations, the book delves into rules of brain development and asks how changes in brain structure impact function and behavior. Two chapters focus specifically on how mammal brains diverged from other brains and how Homo sapiens evolved a very large and “special” brain.

Parrots are unusual among birds and animals in general in the extent of their ability to learn new vocalizations throughout life and irrespective of season. The budgerigar (Melopsittacus undulatus), a small parrot that is well suited for laboratory studies, has been the subject of numerous studies investigating the neurobiology of vocal learning. To date, few studies have focused on the function of vocal imitation by parrots. Previous work from our research group has shown that vocal imitation in budgerigars is sex-biased, as males paired with females learn vocalizations from their new mates, but not vice versa. This bias led us to hypothesize that vocal learning has a reproductive function. To test this hypothesis, we conducted two experiments. In the first experiment, we tutored males so that they could produce a call similar to one shared by a group of experimental females. The experimental females were then presented with one of the tutored males and another, equally unfamiliar, male that had not been tutored. We found that the females spent a greater proportion of time in proximity of, and made more affiliative displays toward, the tutored males. In the second experiment, seven males received small bilateral brain lesions that disrupt vocal learning. These males and an equal number of control males were then released into an aviary containing females and reproductive resources. We found that lesioned and control males were equally successful in obtaining social mates, but females mated to lesioned males were more likely to engage in extra-pair activities. These experiments indicate that a male's ability to imitate a female's call can influence the sexual behavior of the female even though lack of imitation ability does not appear to influence social pairing. We hypothesize that mate choice in budgerigars has multiple stages. Upon meeting a strange male, a female quickly assesses its ability for social acquisition of calls by the presence or absence of a call type similar to its own in its repertoire. As courtship proceeds into pair formation, the female assesses the ability of male to learn more directly by the extent of the male's perfection of imitation.

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.

Budgerigars are well known for their ability to imitate sounds, but little is known about the functional contexts in which they use these imitations. Recently, we have shown that male budgerigars consistently imitate the contact calls of the females with whom they are paired. Here we investigate whether males produce these imitations more frequently when they are with their mates than when they are with other females. In one experiment, we established seven budgerigar pairs and then tested each male with his mate and with an unfamiliar female. In the second experiment, we allowed pairs to form freely in an aviary and then tested the males with their mate and with a familiar mated female. In both experiments, the males produced significantly more imitations of their mate's call (defined as calls that were more than 75% similar to the mate's predominant contact call) when they were with their mate than when they were recorded with another female. Under aviary conditions, this difference was due to both a general increase in the males' rate of calling and to an increase in the percentage of the males' calls that were imitations. These data show that male budgerigars modify their contact call rates and repertoires in an audience-specific manner. This audience effect is unusual because it involves a learned vocalization and is extremely specific to a particular audience, namely the mate. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.

Vocal imitation is a complex form of imitative learning that is well developed only in humans, dolphins, and birds. Among birds, only some species are able to imitate sounds in adulthood. Of these, the budgerigar (Melopsittacus undulatus) has been studied in most detail. Previous studies suggested that the vocal motor system in budgerigars receives auditory information from the lateral frontal neostriatum (NFl). In the present study, we confirm this hypothesis by showing that infusions of the GABA agonist muscimol into NFl reduce the strength of auditory responses in a telencephalic vocal motor nucleus, the central nucleus of the lateral neostriatum (NLc). To test whether the auditory information conveyed from NFl to NLc plays a role in vocal imitation, we lesioned parts of NFl and the overlying ventral hyperstriatum (HVl) in seven adult male budgerigars and then examined whether the lesioned males would imitate the calls of females with whom they were paired. We found that, compared to sham-lesioned controls, the lesioned birds were significantly impaired in their imitation of female calls. Yet, the lesioned males were clearly not deaf (e.g., their previously learned calls did not degrade as they do after deafening). Therefore, the data suggest that NFl/HVl lesions impair vocal imitation by reducing the amount of auditory information that reaches the vocal motor system. Interestingly, the females that were paired with lesioned males displayed more vocal plasticity than the females in the control group, and some even imitated their male's prepairing calls.

Current efforts to homologize brain regions across species are often motivated by the expectation that "functional homology" can be deduced from structural homology. Research guided by this "extrapolationist" assumption has been quite successful in molecular biology and, to a lesser extent, in comparative neurobiology. For example, several studies have shown that the hippocampal formation performs similar behavioral functions in birds and mammals, despite significant differences in both anatomy and physiology. However, the extrapolationist assumption can also impede progress because it disregards the possibility that brain regions may change their function during the course of evolution. For example, data gathered at the end of the 19th century on the behavioral effects of large telencephalic lesions were quite confusing until Ferrier recognized that the lesion effects simply differ between species. This realization gave rise to the concept of "functional encephalization," according to which behavioral functions generally shift from "lower" to "higher" brain regions as one ascends the so-called phylogenetic scale. This idea is now discredited, but there is still no adequate theory to explain the species differences in lesion effects. The present paper outlines how one might begin to construct a theory of evolutionary changes in brain function.

The budgerigar (Melopsittacus undulatus) is a promising model species for the study of adult vocal learning. To date, several studies have confirmed the existence of vocal plasticity and, more importantly, rapid imitation of contact calls by adult male budgerigars. Vocal learning has not been investigated in female budgerigars, however. Since one likely function of the contact call is to denote group affiliation, we tested the hypothesis that female budgerigars, when placed into groups, would develop a shared contact call. We recorded the contact call repertoires of eight adult female budgerigars that were unfamiliar with one another, then placed them into two groups. Each group was deprived of visual contact with other birds. Recording sessions continued for the subsequent 8 wks, and behavioral observations were also conducted during this time. Within 4-7 wks, females in both groups converged on a common call type. This rate of convergence is slower than that observed in prior experiments limited to male birds, and much slower than vocal imitation by male budgerigars paired with females. Therefore, while our study documents vocal plasticity in adult female budgerigars, it also suggests that female budgerigars learn new vocalizations more slowly than males do.

Previous studies had concluded that the avian telencephalon develops according to an outside-in schedule of neurogenesis, with relatively little migration of young neuroblasts past older cells. These previous studies had, however, been based on the “cumulative labeling” method, which is less accurate than the “pulse-labeling” method typically used in mammals. In the present study, we pulse-labeled chick embryos by injecting low doses of the thymidine analog bromodeoxyuridine (BrdU) directly into the circulatory system of chick embryos at 6 d of incubation. The brains of these embryos were then examined for anti-BrdU-labeled cells at postinjection survival times from 30 min to 10 d. Comparisons across different survival times, as well as with cases in which BrdU was injected on day 7, suggested that our effective pulse duration is

Budgerigars (Melopsittacus undulatus) are small Australian parrots that can imitate novel sounds in adulthood and therefore serve as a convenient model system for the study of vocal learning in adult animals. Previous anatomical studies had indicated that known auditory regions in the telencephalon of budgerigars are connected, albeit indirectly and rather sparsely, to vocal motor nuclei. Physiological evidence for connections between the auditory and vocal motor systems in budgerigars had been lacking, however. Here, we show that neurons in a telencephalic vocal motor region, i.e., the central nucleus of the lateral neostriatum (NLc), are responsive to auditory stimuli in isoflurane-anesthetized budgerigars. These responses are highly variable from trial to trial and frequently have latencies in excess of 100 ms. Neurons in NLc generally respond better to a budgerigar's own contact call than to a white noise stimulus, but the response preferences of NLc neurons in budgerigars are generally weaker and more diverse than the response preferences of neurons in the high vocal center of songbirds, which is probably analogous to NLc. These data indicate that parrots and songbirds, which have evolved the ability to learn vocalizations independently of one another, have both evolved physiologically effective connections between their auditory and vocal motor systems. Interestingly, however, the anatomical pathways by which the auditory and vocal motor systems interact, and the physiological details of how they communicate, appear to be significantly different between the two taxa.

Almost 100 years ago, in an influential book titled On Growth and Form , D'Arcy Thompson called for the integration of biology with mathematics and physics ( 1 ). Fulfillment of his vision has been slow, but more and more scientists are heeding Thompson's call, attempting to explain problems of “growth and form” through physics and mathematics. An excellent example of this trend is the report by Mota and Herculano-Houzel ( 2 ) on page [74][1] of this issue. They provide a novel mathematical description of how the degree of neocortical folding in mammalian brains varies with other biological parameters, notably cortical thickness and surface area, and they offer the crumpling of a paper ball as a physical model to explain the observed scaling rules. [1]: /lookup/doi/10.1126/science.aaa9101

Darwin's theory of evolution raised the question of how the human brain differs from that of other animals and how it is the same. Early students of brain evolution had constructed rather grand but speculative theories which stated that brains evolved in a linear manner, from fish to man and from simple to complex. These speculations were soundly refuted, however, as contemporary comparative neurobiologists used powerful new techniques and methodologies to discover that complex brains have evolved several times independently among vertebrates (e.g., within teleost fishes and birds) and that brain complexity has actually decreased in the lineages leading to modern salamanders and lungfishes. Moreover, the old idea that brains evolved by the sequential addition of new components has now been replaced by the working hypothesis that brains generally evolve by the divergent modification of preexisting parts. Speculative theories have thus been replaced by testable hypotheses, and current efforts in the field are aimed at making phylogenetic hypotheses even more testable. Particularly promising new directions for comparative neurobiology include (1) the integration of comparative neuroanatomy with comparative embryology and developmental genetics in order to test phylogenetic hypotheses at a mechanistic level, (2) research into how evolutionary changes in the structure of neural circuits are related to evolutionary changes in circuit function and animal behavior, and (3) the analysis of independently evolved similarities to discover general rules about how brains may or may not change during the course of evolution.

Telencephalic organization in birds is so unusual that many homologies between avian and mammalian telencephalic areas remain controversial. Particularly contested is the avian “neostriatum,” which has historically been homologized to either mammalian striatum, lateral neocortex, or endopiriform claustrum. Because homologies between these adult structures have been so difficult to resolve, we have begun to examine how telencephalic development diverges between birds and other vertebrates. To this end, biotinylated dextran was injected into the lateral telencephalon of chick embryos at 3 d of incubation, and the distribution of labeled cells was examined up to 14 d later. The data show that a definite boundary to cellular migration develops just ventral to the neostriatum between 5 and 8 d of incubation. Labeled polyclones within the neostriatum stretch from the ventricular zone to the brain surface and exhibit an increasingly rostrocaudal orientation as development proceeds. Individual polyclones contribute cells to several of the distinct auditory, visual, somatosensory, and olfactory regions within the neostriatum. A comparative analysis suggests that the avian neostriatum develops from a precursor region that in other vertebrates gives rise to olfactory cortex and, when present, to other components of the piriform lobe, such as the endopiriform claustrum and basolateral amygdala. Conclusions about lateral pallial homologies between birds and mammals remain uncertain, however, primarily because so little is known about the development of the lateral pallium in mammals. This lacuna might be filled by applying to mammals the novel fate-mapping method described in the present paper.

A discrete neural circuit mediates the production of learned vocalizations in oscine songbirds. Although this circuit includes some bilateral pathways at midbrain and medullary levels, the forebrain components of the song control network are not directly connected across the midline. There have been no previous reports of bilateral projections from medullary and midbrain vocal control nuclei back to the forebrain song system, but the existence of such bilateral corollary discharge pathways was strongly suggested by the recent observation that unilateral stimulation of a forebrain song nucleus during singing leads to a rapid readjustment of premotor activity in the contralateral forebrain. In the present study, we used neuroanatomical tracers to demonstrate bilateral projections from (a) the rostral ventrolateral medulla (RVL), which may control respiratory aspects of vocalization, to nucleus uvaeformis (Uva), and (b) the dorsomedial intercollicular nucleus (DM), a midbrain vocal control region, to Uva. Both RVL and DM receive descending projections from the forebrain song nucleus robustus archistriatalis, and Uva projects directly to the forebrain song nuclei interfacialis and high vocal center. We suggest that the bilateral feedback projections from DM and RVL to Uva function to coordinate the two hemispheres during singing in adult songbirds and to convey internal feedback of premotor signals to the forebrain in young birds that are learning to sing.

Radial glia are known to have a sparse and uneven distribution in the telencephalon of adult birds. The present study utilizes antibodies against vimentin to reveal a more extensive, and more clearly radial, set of radial glia in the chicken telencephalon during the first half of embryogenesis. This initially extensive radial glial fiber system becomes distorted and reduced between 10 and 14 days of incubation. This reduction coincides with the cytoarchitectural differentiation of the telencephalon into its major adult subdivisions. Because developing neurons tend to migrate along radial glial fibers in both birds and mammals, a topological projection of these major subdivisions onto the embryonic ventricular zone along the radial glial fibers suggests hypotheses about lineage relationships that can be tested by subsequent experimental methods. This analysis suggests that the major components of the avian dorsal ventricular ridge, i.e., the ventral hyperstriatum, the neostriatum with its various subdivisions, part of the archistriatum, and probably also the piriform cortex, all derive from overlapping portions of the lateral pallial ventricular zone. Staining with antibodies against neurofilament suggests that this developmental parcellation of the lateral pallial complex is associated with the development of neuronal fiber systems. J. Comp. Neurol. 387:399–420, 1997. © 1997 Wiley-Liss, Inc.

Numerous scientists have sought a homologue of mammalian isocortex in sauropsids (reptiles and birds) and a homologue of sauropsid dorsal ventricular ridge in mammals. Although some of the proposed th

Numerous scientists have sought a homologue of mammalian isocortex in sauropsids (reptiles and birds) and a homologue of sauropsid dorsal ventricular ridge in mammals. Although some of the proposed th