Monday, April 27, 2015

Why hummingbirds taste sweets but chickens can't

Chicken tastes good but, like most birds,
 chickens can't taste sweets1.
What about hummingbirds?

Hummingbirds taste sweets because natural selection remade a savory receptor inherited from ancient fish into a unique sugar receptor. The elegant research was published in 2014 2.

In mammals, fish, amphibians, and reptiles, taste buds (shown to the left) distinguish five taste modalities - sour, bitter, salty, savory (also called umami) and sweet. The sweet and umami receptor proteins are "dimers", pairs of proteins that wind back and forth across the cell membranes of taste cells like the green taste receptor proteins shown in the cell membrane to the right. Sweet receptors, inherited from a fish ancestor, are paired T1R1 and T1R2 proteins while umami receptors are T1R1-T1R3 dimers.
Thanks to Maude Baldwin, a graduate student at Harvard University, we have recently learned a great deal about the story behind hummingbird sugar receptors2.

At the start of her work, Maude Baldwin knew that:
   = Hummingbirds feed on nectar so can't be sugar-blind.
   = T1R1 and T1R3 genes are present in chickens3.
   = The T1R2 gene in the ancestral sugar receptor is
      completely missing from a chicken's DNA3.

As fish evolved into ancient reptiles and reptiles gave rise to birds, when was the gene lost? When Maude looked at the DNA of several different species of birds, she found T1R1 and T1R3 but no T1R2. She examined alligator (primitive reptile) DNA and found all three genes. From this result, she surmised that some early ancestors of birds, probably dinosaurs, must have lost the T1R2 gene2

Next, Maude Baldwin made a very clever guess:
  • Maybe natural selection, operating over many millions of years, repurposed the hummingbird T1R1-T1R3 receptor by transforming hummingbird T1R3 into a sweetie detector? 
As she searched for ways to test that hypothesis, Maude talked with Stephen Liberles, a Harvard medical school faculty member specializing in the cell biology of chemoreception. Liberales connected Maude with Yasuka Toda, another graduate student halfway around the globe at the University of Tokyo.

Yasuka Toda and her colleagues had invented a sophisticated technique to study human T1R1, T1R2, and T1R3 function by inserting the corresponding genes into engineered laboratory-cultured human kidney cells (HEK293T).  Whenever sugars bind to T1R1-T1R2 or whenever savories bind T1R1-T1R3, the HEK293T cell emits a flash of light.  The cell is a reporter that announces sugar binding with its bioluminescece.

In response to a request from Maude Baldwin, the Tokoyo group inserted hummingbird T1R1 and T1R3 genes into their reporter HEK293T cells and applied either sugary or savory stimuli.  The modified cells with only one hummingbird gene (T1R1 or T1R3) showed no response. However, cells with both hummingbird T1R1 and hummingbird T1R3 flashed brightly when exposed to sugar.

Maude Baldwin's schrewd guess was proved correct! The ancestral dimer for savories (T1R1-T1R3) has become adapted for sugars in hummingbirds.

Not content with this beautifully clear result, the team went further and asked exactly which parts of the modified T1R3 protein were most critical.

Proteins are long loopy chains of amino acids. The Tokyo group constructed protein "chimeras". Chimera means a multi-species hybrid. The word traces back to a mythical Greek monster-lion with the head of a goat on its back and a snake in place of the tail.  The hummingbird team concentrated on the Venus Flytrap Domain of the hummingbird T1R3 gene (binds sugars) into which they stitched sequences of the chicken T1R3 gene (binds savories).

The chimeric T1R3's allowed the researchers to map exactly which amino acids are necessary to bind sugars, as shown in color on the T1R3 model to the right.

Next, the scientists exposed hummingbird T1R1-T1R3's in HEK293T cells to a broad panel of tastants (sucrose, various sugars, artificial sweetners like aspartame, and others). By making an inventory of tastants that triggered light flashes, they defined the taste spectrum for this human cultured cell with hummingbird T1R1-T1R3 receptors.

Do the impressive laboratory results fit with the natural world?  Does the taste spectrum, deduced from precisely controlled laboratory experiments with cultured human cells, really mesh with the way that hummingbirds taste different sugars?

To find out the answer,  Baldwin tested Ruby-throated Hummingbirds in her Harvard laboratory and another collaborator, Klaus Klasing, tested Anna's hummingbirds in the Santa Monica Mountains of California with a panel of tastants. The birds briefly tasted pure water (upper) but drank long at the sugar solution (lower) in the video from Baldwin's lab.

The real-world choices of intact birds in Massachusetts and California agreed well with the taste spectrum predicted by the HEK293T cell chimeras.  Hummingbirds have evolved the taste talent that matches their feeding ecology because natural selection retuned the ancestral savory sensor into a sugar sensor.
This astounding tour de force demonstrates the best practices of 21st century science - reaching across disciplinary boundaries to ask about animal adaptations and their evolution.

In closing, we should identify the roles of the members of the team:
  • Maude Baldwin, graduate student at Harvard who spearheaded the research,
  • Scott Edwards, Professor of Organismic and Evolutionary Biology and Curator of Ornithology in the Museum of Comparative Zoology and Baldwin's  faculty sponsor at Harvard,
  • Yasuka Toda (graduate student) and colleagues Associate Professor Takumi Misaka and Tomoya Nakagita in the Department of Applied Biology at the University of Tokyo who developed the cellular assay system for tastant proteins, 
  • Mary J. O'Connell in Dublin, Ireland who provided computational and bioinformatics expertise, 
  • Kirk Klasing at UC Davis who did field tests on Anna's hummingbirds, and 
  • Stephen D. Liberles, a cell biologist at Harvard's medical school who specializes in the molecular cell biology of chemoreception, including responses to pheromones.
For much of the 20th century, the chemical ecology of birds was neglected, but bird taste and olfaction are fast becoming hot topics.

Baldwin's lovely study of hummingbird sweet taste is particularly solid because it sweeps from natural behavior in the field to sophisticated molecular and cell biology in the lab and ties the story together with evolution, the unifying intellectual theme of all biology.

There are many related research questions. No ancestral sugar receptor gene has been found in any bird yet many species, for example house finches, are attracted to colorless sugary solutions.

It is heartening to learn from her webpage that Maude Baldwin is now applying her impressive intellect to bird pheromones.  In the next few decades, I expect myriad exciting new insights about avian chemical communication channels and their biological significance. See for example our speculation about the role of pheromones in Sandhill Crane reproduction.

References & Notes

1. BP Halpern 1982. Gustatory nerve responses in chickens. Am J Physiology 203:541-4

2. MW Baldwin, Y Toda, T Nakagita, MJ O'Connell, KC Klasing, T Misaka, SV Edwards, and SD Liberles, 2014. Evolution of sweet taste perception in hummingbirds by transformation of the ancestral umami receptor. Science 345:929-933.

3. P Shi, J Zhang, 2006. Contrasting modes of evolution between vertebrate sweet/umami receptor genes and bitter receptor genes. Mol Biol Evol 23:292-300.

4. Taste modalities are repeatedly lost in evolution. Penguins, like all birds, lack the ancestral sugar receptor. In  addition, penguins have lost the functional genes for both umami and bitter taste receptors. See  H Zhao, J  Li,  J Zhang, 2015. Molecular evidence for the loss of three basic tastes in penguin. Current Biology 25:R141-R142.

Sunday, April 21, 2013

"Bird brained" is a bum rap (2013 version)

The earliest vertebrates on the earth were fish. When their descendants first ventured into land environments, they had to return to the sea to lay their eggs.

About 300 million years ago, one vertebrate lineage made a major evolutionary breakthrough by evolving a special sac, called an "amnion", that protects an embryo from dessication when the egg is laid away from water.

The stem amniotes became reptiles that dominated terrestrial environments and gave rise to therapsids, ancestors of modern mammals, and dinosaurs, ancestors of modern birds.

Most modern mammals have remained quadrupeds that use all four appendages for walking. Many dinosaurs became bipedal, with pedestrian bodies balanced on the rear legs so that front legs that could be used for catching and manipulating food.1

In some bird-like dinosaurs, front legs evolved into wings. Manipulative skills were largely relegated to the beak at the end of an elongate flexible neck, seen to the right in a primitive Archaeopteryx from the Late Jurassic, 147 million years ago.2

Natural selection bio-engineered birds for flight. Flying isn't accomplished simply by plastering feathers on front appendages. Birds became deft flying machines over hundreds of millions of years by reorganizing their body parts. They transformed into a compact streamlined shape that enclosed major organ systems and all large muscles, as gracefully described in Gary Kaiser's recent book, The Inner Bird.1

Flight required precise motor coordination and wide-angle surveillance to process a snowstorm of visual input and thus to avoid collisions. Many of the transitional innovations for flight aren't well preserved in fossil bones, but the shape of the brain can be deduced by the shape of a skull. The progress toward a modern avian brain is already evident in the Archaeopteryx brain which has been beautifully reconstructed after CT scanning of an ancient fossilized skull.3

The brain of Archaeopteryx  (to the right) is about three times bigger than that of a comparable modern lizard but still much smaller than the brain of a modern bird. The enlarged optic lobes (ol), olfactory tract (ot), and well-developed inner ear likely reflect the importance of vision, olfaction, and hearing. The expanded cerebellum (cb) and cerebrum (c) suggest improved fine control of movement and increased cognitive sophistication in this primitive bird-like dinosaur.

A large asteroid struck at the K-T (Cretaceous-Tertiary) boundary, disrupting the earth's ecology and decimating most groups of dinosaurs.  Birds and mammals came through the chaos, Their better brains were among the most critical adaptations that permitted survival4 in the 65 million years since. 

As the body plans of birds and mammals adapted to contrasting lifestyles, their brain anatomies divergedAll vertebrate brains begin in the embryo as a chain of hollow bulbs, the forebrain, midbrain, and hindbrain, at the front of the nerve tube. The upper part of the embryonic forebrain is called the pallium (named for the woollen cloak that Popes confer on Archbishops) and the lower part, the basal ganglia. In the course of embryonic development, nerve cells in the pallium and basal ganglia multiply and mix together according to an elegant program that establishes the adult brain anatomy.

The embryonic pallium becomes the cerebral cortex, a complex living plywood that often wrinkles and folks as it laps over the basal ganglia in adult mammals. To support teeth and chewing muscles, mammals evolved a massive bony skull that is also serves as an armored brain vault.

Bird lifestyles preclude a massive skull. A heavy head, pendulous and swaying at the tip of an elongate neck, would be an aeronautical liability, so natural selection kept birds' heads small and bird brains compact.  Nonetheless, birds got brighter as their forebrains reorganized over hundreds of millions of years of evolution.

Bird brain architecture is broadly reminiscent of modern minimalist "tiny houses".  Bird brains are space-efficient. Pallial neurons within an avian brain are clumped in nodules, called nuclei. Like scores of tightly-packed garlic cloves, the nuclei are squeezed together and linked to one another via nerve processes.   One researcher reported that a bird brain has twice as many cells per unit volume as a mammal brain.

                             Picture from Jarvis et al, 2005.

The compact bird brain is protected by a thin but amazingly resilient skull. If we think of the mammal skull as like a cast-iron helmet, then a bird skull is like a Kevlar helmet. [See the footnote below for more on the amazing skulls of birds.]

Why haven't bird brains gotten more respect?

As scientific knowledge accumulates and is passed down, concepts and terminology constrain our understanding of the natural world. Brain terminology and nomenclature were hampered by many historical accidents.

Mostly working from animal dissections, Erasistratus of Alexandria (304 BC – 250 BC) described and named the cerebrum and cerebellum. Renaissance physicians like Vesalius broke open the skulls of human felons after their executions, found similar structures, and pondered the role of each brain component.

Nineteenth and early 20th century comparative neuranatomists were guided by their classical concept of Darwinian evolution - "up" from amphibians to reptiles to mammals to man. Ludwig Edinger, the father of comparative neuroanatomy5 and many others who followed6, viewed brain evolution as a process akin to the deposition of layers in sedimentary rocks. New centers were wrapped around older ones: first the mesencephalon at the bottom, next the diencephalon, then basal ganglia were layers over the diencephalon, and finally, the pallium on the upper surface.

According to the "ladder of life" evolutionary perspective, man is at the top of the ladder. The apex for brain evolution is the mammalian six-layered neocortex, best elaborated in humans. Higher mental processes are attributed to the cortical cerebral hemispheres while instinct, reflexes and vegetative functions are assigned to the underlying basal ganglia.

Since the bird brain has no wrinkled cerebral cortex, Edinger and his contemporaries reasoned that the majority of a bird's forebrain is basal ganglia. Since they saw bird brains as those with a puny pallium, they concluded that a bird's brain must be largely restricted to simple responses.

The Edinger view of bird brain anatomy remained fashionable among biologists until almost the end of the 20th century. At the same time, It was consistent with behaviorist psychology dogma, then dominant in psychological and ethological circles across North America. Birds were regarded as creatures of reflexes, instincts, and fixed action patterns.

One gifted neuroanatomist, Harvey Karten, was prescient.  His incisive yet understated landmark paper, published in 1969, noted that comparisons between bird and mammal brains "were often tenuous" . He concluded that "at the present time, we are still ignorant of the nature of the greatest number of neuronal elements in the avian forebrain" 7.  In circumspect language carefully buttressed by his original data, Karten argued that the avian pallium is respectably large, but differently organized than the mammalian cortex.

Late 20th century molecular embryology richly vindicated Harvey Karten's 1969 model.

The molecular biology explosion over the last fifty years has enriched not only our understanding of genetics but also of physiology and embryology.  Markers of gene expression allow mapping of gene activity in time and space and thus permit precise definition of the phenotypes of individual cells or groups of cells.  One can find the sites where chemical signals are made, where they are stored, where they are released, where each kind of receptor is located, and how these patterns change with alternations in physiological state. One can reconstruct regulatory circuits.

Gene expression data allows neuroscientists to see where and when particular cell populations arise and then allow them to be tracked through development. Thus one has objective criteria to reliably identify homologs of brain components across species, orders, and classes. Recent systematic studies of gene expression in bird embryos revealed that Karten was quite right8,9.  "The adult avian pallium comprises about 75% of the telecephalon"8 (forebrain) in both birds and mammals.
Names matter. In science as in politics, names color logic and bias conclusions.  The traditional venerated bird brain nomenclature, based on centuries of gross dissections and meticulous studies of pickled tissue slices, was recognized as archaic, outdated, and misleading. The very terms used to describe bird brains reinforced outmoded concepts.

A prestigious Avian Brain Nomenclature Group assembled at Duke University in 2002 to revise bird brain terminology. The cartoons below, drawn by Zina Deretsky for the National Science Foundation10, summarize the conclusions. Notice particularly, at the top left, the small green cap of pallium as depicted according to outdated neuroanatomy, in contrast to the much larger green areas of bird pallium in modern view (bottom left).

The new anatomical nomenclature is congruent with the cognitive revolution in psychology that began at mid-20th century in Europe and is now in full-bloom across the globe.  The 21st century nomenclature facilitates understanding of How birds think.  It helps open new perspectives for understanding animal minds.

Brains are ancient on this earth. In the embryo, virtually identical genes specify the major divisions of the brain in bees, in birds, and in human babies. Neurotransmitters, receptors, brain mechanisms, and developmental decisions reflect very deep homologies that reach back to genes and brains of ancestors from half a billion years ago11

Evolution offers perspective at many levels. Avian neuroscience and mammalian neuroscience overlap widely and deeply. Commonalities in genes, in nerve cell circuits, in division of labor across anatomical brain units, and in behavioral outputs, are legion.

Natural selection has produced an elegant design for bird brains and these brains do wondrous mental feats. Later blogposts will review recent research on bird brains and behavior and will attempt to provide some tentative insights into bird minds.


Footnote: How do birds minimize concussions when they impact windows?

All brains are fragile. But the weight constraints for an efficient flight machine preclude a massive protective skull. Yet, as we all know, birds frequently collide with windows and fall to the ground.  Some die, but quite often the stunned bird recovers in a few minutes.
Why is there relatively little damage?

Two explanations are common:
    First, birds are protected by their "pillow" of head feathers that softens impacts.
  Second, although bird skulls are light and thin, the bone is exceptionally dense and tough12. To use a broad analogy, bird skulls are like Kevlar while mammal skulls are like "Old Ironsides". Even when birds are killed by collisions with windows, actual fractures of skull bones are rare13

Two additional explanations deserve further consideration.
  Third, since the skull bones are "pneumatized" with internal air pockets14, the skull might function like a helmet of bubble-wrap or styrofoam.  In a fascinating older paper that often goes unnoticed, JG and DL Harrison further suggested that air sacs also function like "an inflatable air-suit" that buffers the brain from surges in blood pressure and thus prevents blacking out when birds dive sharply.15
  Fourth, avian neuro-architecture might inherently confer shock resistance. The globular centers packed together in the bird pallium might be less prone to ripping and tearing than the six-layered mammal pallium.

Further research might elucidate the exquisite physiological adaptations of the bird body plan and also (we hope) might facilitate the invention of more humane protocols for poultry slaughter16.


1. Kaiser GW 2007. The Inner Bird - Anatomy and Evolution. U British Columbia Press, Vancouver.
2. Witmer LM  2004. Inside the oldest bird brain. Nature 430:619-620.
3. Alonso PD, Milner AC, Ketcham RA, Cookson MJ, Rowe TB 2004. The avian brain and the inner ear of Archaeopteryx. Nature 430:666-669.
4. Milner AC, Walsh AS 2009. Avian brain evolution:new data from Palaeogene birds (Lower Eocene) from  England. Zool J Linnean Soc 155:198-219. 
5. Smith E 1901. Notes on the natural subdivision of the cerebral hemisphere. J Anat Physiol 35:431-454.
6. Edinger L 1888-1901. Investigations on the Comparative Anatomy of Brain Volumes. Vol 1-5 (Translated from German) Moritz-Diesterweg, Frankfurt/Main.
7. Karten, HJ 1969. The organization of the avian telencephalon and some speculations on he phylogeny of the amniote telecephalon. Ann NY Acad Sci 167:164-179.
8. Jarvis ED, Güntürkün O, (25 other authors) Reiner A, Butler AB, 2005. Avian brains and a new understanding of vertebrate brain evolution. Nature Neuroscience 6:151-159.
9. Reiner A, Perkel DJ, (25 other authors), Jarvis ED, 2004.  Revised nomenclature for the avial telencephalon and some related brainstem nuclei. J Comp Neurol  473:377-414.
10. This color plate uses new nomenclature from reference 4.
11. Strausfeld NJ, Hirth F, 2013. Deep homology of arthropod central comples and vertebrate basal ganglia. Sciene 340:157-161.
12. Dumont ER, 2010. Bone density and the lightweight skeletons of birds. Proc Roy Soc B 277:2193-2198.
13. Veltri CJ, Klem D(Jr) 2005. Comparison of fatal bird injuries from collisions with towers and windows. J Field Orinothol. 72:127-133.
14. Hogg DA, 1990. The development and pneumatisation in the skull of the domestic fowl (Gallus gallus domesticus). J. Anat. 169:139-141.
15. Harrison JG, Harrison DL,1949. Some developmental peculiarities in the skulls of birds and bats. Bull Brit Orinthol Club 69:61-70.
16. Erasmus MA, Turner PV, Nykamp SG, Widowski TM, 2010. Brain and skull lesions resulting from use of percussive bolt, cervical dislocation by stretching, cervical dislocation by crushing and blunt trauma in turkeys.167: Vet Rec 850-858.

Revised 05/23/2011, 9/30/2011, 9/7/2012, 10/4/2012, 4/20/2013

Tuesday, October 2, 2012

Is Sandill Crane dance entirely innate? Does it show motor learning?

Crane dance is iconic. All 15 species of cranes communicate with elaborate body language1. Comparisons among species reveals clear and consistent distinctions.
Do species differences in dance prove crane displays are innate?         We think the question is inappropriate and based on a false dichotomy.

Animal behavior was validated as "real science" when the 1973 Nobel prize in Physiology went to Karl von Frisch, Konrad Lorenz, and Nikolaas Tinbergen.

At the time of that 1973 prize, neurophysiology was limited to electrophysiology of individual nerve cells and included little more than hand-waving at the psychological realm that emphasized learning, emotion and mental processes. 

The research of these 1973 Nobelists was solidly grounded in precise observation of a defined set of behaviors, with a perspective that dodged between the sentimentality of anthromorphism and the formal dogmas of behaviorist psychology rampant in their day. The scientific rigor of these ethologists first bought a measure of scientific respect to biological study of behavior. To encourage a thorough examination of a behavior, Tinbergen2 suggested that each behavior should be explained according to:
  • Function (adaptation)
  • Phylogeny (evolution)
  • Causation (mechanism), and
  • Development (ontogeny. 
None-the-less, ethology also had its own dogmas -  for example, that animal behavior is composed of "fixed action patterns" that are expressed when genetically-defined "sign stimuli" act on an "innate releasing mechanism". 

What physiological mechanisms underlie the fixed-action-pattern concepts? In his early writings, Lorenz attempted to explain behavior by analogy with a hydraulic model which is engagingly depicted in the animated gif borrowed from  Tinbergen used an electrical circuit model.

Neither analogy was readily transferable to flesh and blood.

Bird songs as models for behavior research

The scientific approach to the songs of birds emerged at the same time as the birth of ethology, but "birdsong science" avoided tortured mechanistic analogies. Instead, research on birdsong focused on physiological linkages between behavior observations in the wild and experimental neuroscience in the laboratory.

Songs of nightingales, canaries, and other birds had delighted esthetes and challenged scientists since the Renaissance.

Birdsong research became tractable due largely to the use of the sound spectrograph, a device  invented in World War II for underwater eavesdropping on enemy submarines. In pioneering laboratory and field investigations, William Thorpe, Peter Marler and many others (see Nature's Music3) recorded and dissected the songs of birds and meticulously cataloged the species-specific differences.

Birders (and birds themselves) can readily identify each bird species by its unique song. Does this prove that bird songs are innate?

What happens when young songbirds start to sing? They copy the songs of their fathers:
  • First, young males memorize a song "target image" by listening to a tutor -- usually their father.
  • Then, weeks or months later, the young birds begin to sing an adult tune on their own as they acquire an ability to duplicate the memorized song of the tutor. 
  • As they practice, birds embellish and perfect the song. The best singer get the best territories and attract the best females.
As Peter Marler put it:
"when we adopt a developmental approach, which is what Tinbergen was advocating, the instinctive/learned distinction loses its logical underpinnings."2
Since the mid-20th century, there has been a torrent of scientific papers on the progressive changes as young birds acquire adult song and on the roles of the various brain centers that preside over singing.

"Practice makes perfect."

Birdsong vocal learning is now an attractive general model for research on the cellular basis of motor learning. One example of motor learning is a high school athlete becoming proficient at pitching a curve ball. The rough draft of the "throwing" behavior is already present in our brain and is perhaps innate.  But training and practice profoundly refines that rough draft.

The brain centers and nerve networks

In the last few decades, laboratory scientists have identified the brain centers and networks responsible for birdsong and vocal learning.

The neurocircuit diagram (right), adapted from one published by Michael Brainard's lab at the University of California-San Francisco, offers a reconstructed layout of birdsong pathways5 in the brain. The centers are:
  1. posterior centers (HVC, RA...) that drive motor neurons of the syrinx [shown in black],
  2. anterior centers (Area X, LMAN....) required for song learning [shown in gray & red],
  3. centers that motivate a bird to sing [circled in pink], and
  4. sensory centers [not shown] that monitor each song emitted and thus allow comparisons of output with other songs held in memory.
Now in the 21st century, research of many labs is directed toward exposing the physiological and molecular bases for song variability and individual specificity. Birdsong has become an important biomedical model for probing the cellular bases of learning. We will discuss the centers in more detial in future Blogposts.

As birdsong science took off, the underlying neuroscience of bird brains experienced a revival due to results from molecular embryology. The neuro-geographical map of bird brains was re-interpreted and revolutionized in the last decade (Reiner et al., 20046 and Jarvis et al., 2005 and discussed in our earlier Blogpost).

Birdsong and crane dance

Walking, flight, and birdsong improve with practice, as does the acquisition of dance skills by young Sandhill Cranes (known as colts). Very young crane colts display to each other and interact with their parents, starting in the first few days after hatching.  Over the ensuing weeks, the parents "encourage" the colts to dance, as shown in the image below when the colt was 21 days old.

In the weeks following, the  colt flail-dances with the father parent at 35 days of age (below left below) and dances smoothly with parents by 40 days later (below right).

Sandhill crane displays are complex. Some of the dance lexicon is depicted in print1 and on the web and progressive acquisition of dance skills is generally summarized on a related page.

The table outlines intriguing behavioral parallels between the acquisition of adult song in young male zebra finches and acquisition of dance displays in young cranes.

For finches, the neuroscience/brain center correlates of the behavior are under intensive study in several major research laboratories. There is yet no data on the brain centers that preside over dance in cranes.  However, the acquisition of crane dance behavior is strongly suggestive of motor learning and that is underlain by brain circuits like those for birdsong.

Crane dances are refined over many years. Dance performance probably improves over the 2-3 years while young cranes dance in crowds to assess potential mates. Furthermore, we have a photographic chronicle that demonstrates marked shifts in the selection of postures and the execution of displays for the dances between the male and the female of a pair that we have watched on their nest territory for over a decade.

As Peter Marler noted (quoted above), the instinctive/learned dichotomy for birdsong disappeared when scientists in the 1970's used a developmental approach. Our developmental approach to crane dance appears to yields the same conclusion: crane dance is not wholly innate or wholly learned.

Dance reflects motor learning as the bird refines and develops genetically based capabilities. For dancing of cranes as for vocal learning of songbirds, motor learning optimizes better communication among members of a species.

Birdsong and vocal learning are generally thought to have evolved independently in three avian lineages: oscines (higher passerines), hummingbirds, and parrots. In an important study, Erich Jarvis' lab at Duke University and his German colleagues have shown that brain centers for birdsong are akin to brain motor centers, like those concerned with walking and flying.8 In zebra finches, the "white rat" for birdsong, dance choreography seems to be transmitted from tutor father to pupil son.9 We believe that the ontogeny of dance in cranes reflects motor learning in a fourth avian lineage.

Finches progressively refine and improve their songs by comparing with a memory of their tutor's song which they heard during a sensitive period in their young lives. Whether cranes use memories of their parents or the responses of dance partners (or both) remains to be investigated.  It may be that crane motor learning is lifelong, unlike songbird vocal learning where sensitivity to the tutor is restricted to a particular period in a young bird's life.

1. DH Ellis, SR Swengel, GE Archibald, & CB Kepler, 1988. A sociogram for cranes of the world. Behavioral Processes 43:125-151
2. N Tinbergen, 1963. On aims and methods in ethology Zeitschrift fur Tierpsychologie 20:410-433.
3. P Marler & H Slabberkoorn, 2004. Nature's Music - The Science of Birdsong  Elsevier 
4. P Marler, 2004.  Chapter 1: Science and birdsong: the good old days, pp 1-38 in Nature's Music.
5. TL Warren, EC Turner, JD Chaerlesworth & MS Brainard, 2011. Mechanisms and time course of vocal learning and consolidation in the adult songbird. J Neurophysiol 106: 1806-1821.
6. ED Jarvis, O Gunturkun, (25 other authors) A Reiner & AB Butler, 2005. Avian brains and a new understanding of vertebrate brain evolution. Nature Neuroscience 6:151-159.
7. A Reiner A, (27 colleagues), Jarvis ED, 2004. Revised nomenclature for avian telencephalon and some related brainstem nuclei. J Comp Neurol 473:377-414.
8. G Feenders, M Liedvogel, M Rivas, M Zapka, H Horita, E Hara, K Wada, H Mouritsen & ED Jarvis, 2008. Molecular mapping of movement-associated areas in the avian brain: a motor theory for vocal learning origin. PLoS ONE 3: e1768, DOI 10.1371/journal.pone.0001768
9. H Williams, 2001. Choreography of song, dance, and beak movements in thr zebra finch (Taeniopygia guttata),
J exp Biol  204:3497-3506

Sunday, September 30, 2012

Bird brains are different - An introduction to the blog

"Now that there are strong grounds to dispute Descartes' contention that animals lack the capacity to think, we have to ask just how animals do think."    (emphasis added)   Terrace1
Birds are our distant relatives. In the 300 million years since bird and mammal lineages separated, anatomy, physiology, behavior, and life-styles have diverged: wings vs legs, feathers vs hair, hard-shelled eggs vs placenta, reflect natural selection operating over countless generations. A classic scientific conundrum is understanding the divergence in the most complex organ - the brain.

How birds think asks what we know and what we don't about brain mechanisms that mediate behavior and physiology in birds. Our approach will emphasize comparative biology and attempt to exploit the deep commonalities between bird and mammal brains.

When pioneer anatomists cracked open the skulls of birds and mammals, the brains looked rather similar. Both have the major divisions of the ancient vertebrate brain-plan. In the drawing, the cerebrum (brown region) and cerebellum (gray) are prominent in mammals (top) and birds (middle).2

With the birth of neurophysiology and pharmacology in the early 20th century, scientists showed that  birds, mammals, and other vertebrates share in common the same tools for intercellular signaling:
  • a set of chemical neurotransmitters and neuropeptides, and
  • a library of membrane-bound protein receptors specific for each neurotransmitter.
However, when microscopists peered inside the brains of birds and mammals, their internal organizations looked dissimilar. Although some patches of nerve cells were recognizable in both brains, others were puzzling because the internal architectures of the brains were so different.

Discovering common origins between cell masses of bird and mammal brains is something like trying to understand continental drift during geologic time on the earth. Masses of cells, like continents or parts of continents, moved gradually over evolutionary time.  "Nerve cell drifts" in birds and mammals followed different plans in three dimensions.


Nerve cells in the mammal cerebral neocortex are stacked like layers in plywood (left, above) while those in the bird cerebrum are clumped in nuclei, crowded together, rather like cloves in a large garlic bulb (right, above).  The diagrams have been borrowed from a paper of Clifton Ragsdale and colleagues.3

How should we relate layers to clumps? What nerve cells in birds correspond to what cells in mammals? How did ancestral nerve cell types get scrambled differently as the brains of birds and of mammals evolved in parallel?  Reconciling the discrepancies proved daunting.

In the absence of ancient mummified brains, scientists looked carefully at the development of brains in embryos. The observations were subject to many interpretations. Over decades, various theories were advanced but none was universally accepted. 

A common wiring legacy

In October 2012, clarity emerged. A seminal paper from Clifton Ragsdale's laboratory at the University of Chicago tracked markers showing gene expression as nerve cells develop in birds, mammals, and turtles. The results were a Rosetta Stone for brains.
The same nerve cell types, each identified by a unique gene expression profile, are found in both birds and mammals. Each precisely identified cell lineage could be reliably mapped in birds and in mammals. As embryos develop, identifiable neuron types could be tracked through each stage.

The results of comparative mapping were startling. A stable pattern of cell-to-cell contacts (synapses) has endured through evolutionary time, in spite of the selective pressures that yielded different overall geography and often different cellular geometry in bird and mammal brains.

The Ragsdale results reveal the existence of an underlying wiring legacy - a shared heritage of nerve cell circuits shared by birds and mammals.  

Put another way, the input and output characteristics for specific lineages of nerve cells are stable; they have not changed even though the cells came to migrate in different ways during embryonic development and the adult cells have assumed different shapes in birds and mammals. 

. One of Ragsdale's examples is a chain of four nerve cells.  The input for the pathway comes from a neuron (dTh) in the thalamus, a brain region that lies the beneath the cerebrum; next there are two cells (green and blue) within the cerebrum, and finally the output (red) runs to the brainstem (Bst).

The neuron from the thalamus (black in the diagram) inputs to a cerebral nerve cell (green) that connects to a second cerebral cell (blue). These cells play similar roles in both bird and mammal brains. But since the anatomy and geography of the cerebra have diverged, green cells are found in layer 4 of the modern mammal cerebral neocortex whereas they are packed within a nucleus of the cerebral entopallium in birds. Blue cells are in layer 2/3 of mammals and in the nidopallium of birds3.

When biologists try to map a brain function between mammals and birds, it can be confusing. Careful physiological, cellular, and developmental research on living creatures is required. 

Consider for example high-level cognitive functions, like paying attention, planning, multi-tasking, integrating converging sensory information, and monitoring of actions.

The "executive crossroads" for high-level cognitive functions in mammal brains is the prefrontal cortex (PFC) which lies at the front of the cerebrum. The equivalent center for convergence and coordination in bird brains, called the nidopallium caudolaterale (NCL), is at the rear of the cerebrum.

The drawing, borrowed from a paper of Onur Güntürkün4, shows brains of a human and a pigeon, viewed from the left side. The executive center of the human brain (PFC)  is at the front while that of the pigeon (NCL) is at the back of the cerebrum. 

Deciphering the bird brain is intrinsically exciting because it helps us understand and better appreciate bird behaviors that so many people find entrancing.

Perhaps even more interesting is the possibility that a better understanding of commonalities and contrasts between brains might offer new perspectives on the connection between anatomy and mentality.

In How birds think, we will draw upon field observations, laboratory experiments, and comparative biology to explore function, development, and evolution of bird brains.

1. HS Terrace, 1987. Thoughts without words. In Mindwaves: Thoughts on intelligence, identity, consciousness, ed. C. Blakemore & S. Greenfield, Oxford Press.
2.  RG Northcutt RG, 2011. Evolving large and compact brains. Science 332:926-927.
3. J Dugas-Ford, JJ Rowell & CW Radsdale, 2012. Cell-type homologies and the origins of the neocortex. Proc Nat Acad Sci US 109:16974-9, doi:10.1073/pnas.1204773109. 
4. O Güntürkün, 2012. The convergent evolution of neural substrates for cognition. Psychol. Res. 2:212-219.