Avian Visual Cognition

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II. Evolution of the Amniote Brain 

Amniote Evolution 

Onto the land: Tetrapod origins. All extant tetrapods (i.e., amphibians, reptiles, birds, and mammals) originally derived from water-dwelling amphibians.  Their amphibial ancestors first appear somewhere in the Devonian period of the Paleozoic era (Norman, 1994).  The Paleozoic amphibians laid jelly-covered eggs in water, as do their modern counterparts.  However, there are many differences between the Paleozoic and modern amphibians.  Generally, the Paleozoic amphibians were rather large (0.6 - 1 meter long) and, although they possessed legs, were primarily water-based and fed mainly on bony fish (Norman, 1994).  

The reproductive strategy of amphibians was not a suitable means of reproduction for those tetrapods who broke with a water-based existence.  Moving from shorelines to farther inland, these forms began to lay Click here to see evolutionary paths their eggs on land, and embryos were protected by membranes (i.e., amnion) and hard shells.  With the innovation of the shelled egg, these organisms were closer to fully integrating into land-based lifestyles. These were the earliest reptiles, whose modern descendants are included in the larger classification of the amniotes. 

The earliest amniotes were the Captorhinida, which eventually gave rise to modern amniotes (reptiles, birds, and mammals).   The ancient reptilian group the Captorhinida derived early in the Carboniferous (360-286 Million Years Ago; MYA) from the anthracosaurs, a group of Paleozoic amphibians (Carroll, 1988).

By the end of the Carboniferous, amniotes could be categorized into three groups on the basis of skull anatomy.  There are openings in the dermal skull roof behind the orbits, whose pattern is used for classifying the ancestral amniotes.  The earliest amniotes, including the Captorhinida, had no such opening, and they are called Anapsida.  Turtles are often included in this group since their skull is entirely covered with bone.  The first group which diverged from the early anapsids are the Synapsida (one temporal opening), which ultimately evolved into mammals.  The second group which separated from the basal anapsids were the Diapsida (two openings), which evolved into reptiles (including dinosaurs) and birds.  

Birds. The diapsids eventually gave rise to the dinosaurs, modern reptiles, and birds.  Diapsids are further divided into two major groups: the Lepidosauromorphs and the Archosauromorphs.  The former group includes sphenondontids, lizards, and snakes, whereas the latter includes archosaurs, such as dinosaurs and crocodiles.  The earliest birds are phylogenetically close to the archosaurs, but the precise origin and evolution of birds is still the matter of some debate.  The first true birds appear sometime in the late Jurassic or perhaps earlier (for details see the section Dinosaurs Among Us?, this chapter). 

Major radiations of birds occurred during the Cretaceous (135-65 MYA) and the Tertiary period of the Cenozoic era (65-1.9 MYA).  In the 85 million year span between the Jurassic and the beginning of the Cenozoic, two major groups of Cretaceous birds arose, the Enantiornithes and the Ornithurines.  The Enantiornithes ("opposite birds") were so named because of their metatarsals being fused proximal to distal, which is opposite that of modern birds (Feduccia, 1996).  The Ornithurines eventually led to currently existing modern forms, along with extinct loon-like Hesperornithiformes (toothed birds, mostly flightless swimmers) and tern-like Ichthyornithiformes (toothed flying birds which probably fed on fish).  From existing evidence, it appears none of the toothed birds survived the Cretaceous extinction.  There is some scattered evidence that the ancestors of modern shorebirds may have extended back into the late Cretaceous and survived the massive extinctions in which the dinosaurs perished.  

Most modern birds have ancestors which appeared by the end of the Miocene (5.5 MYA).  The diversification of birds after the Cretaceous extinctions was very rapid, with the ornithurine birds diverging into Click here to see number of bird species over time almost all the present orders within 5-10 million years.  Modern bird orders appear in the late Paleocene and by the Oligocene most of the orders of birds recognized today were in existence.  By the Miocene the dominant land birds had become the passerines.  However, none of those actual Miocene species during that period survive today.  All modern species probably have evolved only in the last 1-2 million years.  Data from studies of the accumulation of point mutations causing amino acid substitution in proteins between all 27 orders of birds indicate a relatively modest change between species.  This conservation of genetic sequences indicates a rapid divergence of species in only the past million years or so (Feduccia, 1996).

Birds are the most successful of the terrestrial vertebrates, found on every continent and in almost every ecological niche.  Birds are a diverse group, with over 9,000 species, compared to the amphibians (3,000 species), reptiles (6,000), and mammals (4,100); (Chatterjee, 1997).  There are 27 to 28 orders of modern birds that can be classified into two superorders, the Palaeognathae and Neognathae.  The Paleaognathae include the emu, ostrich, rhea, cassowary, tinamous, and kiwi; most of these forms have lost the ability to fly.  The Neognathae encompass all other orders of birds and is divisible into the passerine (perching) and non-passerine subgroups.  The passerines incude zebra finches, swallows, and sparrows; the non-passerines include owls, chickens, quail, and pigeons. 

Mammals. Mammals evolved from Mesozoic synapsid reptiles, which included the pelycosaurs and therapsids.  Mammals diverged from this reptilian group around the late Triassic / early Jurassic, about 200 million years ago.  The Mammalia consist of three major divisions, representing three branches which derived from the therapsids (mammal-like reptiles).  The three present classifications of mammals, the monotremes, marsupials, and placentals, arose at an early stage and thus have evolved independently during that time.  The monotremes are egg-laying forms, whose only modern representatives are the duck-bill platypus (Ornithorhynchus) and the spiny ant-eater, or echidna (Tachyglossus and Zaglossus).  The marsupials have eggs but hatch them inside the body and bear the young in an embryonic condition. The young then continue their development typically in an abdominal pouch, feeding on the motherís milk.  The placentals make up the third classification and includes a huge variety of organisms inhabiting sea (e.g., dolphins, whales), air (e.g., bats), and land (e.g., elephants, primates, horses).  The earliest placental mammals were insectivores.  Sometime in the Mesozoic, they diversified into several lines of descent, one of which was the Lipotyphla, who continue to the present day in the hedgehogs, shrews, and moles.  From the Lipotyphla there derived a branch called the Menotyphla whose living members are the tree and elephant shrews. Three branches at different points in evolutionary history became the Dermoptera (flying lemurs; Galeopithecus and Galeopterus), the Chiroptera (bats), and the Primates (Walls, 1942).  Given the early divergence of the monotremes and placentals, caution is warranted when looking to the egg-laying mammals (e.g., echidna or platypus) as a kind of ancestral link between reptiles and modern placental mammals. 

Amniote Brains 

Many similarities exist in the overall organization of modern amniote brains, and in the basic organization of their visual systems.  Our knowledge of the brains of ancestral amniote forms is limited to what can be derived from fossil skulls.  Observations of the cranial structure provide gross morphological measures, and endocasts can even provide some surface detail.  From such data tentative guesses about the olfactory bulbs, forebrain structure, optic lobes, and cerebellar development can be made.  Considering the relative size and development of these structures can help somewhat in constructing what kind of lifestyle the organism exhibited.  This can be considered with environmental and geographical factors probably existing at the time, along with estimated predator/prey ratios, et cetera, to construct a picture of how these long extinct organisms lived.  Most extra-retinal structures relevant to discussions of avian visual evolution are found in the midbrain and forebrain regions.  

Tectum. The tectum of the mesencephalon is an important visual structure in the amniote visual system.  The tectum receives topographic, highly organized projections from visual, auditory, and somatosensory systems.  The "maps" formed from this input are in good register with each other, allowing the organism a well-formed representation of its sensory space.  The organization of this structure also supports the coordination of behaviors elicited by visual, auditory, or somatosensory stimuli in the sensory space.  The optic lobe, or optic tectum, plays a prominent role in the visual behaviors of modern reptiles and birds.  Its importance in mammals has historically been over-shadowed by research into the more prominent geniculo-striate system.  However, the importance of the mammalian optic tectum (i.e., superior colliculus) in visual behaviors is becoming better appreciated with studies in cats and primates (Chalupa, 1977; Petersen et al, 1985, Ungerleider & Pribam, 1977).

Dorsal Thalamus & Pallium. Structures in the diencephalon and telencephalon are also crucial to visual behavior in amniotes.  The major visual recipient area of the diencephalon in all vertebrates is the dorsal thalamus, which is composed of several nuclei which relay ascending sensory information to the telencephalon.  Dorsal thalamic nuclei in amniotes which receive ascending visual input from the retina receive such input either directly (as in the thalamofugal or lemnothalamic pathway) or indirectly via the tectum (as in the tectofugal or collothalamic pathway).  The telencephalon is divisible into both a dorsal and ventral component, the pallium and subpallium, respectively.  The pallium is divisible into dorsal, lateral (olfactory or piriform), and medial (limbic) divisions.  The subpallium includes the basal ganglia and septum.  

Common to amniote forebrain organization is that ascending sensory information is relayed through dorsal thalamic nuclei to parts of both the pallium and subpallium.  The pallial areas tend to be specialized into discrete regions in receipt of afferents from one particular sensory modality.  In non-mammalian amniotes, the dorsal pallium contains dorsal cortex.  In birds, a rostral expansion of the dorsal pallium which receives visual input from the lemnothalamic system has been termed the visual wulst.  The dorsal and lateral pallia in mammals have undergone a spectacular expansion, developing into the laminar isocortex.  The six-layered cortex, with its marked sulci and gyri, is often considered the defining characteristic of mammalian brains, and was once considered a pre-requisite for true higher-level sensory and cognitive activities.  Subsequent research into the cognitive and sensory capacities of birds and other organisms has discredited this idea.  The differences, however, between the avian/reptilian dorsal ventricular ridge and mammalian isocortex are instructive in both the attempt to reconstruct visual system evolution and understand visual processing in these very different brains.

DVR and Cortex

The dorsal ventricular ridge (DVR) is a pallial structure unique to the non-mammalian amniotes (reptiles and birds).   The telencephalon of different vertebrate forms start similarly.  A vesicle at the rostral end of the neural tube is the foundation of the telencephalon in all vertebrates.  Subsequent development after this formation differs among the amniotes.  Reptiles and birds exhibit the formation of the DVR, which protrudes into the lateral ventricle and forms the lateral walls of the telencephalon. The DVR can be further divided into anterior (ADVR) and basal portions (BDVR; called archistriatum in birds).  In mammals, the floors of the hemispheres protrude into the lateral ventricles to form the basal ganglia, while the telencephalic roof expands and forms the distinctive lamination of the isocortex (Ulinski, 1983).

Type I and Type II DVR. The DVR is divisible into two basic patterns (Type I and Type II) based on the distribution of neurons.  The first pattern is called Type I DVR, or a corticoid band-core arrangement (Butler, 1980).  Type I DVR demonstrates three relatively distinct zones, defined by the cytology and distribution of neurons in the ADVR (Ulinski, 1983).  These zones have the following characteristics: 

  • Dorsal Zone: relatively cell-poor zone with a cluster of juxtaependymal neurons whose dendrites extend concentrically with the ventricular surface

  • Second Zone: relatively larger numbers of stellate neurons which form clusters, with the neurons' somata touching

  • Ventral Zone: consists of stellate neurons with both scattered individual neurons and occasional clusters present

The stellate neurons of the second and third layers can either be spiny or spine-poor.  These neurons have a radial orientation which enables them to form interconnections with each other.  This first pattern of DVR organization is found in snakes, tuatara (Sphenodon), turtles, and most lizards.  

In birds and crocodiles a second type of organization is seen, called Type II DVR, or a nuclear arrangement.  Type II DVR does not possss a distinct periventricular cell cluster zone in ADVR.  In addition there are isolated neurons as well as prominent neuronal clusters scattered throughout the forebrain in Type II DVR (Ulinski, 1983).  Other characteristics include: 

  • Dorsal region: juxtaependymal neurons with dendrites concentric to the ventricular surface

  • Individual and clustered neurons are typically spiny with stellate-shaped dendritic fields possessing variable numbers of spines

In Alligator there is a tendency for clusters to form a periventricular zone within the dorsomedial area but not in other areas as in Type I reptiles.   In birds, clusters of neurons also occur throughout the ADVR.  Several distinct types of neurons have been recognized in different avian species, but most neurons can be characterized as having stellate-shaped dendritic trees with varying numbers of spines.  In addition, there are neurons with radially oriented connections seen in several sensory areas of birds (e.g., ectostriatum to peri-ectostriatal belt; interconnections of Field L areas); (Ulinski, 1983). 

Despite differences in DVR organization, common to all reptiles and birds is the basic connectivity of the ADVR and BDVR.  Ulinski (1983) suggested that the basic organization of the DVR is to serve as a linkage between sensory inputs and motor outputs; an interface between sensory and perceptual processing and mechanisms which modulate behavior.  ADVR receives visual, auditory, and somatosensory information and sends outputs to the BDVR and basal ganglia.  It also appears that this is the basic function of mammalian isocortex.  One of the overriding questions in comparative neurobiology is the relationship between the neural groupings characteristic of DVR and the laminar arrangement of neurons found in the mammalian isocortex.  This debate usually centers around the question of whether their is a homologous relationship between DVR and cortex.  

Comparing DVR & mammalian isocortex. The six layered isocortex in mammals may not be as different from the DVR of diapsid reptiles and birds as it appears.  The radial, outward migration of neuroblasts from the ventricular surface of the telencephalon results in the basic six layered pattern characteristic of mammalian isocortex.  Isocortical neurons include the pyramidal cells in the third and fifth layers and several non-pyramidal varieties.  Despite the morphological differences between DVR and cortex, these areas may process information similarly.  The isocortex is in a similar processing position to that of DVR, being an area which links sensory inputs and directing motor responses (Ulinski, 1983).  Anatomical connections indicate that the nuclear groupings of DVR could be homologous to certain areas of mammalian isocortex.  With the possibilities of convergent evolution, and alternative theories of cortical evolution, however, DVR / isocortex homology is still a debated theory (Butler & Hodos, 1996).  There is some evidence that a simple definition of cortex as a laminar arrangement of cells and fibers may be too restrictive; some of the same populations of cells present in cortex may be present in nonmammals, with similarities in neural connections but arranged in a different fashion (Hodos, 1976). 

The ADVR and mammalian isocortex share similarities in the organization of their sensory circuits.  The ADVR has been compared to the mammalian isocortex based on the similarities of sensory circuits between the nuclear groupings of non-mammalian amniote brain and the distinctly laminar mammalian isocortex (Northcutt, 1981; Karten & Shimizu, 1989; Reiner, 1993; Butler, 1994; Veenman et al., 1995; Karten, 1997).  Both the mammalian and avian systems are characterized by major thalamic input to the telencephalon (e.g., layer IV in mammals; the core ectostriatum in birds) which is then relayed to overlying areas (layer IV projections to layers II and III in mammals; core ectostriatum projections to peri-ectostriatal belt and overlying neostriatum in birds).  Additionally, in mammals, there are descending projections from layers II and III to layers V and VI, from which output is directed to the tectum.  From the intermedial, lateral neostriatum in birds there are descending projections to the archistriatum (Ritchie, 1979; Husband et al., 1995), which in turn is a source of projections to the tectum (Zeier & Karten, 1971).  The comparisons of cortical layers with the nuclear groupings of birds noted above indicate a similar pattern of information processing in amniote brains.  These similarities could be due to homology; however, they may also be unrelated to the condition of the ancestral amniote brain, having arisen through other mechanisms.  The source of the similarities in patterns of amniote brain organization, therefore, remains unresolved.  

Avian ADVR organization, in conjunction with the outdated "-striatum" designation for avian forebrain structures, may unnecessarily confuse comparisons of neuroanatomy and function of amniote sensory systems.  The ADVR in birds is organized into cytoarchitectonically distinct cell groups along the dorsal-ventral axis: a medially located neostriatum (including the ectostriatum) and a dorsally located hyperstriatum.  Several commonalities between the isocortex and ADVR are apparent when considering the arrangement of sensory-recipient areas in telencephalon.  Both isocortex and ADVR have the cell groups of their sensory circuits (i.e., cortical layers or ADVR nuclei) organized perpendicular to the lateral ventricle.  The afferent and efferent connections, as well as their radial pattern of organization, indicate that isocortex and ADVR share similar general principles of telencephalic sensory processing.  These similarities may have arisen with the ancestral stem reptile which gave rise to modern amniotes.  The stem reptiles may have possessed nonlaminar groupings of functionally specialized neural populations (Shimizu & Karten, 1993).   However, anatomical and functional similarities could have also evolved through convergence.  In other words. these similarites could be homoplastic rather than homologous.  In any event, the neural systems of birds, reptiles, and mammals may have much more in common than is evident from the distinctly non-laminar appearance of sauropsid (aivan and reptile) brains.

Brain Evolution 

Reconstructing the evolution of the brain from the early tetrapods to modern forms poses several challenges.  The fossil record is incomplete and detailed endocasts are rare.  However, in those fossils and endocasts that have been discovered there are some reasonable conclusions to be drawn about brain organization.  We can begin to reconstruct the rudiments of overall brain morphology from ancestral to modern forms.  By analyzing the similarities in modern forms, from the crocodiles, turtles, birds, and mammals we can make assumptions about the condition of the neural structures within the brain in their amniote ancestors.  Such reconstructions, however, must take into account the long divergence of these forms from their common ancestor.  

Forebrain Expansion. The pattern of the evolving brain has been generally marked by changes in the ratio of midbrain and forebrain structures, and in the expansion of the forebrain itself.  These transitions are seen in the evolution from stem reptiles to the "mammal-like" reptiles (carnivorous pelycosaurs and therapsids) to the ancient mammals.  Forebrain expansion probably occurred throughout the Jurassic and Cretaceous in all of the lineages leading to modern birds, reptiles, and mammals.  In a genus close to the stem reptiles, Diadectes had a somewhat tubular and narrow midbrain and forebrain, superficially resembling that of the lungfishes and amphibians of today (Ulinski, 1983). 

However, there is evidence modern amphibians have undergone simplifications (e.g., in skeletal structure).  These present forms have also had a great deal of evolutionary time to evolve and adapt to their particular niches; therefore caution is warranted when considering them as models of the ancestral reptilian brain.  Early archosaurs, such as the pseudosuchians of the middle Triassic, also exhibited narrow midbrains and forebrains.  By the late Triassic, however, the forebrain of archosaurs like Desmatosuchus had grown to similar proportions of that seen in the Crocodilia (Hopson, 1979). 

In the line of forms leading to mammals, pelycosaurs exhibited narrow midbrains and forebrains.  Eventually, a gradual increase in the relative size of brain versus body size is seen.  The therapsids, such as Probainognathus, possessed telencephalons like elongate tubes.  By the Mesozoic, the mammals show an expansion of the forebrain, such as that in Ptilodus.  Later placental forms exhibit further widening and expansion of the forebrain, including the sulcal patterns of the brain surface.  One interpretation of the aforementioned trends is that the forebrain expansion in the ancestors of modern reptiles (and eventually birds) reflects the evolution of the DVR, while the evolution of the forebrain in mammals reflects the expansion of the basal ganglia and the uniquely mammalian isocortex (Ulinski, 1983).

Emergence of the DVR. The stem reptiles probably possessed a Type I DVR.  The basic DVR organization could probably be found in the organisms which existed prior to their divergence into the lepidosaur and archosaur lineages.  Sensory system sophistication may be reflected in the emergence of Type II DVR in birds.  The Type II neuronal arrangement involves both the migration of cells away from the ventricular surface and a quantitative increase in the size of the ridge.  This presumably indicates the opportunity for more complex information processing capabilities and perhaps more adaptability in behavioral responses to stimuli.  A type II lizard, Tupinambis, is an active arboreal forager which preys on smaller vertebrates and insects using visual, auditory, and olfactory senses.  Tupinambis has the quantitatively largest DVR of all lizards (Butler, 1980).  In addition, the gecko, a member of the type I DVR class, shares the foraging and arboreal habits of the iguanas and have large DVRs which overlap with species in the lower ranges of the type II reptiles (Butler, 1980).  Increases in volume and a trend toward nuclear configurations of DVR are correlated in snakes, lizards, crocodiles, and birds which exhibit terrestrial and/or arboreal habits with active predation or active avoidance of predation (Butler, 1980).  It would appear that expansion of the forebrain in the ancestral reptiles reflected a growing sophistication in sensory processes, motor control, and behaviors, supported by the development of DVR. 
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