BIO 554/754
Ornithology

Nervous System: Brain & Senses

See The Bird in Black

An updated version of these notes can be accessed from a new "Avian Biology' page
(http://people.eku.edu/ritchisong/avian_biology.html).

 

The Avian Nervous System consists of

The functions of the avian nervous system are to

Comparison of the spinal cords of a typical bird (left), snake (center), and human (right).
 In the bird spinal cord, the enlargement in the cervical region is due to the many axons needed to control the
muscles of the wings. The lumbar enlargement is due to the many axons that control the legs. The thoracic section
is rather thin because movement of the wings and limbs need not be coordinated (so fewer interneurons needed).
(Source: http://faculty.washington.edu/chudler/spemap.html)

Accumulation of testosterone in the spinal cord of a bird with an elaborate courtship display -- Elaborate courtship displays are common features of the reproductive behavior of male birds. However, little is known about their neural and hormonal control. One bird that performs such a display is the Golden-collared Manakin (Manacus vitellinus) of Panamanian forests. Adult males, but not females, perform a display requiring substantial neuromuscular control of the wings and legs. Schultz and Schlinger (1999) tested the hypothesis that steroid sensitivity is a property of neurons in the manakin spinal cord. Males and females were captured from active courtship leks, treated with drugs to block steroidogenesis, injected with 3H-labeled testosterone, and the spinal cords were removed and processed for autoradiography. Most sex steroid-accumulating cells were found in the cervical and lumbosacral enlargements. Because motor neurons in these areas control muscles of the wings and legs, these cells may have multiple behavioral functions, perhaps innervating muscles controlling the elaborate dancing and wing-snapping of these birds. This evidence indicates that sex steroids may control diverse behaviors in male birds in part by acting directly on the spinal neural circuits.
Figure to the right. Distribution of sex steroid-accumulating cells in the manakin spinal cord. Each symbol represents three cells. The cord is illustrated at three levels: Ventral, the cord ventral to the bifurcation of the ventral horns; dorsal, the cord dorsal to the beginning of the bifurcation of the dorsal horns out to their tips; and middle, the remaining cord between the ventral and dorsal levels.

Due to common ancestry, the brains of reptiles & birds are similar. However, birds have relatively larger cerebral hemispheres & cerebella. In addition, birds have larger optic lobes & smaller olfactory bulbs (Husband and Shimizu 1999).


Source: http://www.pigeon.psy.tufts.edu/avc/husband/avc5vpth.htm

The avian brain includes:
  • medulla - part of the brainstem; includes neurons that help control heart rate, respiration, & blood pressure
  • optic lobe - part of the midbrain; relatively large in birds compared to other vertebrates (reflecting the importance of vision for most birds)
  • cerebellum - involved in the coordination of skeletal muscle activity; relatively large (reflecting the need for precise coordination of muscle activity during flight)
  • cerebrum - consisting of 2 cerebral hemispheres plus olfactory lobes; the olfactory lobes are relatively small in most birds (suggesting a poor sense of smell, but some birds do have a well-developed sense of smell)

Source: http://www.uoguelph.ca/zoology/devobio/210labs/ecto3.html


Side views of  Zebra Finch & human brains. Inset (next to human brain) is the
Zebra Finch brain to the same scale (From: Jarvis et al. 2005).

Avian brains and a new understanding of vertebrate brain evolution -- A consortium of neuroscientists (Jarvis et al. 2005) has proposed a renaming of the structures of the bird brain to correctly portray birds as more comparable to mammals in their cognitive ability. The scientists assert that the century-old traditional nomenclature is outdated and does not reflect new studies that reveal the brainpower of birds. "We believe that names have a powerful influence on the experiments we do and the way in which we think," wrote the consortium members. "For this reason, (we have) reconsidered the 100-year-old terminology used to describe the avian cerebrum. Our current understanding of the avian brain requires a new terminology that better reflects these functions and the homologies between avian and mammalian brains." The old terminology -- which implied that the avian brain was more primitive than the mammalian brain -- has hindered scientific understanding. 

The  revised nomenclature for avian brains is aimed at replacing the system developed in the 19th century by Ludwig Edinger, the father of comparative neuroanatomy. Edinger used prefixes such as palaeo- ("oldest") and archi- ("archaic") to designate structures in the avian brain and neo- ("new") to designate supposedly new structures, particularly in the mammalian brain. "According to this theory, the avian cerebrum is almost entirely composed of basal ganglia, a structure involved only in instinctive behavior, and the malleable behavior thought to typify mammals exclusively requires the so-called neocortex," wrote the researchers. However, "We have to get rid of the idea that mammals -- and humans in particular -- are the pinnacle of evolution. We also have to understand that evolution is not linear, but an intricate branching process. So, we can't automatically expect to track a structure in the human brain back to other current vertebrate species."


Image credit: Zina Deretsky - NSF


Classic view of avian and mammalian brain relationships. Ac, accumbens; B, nucleus basalis; Cd, caudate 
nucleus; CDL, dorsal lateral corticoid area; E, ectostriatum; GP, globus pallidus (i, internal segment; 
e, external segment); HA, hyperstriatum accessorium; HD, hyperstriatum dorsale; HIS, hyperstriatum 
intercalatus superior; HV, hyperstriatum ventrale; L2, field L2; LPO, lobus parolfactorius; 
OB, olfactory bulb; Pt, putamen (From: Jarvis et al. 2005).

Jarvis et al. (2005) describe studies demonstrating that so-called "primitive" regions of avian brains are sophisticated processing regions homologous to those in mammals. These regions carry out sensory processing, motor control and sensorimotor learning just as the mammalian neocortex. Studies have also shown that the avian and mammalian brain regions are comparable in their genetic and biochemical machinery. The neocortex and related areas in the mammalian brain are derived from a region in the embryonic cerebrum called the pallium, which means mantle or covering. Edinger thought, however, that most of this region in the bird cerebrum was part of the basal ganglia. Accordingly, he gave them names that ended in the basal ganglia term “-striatum”, a practice he also employed in naming the parts of the mammalian basal ganglia. As a result of the recent studies, the consortium recommends such changes as renaming the avian brain region called the "archistriatum" as the "arcopallium," (arched pallium); and renaming the region that includes part of the true basal ganglia in birds, the "palaeostriatum primitivum" and the "ventral palaeostriatum" which sits below the pallium as the "pallidum" (pallidal or pale domain). 


Modern consensus view of avian and mammalian brain relationships. Solid white lines are lamina (cell-sparse 
zones separating brain subdivisions). Dashed grey lines divide regions that differ by cell density or cell size; 
dashed white lines separate primary sensory neuron populations from adjacent regions. Abbreviations that 
differ from above diagram (classic view): E, entopallium; B, basorostralis; HA, hyperpallium apicale; 
HI, hyperpallium intercalatum; Hp, hippocampus; MD, mesopallium dorsale; MV, mesopallium 
ventrale (From: Jarvis et al. 2005).

Jarvis pointed out that "there were people in the field of avian neurobiology who knew the real structures behind these names and knew the names were wrong." For example, researchers not familiar with studies demonstrating the sophistication of the avian brain could not understand how birds could exhibit sophisticated cognitive abilities with brains that held only what the nomenclature designated as the equivalent of the human basal ganglia. This new nomenclature will help people understand that evolution has created more than one way to generate complex behavior -- the mammal way and the bird way. And they're comparable to one another. In fact, some birds have evolved cognitive abilities that are far more complex than in many mammals."

The cerebral hemispheres of birds, like those of other vertebrates, consists of 2 regions:

All vertebrates have a cerebrum based on the same basic plan; major phylogenetic changes are due to loss, fusion, or enlargement of the various regions.


Source: http://www.auburn.edu/academic/classes/zy/0301/Topic19/Topic19.html
 


Schematic showing the organization of a sensory system in the bird/reptilian telencephalon (A) and the location
of the homologous neurons in the mammalian cortex (B). The avian telencephalon has only a thin lateral cortex, and
a prominent protrusion into the lateral ventricle (V), the dorsal ventricular ridge (DVR). The dorsal ventricular ridge contains
several different neuronal populations, directly corresponding to those found in different layers of the mammalian neocortex,
including thalamic recipient neurons, interneurons, and descending projections that leave the cortex to contact brainstem
and spinal cord neurons. The dorsal ventricular ridge protrudes into the ventricle of birds and reptiles, and hence for
many years was erroneously thought to be homologous to the mammalian basal ganglia (BG). In mammals (B),
homologous populations of neurons are found within distinct layers of the cortex. The striking similarities in basic neuronal
properties and circuits in reptiles, birds, and mammals led to the proposal that the specific neurons evolved prior to the
evolutionary appearance of mammalian cortex. Hp, hippocampus (Karten 1997).


From: Jarvis et al. (2005).

Increasing sophistication in sensory processes, motor control, and behavior in reptiles and, particularly, birds over evolutionary time may have been the selective force driving the development & increasing volume of the avian pallium.  The basic function of the pallium is to serve as a linkage between sensory inputs and motor outputs; an interface between sensory and perceptual processing and mechanisms which modulate behavior. This is also the basic function of the mammalian cortex.

Schematic summary comparing the neuronal circuitry of auditory pathways in the dorsal ventricular ridge of the avian telencephalon and the equivalent neocortical circuit of the mammalian auditory cortex. In the avian forebrain, the populations of neurons corresponding to the individual layers of mammalian cortex are organized as clusters, rather than layers. This circuit in the mammal is represented as a simplified three-layered cortex, consisting of a layer of thalamic recipient neurons (receiving sensory input; blue) forming layer IV, a group of interneurons (yellow) forming the more superficial layers, and a group of descending motor neurons (DTEs) (red), the output neurons of this cortical region, forming layers V and VI. The morphology of individual neurons, their transmitters, and physiological properties at each parallel step of the circuit are virtually identical in bird dorsal ventricular ridge and mammalian cortex (Karten 1997). 
As Autumn Approaches, New Nerve Cells Put Chickadee Foraging On Fast Track - Every autumn, chickadees gather seeds and store them in hundreds of hiding places in trees and on the ground. Over the winter that follows, chickadees faithfully re-visit their caches to feed. The chickadee's spatial memory is remarkable enough, says Colin Saldanha, assistant professor of biological sciences at Lehigh University. But it is what happens inside the tiny songbird's brain that Saldanha finds amazing. In the fall, as the chickadee is gathering and storing seeds, Saldanha says, its hippocampus, the part of the brain responsible for spatial organization and memory in many vertebrates, expands in volume by approximately 30% by adding new nerve cells. In the spring, when its feats of memory are needed less, the chickadee's hippocampus shrinks back to its normal size, Saldanha says. Songbirds are the first vertebrates in which brain growth during adulthood has been found to occur, Saldanha says. By studying neurogenesis in the Black-capped Chickadee, Saldanha hopes to learn how hormones help guide the brain's development and reorganization. He is particularly interested in the role played by the hormone estrogen in the growth of the hippocampus. Songbirds (like most vertebrates) make estrogen in their ovaries; scientists have determined that their brains also express aromatase, the enzyme that makes estrogen. Perhaps not surprisingly, the area of the songbird brain with the highest estrogen-making capability is the hippocampus. "We know hormones affect the reorganization of the brain in ovo, in utero and during the early physical development of most vertebrates," Saldanha says. "We are trying to figure out whether the ability to make estrogen in the hippocampus is helping the dramatic reorganization of the [adult] brain." His goal is to determine whether estrogen is being made in the cellular body or in the synapse, and whether the location of this estrogen-making ability changes seasonally. "We're looking at the ability of nerve cells and connections to make estrogen in the brain and asking if this ability is involved in brain reorganization," he says. 
Among birds, the DVR is perhaps best developed in crows, parrots, & passerines (i.e., 'intelligent' birds), and is less developed in pigeons & doves, quail, & domestic chickens. As stated by David Attenborough, "The level of intelligence among birds may vary. Each generation of birds that leaves the protection of its parents to become independent has the inborn genetic information that will help it to survive in the outside world and the skills that it has learned from its parents. They would never have met the challenge of evolution without some degree of native cunning. It’s just that some have much more than others."  (see 'Tool Use in Birds')

In general, the cognitive abilities of birds are increasingly appreciated as more complex than presumed several years ago. For example, as listed by Jarvis et al. (2005):

So, many birds have cognitive abilities that are quite sophisticated, and some birds and mammals have cognitive abilities that clearly exceed those of all other birds and mammals.
Bird IQ Index -- Corvids and falcons top the list, followed by hawks, woodpeckers and herons. The world's first bird IQ index was compiled by Louis Lefebvre based on 2000 published observations of unusual feeding behavior. Observation reveal that birds do not deserve their reputation for being featherweight thinkers. Among the examples of bird intelligence was a story of war zone vultures which waited by a minefield for stray animals to be blown up. There have also been many sightings of fly-fishing herons, with heronsl catching  insects and laying them on the water's surface to attract fish. Gulls frequently drop shells onto rocks to break them  and tits in England learned to open milk bottles left on people's doorsteps. Birds also use tools. The most skilled tool-users were New Caledonian Crows, which fashioned specially shaped implements out of leaves to catch insects. At the bottom of the IQ index, in no particular order, were the Emu, theOostrich, New World quails, and the night-jar. Parrots were disappointingly uninventive despite having the biggest brains of any bird. The exceptions were Australian parrots, which were "extremely opportunistic". "I can remember seeing them at the train station where they were loading sacks of grain, and the parrots were ripping up the bags," said Lefebvre. 

http://www.opinion.telegraph.co.uk
Bird Brains Like Human Brains: Episodic Memory Processes Similar - Birds can remember not only where, but when, they hid food items & even dig up less perishable food if too much time has passed & their favorite worms have probably rotted (Clayton and Dickinson 1998). The study of Scrub Jays (Aphelocoma californica) marks the first demonstration of episodic, or event-based, memory in animals other than humans. This type of memory is referred to as “mental time travel” because it involves mental images of past events. To remember where you put your car keys, you might “see” yourself walking into the house the night before & placing the keys on a table. Previous work had shown that birds can remember what kind of food they had stored & where they had hidden it, even without sensory clues like smell & appearance. But making decisions based on the timing of past events is crucial to episodic memory. In the study, N. S. Clayton  (Univ. of California-Davis) & Anthony Dickinson (Cambridge Univ.) allowed Scrub Jays to store their favorite food (wax worms) on one side of a sand-filled tray & peanuts on the other side. Jays retrieved the wax worms if less than four hours old, but birds that had learned that wax worms decompose avoided older worms in favor of peanuts. 
Half-asleep birds choose which half dozes - Birds that are literally half-asleep - with one brain hemisphere alert & the other snoozing - control which side of the brain remains awake. The brain hemispheres take turns sinking into the sleep stage characterized by slow brain waves. The eye controlled by the sleeping hemisphere shuts, while the wakeful hemisphere's eye stays open and vigilant. Birds also can sleep with both hemispheres resting at once. To check whether birds can control half-brain sleeping, Rattenborg et al. (1999) rows of Mallards napping. Decades of studies of bird flocks led researchers to predict extra vigilance in the more vulnerable, end-of-the-row sleepers. Sure enough, the end birds tended to keep peeled the eye on the side away from their buddies. Mallards snuggled into the inner spots showed no preference for gaze direction. Also, birds dozing at the end of the line resorted to single-hemisphere sleep, rather than total relaxation, more often than inner ducks did. Rotating 16 birds through the positions in a four-duck row, the researchers found outer birds half-asleep during some 32% of snoozing time versus about 12% for birds in internal spots. "We believe this is the first evidence for an animal behaviorally controlling sleep and wakefulness simultaneously in different regions of the brain," the researchers said. The results provide the best evidence yet for a long-standing conjecture that single- hemisphere sleep evolved as creatures scanned for predators. The preference for opening an eye on the lookout side could be widespread. Useful as half-sleeping might be, it's only been found in birds and such aquatic mammals as dolphins, whales, seals, and manatees. Presumably, keeping one side of the brain awake allows a sleeping animal to surface occasionally to avoid drowning, explains Rattenborg. 

Proportion of time in each behavioral state for nonmigrating (top) and migrating (bottom) birds. The proportion of every 
10-min period spent in each sleep/wakefulness state was averaged for all birds: wakefulness (black), drowsiness 
(gray), slow-wave sleep (blue), and REM sleep (red). Note that overall sleep propensity in migrating birds is greatly diminished between about 22:30 and 06:00. Note also the increased propensity for REM sleep from 18:00 to 20:00 as compared to the same 
time period when not migrating.

No rest for the weary? -- Every spring and fall, billions of songbirds fly thousands of miles between their summer breeding grounds and their wintering grounds in Mexico, and Central and South America. While some birds fly during the day, most fly at night. The migratory pace of most birds—as well as the increased activity required to sustain migrations—suggests little time for sleep. Yet field observations indicate that presumably sleep-deprived fliers appear no worse for wear, foraging, navigating, and avoiding predators with aplomb. How do songbirds cope with so little sleep? 
      Rattenborg et al. (2004) characterized the activity levels of White-crowned Sparrows with motion-detection measurements and video recordings, and placed sensors on their brains to monitor their seasonal sleep patterns. Brain recordings showed a seasonal difference: migrating birds spent about two-thirds less time sleeping than nonmigratory birds and fell into REM sleep (the dream stage of sleep, marked by rapid eye movements) sooner. Cognitive tests - birds performed a task involving pecking a key for  seed - revealed that birds in the nonmigrating state suffered cognitive deficits when sleep-deprived, but displayed an “unprecedented” ability to maintain cognitive function in the face of ongoing sleep loss in the migratory state.
       These results suggest that birds sleep much less during migration, though it's impossible to know for sure without recording the birds in action. And it is unclear what molecular mechanisms jumpstart the migratory mindset. Whatever the mechanism, the unprecedented imperviousness of migrating songbirds to sleep deprivation, clearly warrants further testing. Source: (2004) No Rest for the Weary: Migrating Songbirds Keep Their Wits without Sleep. PLoS Biol 2(7): e221.

Sense organs

Birds "Feel" Their Prey Under the Sand - Red Knots (Calidris canutus) can locate their favorite food (shellfish) in wet sand by inserting their beak half a centimeter into the sand for a few seconds (Piersma et al. 1998) This ability was demonstrated in experiments in which researchers hid small stones in the sand. Because stones do not send out any signals, the ability of Knots to detect them must be based on the sensitivity of their beaks to differences in currents in the water in wet sand between the individual grains, stones, or shells. Knots used in the experiments were unable to find hidden stones in dry sand. At the end of their beak, knots have clusters of 10 to 20 Herbst corpuscles that are sensitive to differences in pressure. When the bird sticks its sensitive beak into the sand at low tide, it produces a pressure wave because of the inertia of the water in the interstices between the particles. The pattern thus created betrays the presence of objects larger than the grains of sand. The rapid up-and-down movements of the bird's beak loosen the grains of  sand, which then become packed together more tightly, displace the interstitial water, & cause the residual pressure around the object to increase. The nature of their localizing ability means that knots cannot distinguish between stones & shellfish in the sand, which is why they rarely look for food in areas where the sand contains stones, no matter how much shellfish could be found there. 
www.abc.net.au/science/scribblygum/March2000/default.htm

Smell (olfaction):

Anatomical features of procellariiforms indicate that they should have a well-developed sense of smell. Within the complex turbinate
structure of a snow petrel's nose (above), large amounts of surface area are lined with olfactory epithelium, containing cells that
detect odor (light green). A puffin's nose is smaller and has less olfactory epithelium. Procellariiforms are often called "tubenose"
seabirds because of the prominence of these structures, seen clearly in a White-chinned Petrel’s profile (right). They also have
enlarged brain structures that process scents (Nevitt 1999).

Taste:

Nervous System: Brain & Special Senses II

Literature Cited

Clayton, N. S. & Dickinson, A. D. 1998. What, where and when: evidence for episodic-like memory during cache recovery by Scrub Jays
Nature 395: 272- 278.

Curcio, C.A. & K.A. Allen. 1990. Topography of ganglion cells in human retina. J. Comp. Nuerol. 300:5-25.

Emmerton, J., & J. D. Delius.  1980. Wavelength discrimination in the 'visible' and ultraviolet spectrum in pigeons. J. Comp. Physiol. A 141: 47-52.

Fox, R., S.W. Lehmkuhle, & D.H. Westendorf. 1976. Falcon visual acuity. Science 192:263-265.

Gunturkun, O. 2000. Sensory physiology: vision. Pp. 1 - 19 in Sturkie's Avian Physiology, fifth edition. Academic Press, San Diego.

Husband, S. and T. Shimizu. 1999. Evolution of the avian visual system. http://luna.cas.usf.edu/~husband/evolve/default.htm.

Jarvis, E.D., O. Güntürkün, L. Bruce, A. Csillag, H. Karten, W. Kuenzel, L. Medina, G. Paxinos, D. J. Perkel, T. Shimizu, G. Striedter, M. Wild, G. F. Ball, J. Dugas-Ford,  S. Durand, G. Hough, S. Husband, L. Kubikova, D. Lee, C.V. Mello, A. Powers, C. Siang, T.V. Smulders, K. Wada, S.A. White, K. Yamamoto, J. Yu, A. Reiner, and A. B. Butler. 2005. Avian brains and a new understanding of vertebrate brain evolution. Nature Reviews Neuroscience 6:151-159.

Karten, H.J. 1997. Evolutionary developmental biology meets the brain: The origins of mammalian cortex. Proc. Natl. Acad. Sci. USA 94:2800-2804.

Knudson, E. 2002. Instructed learning in the auditory localization pathway of the Barn Owl. Nature 417:322-328.

Mason, J.R, & L. Clark. 2000. The chemical senses of birds. Pp. 39 - 56 in Sturkie's Avian Physiology, fifth edition. Academic Press, San Diego.

Medina, L. and A. Reiner. 2000. Do birds possess homologues of mammalian primary visual, somatosensory and motor cortices? Trends Neurosci. 23:1-12.

Nevitt, G. 1999. Foraging by Seabirds on an Olfactory Landscape. American Scientist 87:46-54.

Piersma, T., R. van Aelst, K. Kurk, H. Berkhoudt, & L.R.M. Maas. 1998. A new pressure sensory mechanism for prey detection in birds: the use of principles of seabed dynamics? Proceedings of the Royal Society of London B 265:1377-1383.

Rattenborg, N.C., S.L. Lima, and C.J. Amlaner. 1999. Half-awake to the risk of predation. Nature 397:397.

Rattenborg, N. C., B. H. Mandt, W. H. Obermeyer, P. J. Winsauer, R. Huber, M. Wikelski, and R. M. Benca1. 2004. Migratory Sleeplessness in the White-Crowned Sparrow (Zonotrichia leucophrys gambelii). PLoS Biol 2(7): e212.

Schultz, J. D. and B. A. Schlinger. 1999. Widespread accumulation of [3H]testosterone in the spinal cord of a wild bird with an elaborate courtship display. Proc Natl Acad Sci U S A 96: 10428–10432.

Ulinski, P.S. 1983. Dorsal Ventricular Ridge: A Treatise on Forebrain Organization in Reptiles and Birds. John Wiley & Sons, New York.

Useful links:

Avian Brain Nomenclature Issues

Bird Learning: an Example of a Vertebrate Model

Bird Vision - What Do They See?

Color Vision of Birds

Hearing and the Bird Ear

Ecology of Vision: Exploring the Fourth Dimension

Evolution of the Avian Visual System

Studies to Determine the Intelligence of African Grey Parrots

The Bird That Never Forgets

The Life of Birds: Bird Brains

The Nervous System and Senses

Tool-Using Crows Give New Meaning to Term 'Bird Brained'

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