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 flyfishingdevon.co.uk.  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.