BIO 554/754
Ornithology

Nervous System: Brain and Special Senses II

 

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

 

Vision - Birds, with the possible exception of diurnal primates (e.g., humans), are the vertebrates which may rely most heavily on vision to function in their environment. The most obvious visually-dependent behavior of birds is flight, but birds also exhibit an impressive range of visually guided behaviors other than flight, e.g., foraging, predator detection, & mate choice.

The avian eye is large relative to the size of the head & brain. For example, human eyes make up about 1% of the total mass of the head; European Starlings eyes make up about 15% of the mass of their head. The advantage: large eyes provide larger & sharper images. Birds also have 3 eyelids; one upper and one lower eyelid plus a nictitating membrane. This nictitating membrane is between the other two eyelids and the cornea and has its own lubricating duct equivalent to our tear duct.

The nictitating membrane, or third eyelid, is unique to vertebrates, although not found in all groups. In many species, it represents the principal mechanism of ocular cleansing. In birds, the external eyelids possess smooth muscle, and may close only during sleep. The nictitans, on the other hand, is operated by two striated muscles and is capable of extremely rapid sweeps across the ocular surface to clear the cornea of debris. Ocular surface lubrication originates from two secretory glands. The lacrimal gland is situated in the inferior temporal quadrant associated with the more active lower eyelid, although in many species this gland is absent or rudimentary. Additionally, most birds, especially cormorants and falcons, have a second secretory gland called a Harderian gland located in the posterior and nasal aspect of the orbit associated with base of the nictitating membrane. In falcons, this secretory gland produces a viscous solution to moisten the cornea during the breathtaking stoops that are the falcon’s trademark. Although the composition of these secretions is not known, a compound such as hyaluronic acid would moisten the surface without the rapid evaporation seen with a more dilute tear film. Such a coating would maintain a smooth surface, but might pose other difficulties by collecting debris (Schwab and Maggs 2004).


The nictitating membrane of many such birds has a cartilaginous-like connective tissue fold along the leading edge of the membrane called the marginal plait (photomicrograph to the right). With each blink this flange-like flap collects the tear film and any associated debris to drain through the enlarged puncta (openings that act like little valves to take tears out of the eye) into the nasolacrimal system. It is probably aided in this corneal cleansing role by a layer of "feather epithelium." This remarkable adaptation of a surface epithelium is believed to be unique to the epithelium lining the nictitans of many birds and reptiles. Long microvilli with club-like termini and numerous secondary projections from their long axis extend from the apical membrane of epithelial cells lining the bulbar surface of the third eyelid. Those of Peregrine Falcons (above) are extremely robust and likely form a "histological feather duster" that sweeps the cornea clean with each darting excursion of the clear nictitans (Schwab and Maggs 2004).


Eye size, brain size, prey capture and nocturnality -- Behavioural adaptation to ecological conditions can lead to brain size evolution. Structures involved in behavioural visual information processing are expected to coevolve with enlargement of the brain. Because birds are mainly vision-oriented animals, Garamszegi et al. (2002) tested the predictions that adaptation to different foraging constraints can result in eye size evolution, and that species with large eyes have evolved large brains to cope with the increased amount of visual input. Using a comparative approach, Garamszegi et al. (2002) investigated the relationship between eye size and brain size, and the effect of prey capture technique and nocturnality on these traits. After controlling for allometric effects, they found a significant, positive correlation between relative brain size and relative eye size. Variation in relative eye and brain size were significantly and positively related to prey capture technique and nocturnality. These findings suggest that relative eye size and brain size have coevolved in birds in response to nocturnal activity and, at least partly, to capture of mobile prey.

 Structure of the avian eye:


Source: http://www.lsi.usp.br/~bioinfo/chickeneye.html
 


Source: Rowe (2000)


Owls have tubular eyes with little extraocular musculature, to maximize the size of the eyes.
To compensate, most owls can turn their heads with great speed, nearly 270° atop a thin,
lightweight spinal column; so quickly that myths of complete 360° cranial revolution have
sprung up adding to the mythology of owls. As can be seen in the cranial slice taken at the
midline of the cornea above the upper mandible, the eyes of Eastern Screech-Owls are large, both
on an absolute and relative basis. They are frontally placed, providing as much binocular stereopsis
as possible, as is typical for avian predators. The stereoscopic binocular visual field is approximately 60-70°,
although the visual field is larger. The eyes together outweigh the brain as often occurs in
raptorial species, especially the nocturnal owls (British Journal of Opthamology, Sept. 2000 issue).
 


Rings of bony plates surrounding the iris of the eye are present in most birds. On the left is a drawing of the
arrangement of the plates in an albatross eye showing how the ossicles shape the junction between the cornea and the sclera.
To the right is the skull of an eagle showing the positioning of the ossicles within the orbit. The primary purpose of the
ossicles appears to be to reinforce the corneal scleral junction. In birds, the ossicles allow the animals to adjust the shape of the
cornea during accommodation (Rowe 2000).


Collared Scops Owl (Otus lettia)
Photo by Wayne Hsu (& used with his permission)
(Source: http://www.owlpages.com/species/otus/lettia/collared_scops1.html)

Source: http://www.fieldandstream.com

Monocular vs. Binocular Vision

The eyes of most birds are on the side of their heads, allowing them to see objects on each side at the same time (monocular vision). This provides birds with a wide field of view, e.g., Rock Doves (pigeons) can see 300 degrees without turning their head and American Woodcocks can see 360 degrees! With monocular vision, birds may have a harder time judging distances and have poorer depth perception. Of course, these birds do have a limited field of binocular vision directly in front of them (and woodcocks also have a field of binocular vision behind them). Other birds, like owls, have their eyes located to the front giving them a much wider field of binocular vision. These birds may have a 180 degree field of overall vision with most of that binocular. See 'The Bird Site - Senses'


Source: http://www.lam.mus.ca.us/birds/guide/pg006.html


The eyes of most birds are aligned laterally, and each visual axis gives a lateral, or monocular, view. This lateral visual field serves to monitor predators and conspecifics, as well as to detect food at some distance. Most birds also have, in addition to a central fovea, a second retinal fovea, located in the temporal retina. The cyclopean area is the combination of the frontal and lateral visual fields.

Visual fields of birds have been categorized as:

  • Type 1 (a). Large cyclopean area; largely monocular vision (e.g. Rock Pigeon Columba livia, Starling Sturnus vulgaris and Cattle Egret Bubulcus ibis)
  • Type 2 (b). Very large cyclopean area; small binocular fields in front and back  (e.g. Eurasian Woodcock Scolopax rusticola)
  • Type 3 (c). Larger frontal area with large binocular field (e.g. Tawny Owl Strix aluco).

                                                From:
Fernandez-Juricic et al. (2004)

A view to a kill: why airborne hunters don't dive straight in (New Scientist; 11/25/00) - The mystery of why birds of prey spiral in towards their victims may have been solved. They do it to make the most of their pin-sharp sideways vision. Vance Tucker of Duke University has long been puzzled by the way birds of prey approach their dinner. In studies of Peregrine Falcons, he & his colleagues found that the birds almost always follow a curved path once they get within 1.5 km of their prey (Tucker 2000). "We had observed these curved paths for years, and I was racking my brains to explain that," says Tucker. He suspected the explanation lay in the birds' vision. Tests have shown they see objects in front of them most clearly when they turn their heads about 40 degrees to one side. But turning their heads in mid-flight might increase the birds' aerodynamic drag, slowing them down. To test this, Tucker placed models of Peregrine Falcons and Red-tailed Hawks in a wind tunnel. Force sensors showed that, at a wind speed of 42 km per hour, the drag on birds whose heads were turned 40 degrees was more than 50% greater than on those looking straight ahead. To avoid this, Tucker concludes, the birds keep their heads straight and follow a path called a logarithmic spiral. That way, they can keep one eye fixed on their prey. And while a spiral path is longer, the speed advantage more than compensates. 


Source of photo on the right: http://www.pigeon.psy.tufts.edu/avc/pblough/introduction.htm

The avian retina, in contrast to that of mammals, is avascular (contains no blood vessels), which prevents shadows & light scattering. This 'improvement' is possible because of a uniquely avian structure - the pecten. This highly vascular structure projects from the retina (see diagrams above; for photo on the right: P = pecten, R & Y = areas of the retina, & F = fovea) and nutrients & oxygen diffuse from it, through the vitreous body (see diagram above), to the retinal cells - the rods and/or cones.


On the left, a goat fundus (or back of the eye) with retinal blood supply from central
or cilioretinal arteries (same as humans). On the right, a screech-owl fundus with no
vessels in the retina.
(Source: www.vetmed.ucdavis.edu/courses/vet_eyes/conotes/con_chapter_12.html)

The avian retina has three types of photoreceptors that 'translate' light into nervous impulses:


 Five major classes of retinal neurons are also recognized:  photoreceptors,
bipolar cells, horizontal cells, amacrine cells, and ganglion cells. The photoreceptors
(rods and cones), bipolar cells, and horizontal cells make synaptic contacts with each other in the outer
retinal layers. The bipolar, amacrine, and ganglion cells make contact in the inner retinal layers.
(Source: Husband and Shimizu 2001; http://www.pigeon.psy.tufts.edu/avc/husband/avc4eye.htm)

Nocturnal birds, like owls, have retinas consisting entirely of rods, while the retinas of diurnal birds contain both rods & cones. The single cones, as well as one or both segments of double cones, contain oil droplets (see photo to the lower right of oil droplets in the retina of a European Starling) which

These oil droplets:


The transparent or colorless oil droplets found in many birds permit perception of very short spectral wavelengths (ultraviolet or near ultraviolet).  Such perception:



Evolution of vertebrate UV vision. Circles indicate extant organisms, and squares indicate ancestral species.
Black filled symbols indicate UV vision, purple filled symbols indicate violet vision, and open symbols
indicate absence of UV or violet vision. UV vision is mediated by visual pigments that absorb light maximally at 360 nm.
Violet (or blue) pigments absorb light maximally from 390–440 nm. The arrow shows the root of the tree and the
common ancestor of vertebrates (Zhang 2003).


Examination of the phylogenetic distribution of UV and violet vision across vertebrates suggests that violet vision originated at least four times, in frogs, birds, primates, and cetartiodactyls (Zhang 2003). In most extant vertebrates, UV vision was directly inherited from the vertebrate ancestor, but in birds, it was apparently restored from violet vision secondarily. Analysis by Odeen and Hastad (2003) indicates that UV vision was regained at least four times in birds. Shi and Yokoyama (2003) argue that that the presence of UV vision is associated strongly with the availability of UV light in the environment and with UV-dependent behaviors. For example, coelacanths (the so-called "living fossil" that lives at depths 200 m in the ocean) and dolphins(see Figure above) live in marine environments where UV light cannot reach. 

Given an abundance of UV light in their environment, why have so many organisms switched from UV vision to violet vision? Shi and Yokoyama (2003) suggest two major reasons. First, UV light, even at 360 nm, can damage retinal tissues. Second, by achieving violet vision, organisms can improve visual resolution and subtle contrast detection. On the other hand, in the avian lineage, their ancestor lost UV vision, but some of its descendants regained it (See Figure to the right).
Birds use UV vision in many ways: Kestrels (Falco tinnunculus) use UV reflection of vole urine, left as scentmarks, to locate prey (more details on this below). Blue Tits (Parus caeruleus)  use their UV vision to detect camouflaged caterpillars. Female Bluethroats (Luscinia svecica) choose mates based on UV coloration of males. Nestlings in some species advertise their quality to parents via UV reflectance of their ‘flanges’ (the rim around the edge of their mouth).


Type of vision system mapped onto phylogenetic relationship among avian taxa (phylogeny based on DNA–DNA hybridization analysis; Sibley and 
Ahlquist 1990).The passeriform families are 
combined (in bold). White denotes violet 
sensitive (VS), black indicates ultraviolet sensitive
(UVS), and gray indicates taxa with both systems
(Ödeen and Håstad 2003).

Recent work has revealed that some birds of prey see a wider color spectrum than we do, including ultraviolet light. How might this be useful? Kestrels (Falco tinnunculus) are a familiar sight in Europe hovering along motorways and grasslands. They are watching for small rodents. Their quarry is fast and nimble and ranges over habitat that is often uniform and extensive. At times, the kestrel's task must seem like a search for the proverbial needle in a haystack. However, rodents mark their runs with urine and feces, which are visible in ultraviolet light. In tests, wild kestrels brought into captivity were able to detect vole and mouse latrine scents in ultraviolet settings (Koivula et al. 1999). This ability enables them to screen large areas of vegetation in a relatively short time and to concentrate hunting at 'busy intersections'.  Source: www.bbc.co.uk/nature/birds/
Source: www.bbc.co.uk/nature/wildfacts/factfiles/243.shtml

Photopigment absorption spectra for a pigeon and a human.
(Husband and Shimizu 2001, adapted from Bowmaker 1991)


Animals extract information about the spectrum of light striking different regions of their retinas by contrasting the responses of photoreceptors containing different photopigments. This figure shows the absorption spectra of the three types of photopigment that
mediate human color vision and the four types of photopigment that mediate color vision in European Starlings. Because Starlings
have four cone photopigments, there are four different outputs, and none are identical to any of the three outputs of the human cones.
Because these photoreceptor outputs are all that nervous systems retain for the analysis of color, the colors we see are different
from the colors seen by a Starling (or any other animal). Objects having one hue to a human may have drastically different hues to a
bird (Rowe 2000).


UV Got Great Feathers, Baby - Female birds see something in their mates that evades the human eye: the ultraviolet gleam of their plumage. Birds, like many other animals, can perceive ultraviolet light as well as the wavelengths visible to the human eye;  insects, for example, use UV reflectance to home in on flowers.  Bennett et al. (1997) wondered what else birds might do with their UV vision. So they captured 16 female starlings and 32 males & designed an experiment to see if females used UV reflectance to pick their beaus. For each test the researchers let a female check out 4 different males, lined up behind transparent filters that blocked UV light. To gauge her interest, the team measured how long the female stood & how many times she hopped in front of each male. Then they let another female size up the same four males. For the next round of tests, they removed the filters and revealed the same males in their full-color glory. They found that under any lighting condition female starlings had very similar tastes. About 90% of the time, the two females preferred the same male of any given four. But the type of light determined which male was deemed top bird. Without the filter, females preferred males whose feathers reflected lower amounts of UV. But without UV light, "females switched their preference away from plumage color," says Innes Cuthill, a behavioral ecologist at the University of Bristol. He's not sure exactly what guided their choice instead, but suspects body language such as rates of feather fluffing. The moral, the researchers say, is not to ignore UV wavelength when studying bird mate choices. "We can't always rely on the colors we see to predict birds' mate choice," Cuthill says. 

Areas & foveae - many birds have a horizontal streak or "central area" across the retina with higher concentrations of sensory cells, usually with a fovea (area of highest concentration of sensory cells) at each end.

Foveae of an Arctic Tern (top) and a human (bottom)
(Source: Husband and Shimizu 2001; http://www.pigeon.psy.tufts.edu/avc/husband/avc4eye.htm)


The eyes of Oilbirds -- An extreme example of a low light-level lifestyle among flying birds is provided by the Oilbird, Steatornis caripensis. Oilbirds breed and roost in caves in northern South America and Trinidad, often at sufficient depth that no daylight can penetrate, and forage for fruits at night. Using standard microscopy techniques, Martin et al. (2004) investigated the retinal structure of oilbird eyes and used an ophthalmoscopic reflex technique to determine the parameters of these birds visual fields. The eyes are relatively small (axial length 16.1 ± 0.2 mm) with a maximum pupil diameter of 9.0 ± 0.0 mm, achieving a light-gathering capacity that is the highest recorded in a bird (f-number 1.07). The relatively large pupil helps the oilbird eye collect four times more light than the human eye. The light-sensitive rod cells within the eye are stacked three deep, with a density of about 1,000,000 per mm2 -- more than double the number usually found in vertebrate eyes. The tiered strategy, which has previously been found only in deep-sea fish, maximizes the chance that every photon of light entering the eye will be intercepted. But extreme sensitivity comes at a cost.The retina’s tiered structure makes it difficult for the brain to work out exactly where the light has come from, so oilbirds have a poor eye for detail. Martin et al. (2004) therefore suggest that these nocturnal birds rely on a combination of information from smell and echolocation, as well as from sight, to forage successfully.

Visual acuity:


Migrating birds may 'see' magnetic field -- Migrating birds navigate without a compass, map, or GPS unit. But they may carry their own navigational array, which lets them "see" the Earth's magnetic field. Ritz et al. (2000) used chemical experiments, physics theory and 3-D computer modeling to show that part of a bird's optical system could be affected at a molecular level by weak magnetic fields. Migrating birds appear to draw from the Earth's magnetic field visual information about whether they're properly oriented along the migration route. The birds aren't simply pointed in a particular direction by the magnetic effect, like flying compass needles. They actually see the field in some way. Ritz et al. (2000) don't know exactly what the birds see. But their research suggests that they get some sort of visual feedback when they're on path and a different cue when they stray, kind of like clear reception when a TV antenna is aligned vs. static when it's not. Migrating birds likely combine this information with other navigational cues. Other animals, like salmon, salamanders and hamsters, likely have similar abilities. Ritz et al. (2000) traced the system to "receptors" in the eyes and brain, proteins that absorb light & provide information about color, day, and night. The retina includes color receptors, black & white receptors, and another type known to regulate circadian rhythms. This receptor, which makes you sleepy at night, also appears to play a role in processing magnetic signals. Scientists have observed magnetic reception previously. For example, the "magnetoreception" of bacteria filled with magnetic particles that make them natural compasses. But the way it's accomplished in higher animals, whose systems aren't chock-full of tiny magnets, has been a mystery. Ritz et al.'s (2000) research doesn't settle the question, but it does provide a promising avenue for further inquiry. -- Greg Kline, Champaign News-Gazette
Source: http://www.ks.uiuc.edu/Research/magsense/ms.html


Study could help identify mechanism of magnetoreception in birds — Migrating birds stay on track because of chemical reactions influenced by the Earth’s magnetic field. The birds are sensitive even to rapidly fluctuating artificial magnetic fields. These fields had no effect on magnetic materials such as magnetite, indicating that the birds do not rely on simple chunks of magnetic material in their beaks or brains to determine direction, as experts had previously suggested. Ritz et al. (2004) exposed 12 European robins to artificial, oscillating magnetic fields and monitored the orientation chosen by these birds. The stimuli were specially designed to allow for responses that could differ depending on whether birds used small magnetic particles on their bodies or a magnetically sensitive photochemical reaction to detect the magnetic field. “We found that the birds faced in the usual direction for their migration when the artificial field was parallel to the Earth’s natural magnetic field, but were confused when the artificial field was applied in a different direction,” said Ritz. “Since the artificial field’s oscillations were too rapid to influence magnetic materials like magnetite, it suggests that the most likely mechanism for magnetic orientation in these birds involves tiny changes to magnetically sensitive chemical reactions, possibly occurring in the eyes of the birds — we are not sure.”

“Unlike our senses involving vision, hearing, smell and touch, we do not know what receptors underlie magnetoreception,” Ritz said. “Migratory birds have long been known to possess a magnetic compass that helps them find the correct direction during their migratory flights. It has remained unknown, however, how birds can detect the direction of the Earth’s magnetic field.

“Now, our study points to what we need to look for a molecular substrate for certain chemical reactions. That is, we can rule out magnetic materials in birds’ beaks and elsewhere as being possible candidates. Magnetite in the beaks, however, may play a role in detecting the strength but not the direction of the Earth’s magnetic field.”


Hearing and Balance - The avian ear, like that of mammals, has three sections: outer ear, middle ear, & inner ear:


Source:
www.bio.purdue.edu/Bioweb/People/Faculty/iten.html

Source: http://www.palaeos.com/Vertebrates/Bones/Ear/Overview.html


Cross-section through a semicircular canal



Head (circles) and body (squares) vertical oscillations, and humeral excursion during 
the wingbeat cycle of a Black-billed Magpie taken from x-ray film (Warrick et al. 2002).

The avian neck as a shock absorber (Warrick et al. 2002) -- During flapping flight when lift production ceases during upstroke, birds experience downward accelerations due to gravity and upward accelerations due to lift. Many forms of locomotion produce similar stresses, but only flying species would experience these oscillations 10 times a second (a typical avian wingbeat frequency). At least two sensory functions could be severely impacted by such rapidly alternating accelerations: vision, and static equilibrium. Vision might be affected by simply introducing extraneous visual flow. Similarly, the maculae of the inner ear,which in all vertebrates use the acceleration due to gravity to provide information regarding the position of the head, would be subjected to accelerations that might compromise this function. Given that birds probably do not need to continuously confirm the vertical oscillations of the body during flapping flight, there may have been selective pressure to isolate the head from these vertical accelerations, leaving their eyes and maculae free to gather only useful information about their paths through and positions in space. Digitized x-ray film of a single Black-billed Magpie (Pica pica) flying in a wind tunnel at 8 m per sec show that they have the ability to isolate the head from the movement of the body during flapping flight. In level flight, the bird's body fell an average (± standard deviation) of 1.44 ± 0.30 cm with every upstroke, while it restricted head vertical movement to as little as 0.14 cm during a wingbeat cycle (average for all wingbeats = 0.43 ± 0.21 cm). The degree to which the bird decoupled vertical movement of the head and body appeared to depend on whether or not the bird was changing position in the wind tunnel. For example, the head exactly followed the body during a brief climb, but was immediately isolated from the sinusoidal body excursion (as it was at the beginning of the series; see Figure above ) as soon as level flight was re-established. This suggests that the isolation of the head from the vertical accelerations may be important in allowing an uncluttered vestibular ‘picture' of the bird's substantive changes in vertical position. While the anatomical details of this dampening mechanism are undescribed, a spinal reflex involving the flexors and extensors of the dorsal and ventral cervical musculature (e.g., the semispinalis capitus, biventer cervicis; longus colli) seems likely.

Birds 'hear' like mammals do:


Bird cochleas are between 2 and 11 mm in length and contain between 3,000 and 17,000 hair cells.
Hair cells form a continuum, ranging from 'tall' to 'short.'  Short hair cells are located on the basilar membrane (blue), a
membrane that moves or vibrates in response to pressure waves in the cochlea. When the hairs move against
the tectorial membrane (yellow), nerve fibers at the base of the hairs are activated and nervous impulses are generated.
The perceived frequency of a sound depends on which hair cells are stimulated (with those further from the oval
window responsible for higher frequencies; in birds, the average space constant, i.e., distance along the cochlea relative
to frequency detected, is < 1 mm/octave (Manley 2000, and figure also from Manley 2000).

Loss or damage of sensory, or hair, cells in the inner ear, results in hearing impairment. These cells can be damaged by overexposure to intense sounds. In mammals, once these hair cells are lost, they are not replaced, so hearing loss is permanent. Birds, however, have the remarkable ability to regenerate and replace the hair cells of the inner ear following damage or loss (Dooling and Dent 2001). Here are scanning electron microscopic pictures of bird inner ears at three different time periods after exposure to a chemical (kanamycin) that destroys hair cells. After 28 days, the number of hair cells in the regenerated bird ear has nearly returned to normal levels.

Source: http://www.bsos.umd.edu/psyc/dooling/HC1.htm

Hearing ranges of birds:


Source: http://elephant.elehost.com/About_Elephants/Senses/Hearing/hearing.html

Sound localization:

Owls note the differences in intensity and timing of sounds between the two ears.

Source: kybele.psych.cornell.edu/~edelman/Psych-214-Fall-2002/pp-week1-2.html


Locating a Mouse by Its Sound - At Caltech in the mid-1970s, Masakazu (Mark) Konishi began studying the auditory system of barn owls to resolve the question:  Why do we have two ears? While most sounds can be distinguished quite well with one ear alone, pinpointing where sounds are coming from requires a complex process called binaural fusion, where the brain compares information received from each ear & translates subtle differences into a perception of a single sound coming from a particular location. The ability to identify where sounds are coming from based on auditory cues is common to all hearing creatures, but owls - especially barn owls - excel at the task. These birds exhibit such extraordinary sound localization abilities that they are able to hunt in total darkness.

Together with Eric Knudsen, now at Stanford University, Konishi undertook experiments in 1977 to identify networks of neurons in the brains of owls that could distinguish sounds coming from different locations. He did so by probing the brains of anesthetized owls with fine electrodes. With electrodes in place, a remote-controlled sound speaker was moved to different locations around the owl's head. As the speaker moved, imitating sounds the owl would hear in the wild, the investigators recorded the firing of neurons near the electrodes. Over several months, Konishi and Knudsen identified an area in the midbrain containing cells called space-specific neurons that fired only when sounds were presented in a particular location. Astonishingly, the cells were organized in a precise topographic array, similar to maps of cells in the visual cortex of the brain. Aggregates of space-specific neurons, corresponding to the precise vertical and horizontal coordinates of the speaker, fired when a tone was played at that location.

"Regardless of the level of the sound, these cells always responded to the sources at the same place in space. Each group of cells across the circuit was sensitive to sound coming from a different place in space, so when the sound moved, the pattern of firing shifted across the map of cells," Knudsen recalls. 

Source: www.hhmi.org/senses/c210.html


Some owls have asymmetrical ear openings, allowing them to accurately note differences in
the intensity and timing of sounds in both the horizontal (azimuth) and vertical (elevation) planes.

(Figure source: web.psych.ualberta.ca/~msnyder/Academic/psych403/week8/w8oh.html)

Echolocation:


The Oilbird (Steatornis caripensis), a nocturnal bird of South America that lives  in caves and feeds on fruit, mainly the nuts of oil palms. Oilbirds are about 30 cm (12 inches) long, with a fanlike tail and long broad wings. They have a strong hook-tipped bill, long bristles around the wide gape, and large dark eyes. Oilbirds use echolocation to find their way within the caves where they roost and nest from Trinidad and Guyana to Bolivia. The sounds emitted are within the range of human hearing: bursts of astonishingly rapid clicks (as many as 250 per second). Oilbirds also utter squawks and shrieks that suggest their Spanish name, guácharo ("wailer"). At night, oilbirds fly out to feed, hovering while they pluck fruit from trees. Two to four white eggs are laid on a pad of organic matter on a ledge high up in a cave. The young, which may remain in the nest for 120 days, are fed by regurgitation until they are 70 - 100% heavier than adults. Indians render the squabs for an odorless oil for cooking and light; hence the bird's popular and scientific names.
Source: www.asawright.org/nature/oilbirds.html

Literature Cited

Bennett, A. T. D., I. C. Cuthill, J.C. Partridge, and K. Lunau. 1997. Ultraviolet plumage colors predict mate preference in  Starlings. Proc. Nat. Acad. Sci. USA  94:8618-8621.

Bowmaker, J.K. 1991. The Evolution of Vertebrate Visual Pigments and Photoreceptors. In J.R. Cronly-Dillon, & R. L. Gregory (Eds.), Vision and Visual Dysfunction, Vol. 2: Evolution of the Eye and Visual System. CRC Press, Boca Raton, FL.

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

Dooling, R. J. and M. L. Dent. 2001. New studies on hair cell regeneration in birds.  Journal of the Acoustical Society of Japan 22:93-100.

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

Fernandez-Juricic, E., J. T. Erichsen, and A. Kacelnick. 2004. Visual perception and social foraging in birds. Trends in Ecology and Evolution  19: 25-31.

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

Garamszegi, L.Z., A.P. Moller, and J. Erritzoe. 2002. Coevolving avian eye size and brain size in relation to prey capture and nocturnality. Proc R Soc Lond B 269:961-967.

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.

Husband, S. & T. Shimizu.  2001. Evolution of the avian visual system. In R. G. Cook  (Ed.), Avian visual cognition [On-line]. Available: www.pigeon.psy.tufts.edu/avc/husband/

Koivula, M., J. Viitala, & E. Korpimäki. 1999. Kestrels prefer scent marks according to species and reproductive status of voles. Ecoscience 6:415-420.

Manley, G.A. 2000. Cochlear mechanisms from a phylogenetic viewpoint. Proc. Natl. Acad. Sci. 97: 11736-11743.

Martin, G.,  L.  M. Rojas, Y. Ramírez, and R. McNeil. 2004. The eyes of oilbirds (Steatornis caripensis): pushing at the limits of sensitivity. Naturwissenschaften 91:26-29.

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.

Ödeen, A. and Olle Håstad. 2003. Complex Distribution of Avian Color Vision Systems Revealed by Sequencing the SWS1 Opsin from Total DNA. Mol. Biol. Evol. 20:855-861.

Ritz, T., S. Adem, and K. Schulten. 2000. A model for photoreceptor-based magnetoreception in birds. Biophysical Journal 78:707-718.

Ritz, T, P. Thalau, J.B. Phillips, R. Wiltschko & W. Wiltschko. 2004. Resonance effects indicate a radical-pair mechanism for avian magnetic compass. Nature 429: 177-180

Rowe, M.P. 2000. Inferring the retinal anatomy and visual capacities of extinct vertebrates. Palaeontologia Electronica 3(1).

Schwab, I. R. and D. Maggs. 2004. The falcon's stoop. British Journal of Ophthalmology 88:4.

Shi, Y. and S. Yokoyama. 2003. Molecular analysis of the evolutionary significance of ultraviolet vision in vertebrates. Proc. Natl. Acad. Sci. 100:8308-8313.

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Tucker, V. 2000. Gliding flight: Drag and torque of a hawk and falcon with straight and turned heads, and a lower value for the parasite drag coefficient. Journal of Experimental Biology 203: 3733 - 3744.

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Useful links:

Bird Learning: an Example of a Vertebrate Model

Bird Vision - What Do They See?

Color Vision of Birds

Hawk-eyed

Hearing and the Bird Ear

Ecology of Vision: Exploring the Fourth Dimension

Evolution of the Avian Visual System

Light Receptor May Be Key In How Animals Use Earth's Magnetic Field

Studies to Determine the Intelligence of African Grey Parrots

Taking a Bird's-Eye View…in the UV: Recent studies reveal a surprising new picture of how birds see the world

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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