The barn owl (Tyto alba) an auditory specalist


The barn owl (Tyto alba) has been said to be one of the most successful nocturnal predatory birds that exist in our world today.  As adults, barn owls rarely miss their target prey.  They owe this to their finely tuned auditory system.  Owls combine excellent hearing with visual tracking to perfectly locate prey and maximize their chances of successful capture (http://www.allaboutbirds.org).  Their auditory tracking system functions based on several key features of barn owl morphology.  The first is that barn owls possess asymmetrically shaped ears.  This means that the owl’s left ear points downward and the right ear points upward.  A sound that appears louder in amplitude on the right side of the owl is interpreted as being higher in elevation than a sound that appears louder in amplitude on the left side of the owl.  This helps the owl discern moving target’s elevations.  The second key feature is the owl’s facial disk.  Barn owls are known for having a heart shaped face.  This facial disk acts like the pinna on humans and helps the owl to amplify sounds. (Koppl et al. 2007)  The last key feature is the owl’s ability to detect timing differences in sounds.  The owl’s midbrain can process the differences in arrival times of a sound between one ear and the other.  The owl can then use this information to help them direct their head towards the prey item. (Spitzer et al. 2006)

Section 1:  The owl as a newborn and its development.

In order to get a complete picture of how barn owls’ amazing auditory mapping works, we will first look at barn owls when they are newborns.  Koppl et al. 2007 were interested in investigating the length of time in which the owls hair cell activity, referred to as cochlear microphonics (CM) and the owls neuronal response to sound measured from the auditory nerves via compound action potentials (CAP) first showed up in the barn owls inner ear post hatching.  They performed the experiment by immobilizing and measuring auditory activity in 26 owlets aged from 5-96 days. Due to the owlets’ face functioning as a pinna, an audio device was inserted directly into their ear canal so as to remove the variable of the sound stimuli amplitude  being altered by the owls facial disk.  Then the owl’s round window was exposed by removing the inner ears round window membrane and using various equipment and software, measurements were taken of the electrical activity found when the bird’s ear was exposed to various sound frequencies.

What they found was that unlike other birds, owlets are essentially deaf to most normal, natural intensity sounds during the first two weeks post hatching.   Subsequent to the first two weeks, CM activity gradually improved until the five week period at which point their CM activity was at normal levels.  This meant that they had the ability to hear in the normal ranges up to 10 kHz.  A surprising thing to note was that the data suggested that CM always matured slightly faster than the CAP activity within normal ranges of frequency.  This was directly confirmed using 12 juvenile barn owls with measurements taken consistently at weekly time intervals.  This faster rate of CM maturation indicated that there was a sequence of maturation from low to high frequencies as the owls got older. This experiment was important to science because it helped to understand how auditory mechanisms work.

Section 2: The owl’s behaviors once it’s older

With some basic knowledge of how owls develop in terms of the arrival of their abilities as auditory locators, we can now look more into how Tyto alba hunts as an adult. Fux et al. 2009 were interested in looking at the nature of the visual tracking that has been observed in barn owls specifically whether or not barn owls were interceptor type predators, which tend to look towards where the collision attack will occur, or if they were tracking type predators following their prey as they moved.  The owls were exposed to live voles in captivity and recordings were taken on the owls head movements relative to the movements of the voles themselves.  What was found was that barn owls track their prey horizontally in azimuth using head movements.  This effectively moves their stationary prey into a new location in their retina thus helping them to create a more accurate representation of the position of the prey relative to themselves.  Once the prey is spotted, the owl tracks its head over a large area in order to continue to assess the spatial location and to help with calculating the interception point should the prey start to suddenly move. (Fux et. al. 2009)

Once the owl has spotted its prey it will take off and fly towards it in order to attack it.  Hausmann et al. 2008 looked at the owl’s ability to adapt its flight/attack pathway in mid flight to compensate for moving prey.  The researchers placed barn owls into a sound attenuation chamber in complete darkness and using speakers, played an initial tone for the owls that would mimic the relative position in both elevation and azimuth of a potential prey item.  Once the owls took off to attack the item, the sound was replayed at particular delay intervals suggesting to the owls a change in location of the prey.  The landing positions of the owls relative to the timing of the delay were then plotted.  What researchers found was that if a stimulus was applied before 50 percent of the flight time was over, the owls could correctly adjust their path towards the new stimulus.  However, if 80 percent or more of the flight path had been completed, owls no longer adjusted and continued on their original path regardless of the adjusted location of the prey.  Also noted was that regardless if the owls had to change direction mid-flight or not they tended to just slightly undershoot their target, allowing them to still be successful at attacking their prey while also placing them in the most suitable position to relaunch an attack should their prey move in an unpredicted manner. (Hausmann et al. 2008)

Barn owls have evolved to become deadly efficient hunters, armed with traits like asymmetric ears, and wings that allow them to swoop down on prey in silence. (http://www.allaboutbirds.org)  Researchers looked at the success of barn owls in catching prey and the steps that were taken immediately prior to prey capture.  They then noted and discussed various prey responses and the various benefits and disadvantages that arose between the types of responses of predator evasion.  Three evasion categories were identified, freezing, fleeing, and fighting (defensive attacking). (Ilany et al. 2008).

To measure the success rates of the owls in prey capture and the success rates of the mice in evading the barn owl, researchers looked at actual interactions between the spiny mice and the barn owl.  It was found that the owls were most successful at capturing stationary prey.  They determined that spiny mice have adapted to flee at a particular timing when the owls are approaching in their final moments.  The direction that is best suitable for fleeing is to run sideways to the direction the owl is traveling when the owl is approximately 2 meters away from its target (Ilany et al. 2008).  This strategy works best for the spiny mice, which are nimble and fast runners; however other prey might have different strategies for avoiding the owls. By understanding how the prey react to the owl attacks, researchers can better understand what makes the owl a successful predator and how its auditory system copes with these counter reactions.

Section 3: How does the barn owl do this amazing hunting?

One question that has always fueled barn owl research is how owls are able to hear their prey so well. Therefore much of Tyto alba research therefore deals with the barn owls ears and how their auditory abilities tie in neurologically with their brains and inner ears.  Koppl et al. 2007 were interested at looking at the relationship between the barn owls hair cell activity measured via cochlear microphonics (CM) and the owls’ auditory neuronal activity as measured by compound action potentials (CAP).  They performed several experiments in which owls were immobilized and their round windows membranes removed in order to expose their inner ears.  They then took measurements using an electrode placed on the round window area of the inner ear and an audio implant in the middle ear canal to generate various tones.  Activity was measured at various frequencies. Based on the waveforms they observed, researchers deduced that the CMs of the owl remained relatively constant in terms of reactivity from the lowest frequency inputs measured up to the 10 kHz range.  However the CAP was typically defined by a sharp negative peak, which occurred rapidly after they stimulated the ear.  They also found that the largest of the measured CAP amplitudes were observed when sound stimuli between 6-7 kHz were played.  This increase in CAP activity corresponded to the distribution of the number of afferent nerve fibers coming from the regions of the owl’s papilla that would correspond to 6-7kHz stimulation. (Koppl et. Al 2007)

Barn owls are known for being able to hear up to the 10 kHz range so this was odd in that the findings implied it required more neuronal activity and/or higher decibels for the owl’s ear to process and respond to 10kHz ranges then was required for the owls ear to respond to other frequencies.  They postulated that this might have been overcome by the use of single neuronal units being recruited. They performed control experiments to support their findings by dabbing the round window with a chemical (S-AMPA) that destroyed the afferent nerve fibers. When measurements were taken, only the CM responded to stimulus. (Koppl et. Al 2007) This helped future researchers to understand how cochlear microphonics plays a role in barn owls’ hearing.

One amazing ability that barn owls have is the ability to discern specific sounds even in sound cluttered environments.  Humans also have this ability.  This has been dubbed the cocktail effect.  Spitzer et al. 2006 looked at the owl’s ability to discern two separate sounds when played close together.  Owls were placed in a sound attenuated chamber and played a fixed frequency sounds via a sound system over particular intervals. The first sound played would be designated the leading event.  While the leading event was playing the researchers would then begin to play a second sound at the same frequency as the leading sound yet placed at a different position in azimuth. This created sounds that acted similar to those in an echoic environment.  When sounds were more than 10 ms apart owls were able to easily double saccade (turn their gaze) first towards the leading source and then towards the lagging source with very good accuracy.  Once sounds became quicker than 10 ms in timing, owls exhibited higher error rates in determining the location of the leading vs. the lagging sound and generally would orient towards only the leading sound source.  (Spitzer et al. 2006)  According to Helmut Haas The precedence effect (or Haas effect) states that “When two identical sounds (i.e., identical sound waves of the same perceived intensity) originate from two sources at different distances from the listener, the sound created at the closest location is heard (arrives) first. To the listener, this creates the impression that the sound comes from that location alone due to a phenomenon that might be described as “involuntary sensory inhibition” in that one’s perception of later arrivals is suppressed.” (http://en.wikipedia.org/wiki/Haas_effect)  This study helped to show that the precedence effect does in fact take place in barn owls.  The higher the response time between the sound sources the higher the processing time needed by the owls to discern the sound sources.

What researchers noticed about Tyto alba was that sounds of the prey themselves played a huge role in auditory localization of prey, however visual cues also played a large part in how well the owl was able to localize prey.  Whitchurch et al. 2006 measured the timing of head saccades in response to both visual and auditory stimuli and attempted to correlate the amount of error found with both the directionality and intensity of a sound stimulus.  Barn owls use both visual tracking and auditory stimulation in order to create a spatial map of the location of their potential prey.  In response to a sound stimuli, a precise spatiotopic map (a map of a stimuli in space.)  comes first from the brains external nucleus of the inferior colliculus and then translates to the retinotopic map (a map of a stimuli in visual space) towards its optic tectum.  In this way, the barn owl gets both a visual and auditory interpretation of the location of that sound in space.  Researchers tried to find positive violations of Miller’s traditional race model.  The race model states that when two sensory signals race along separate pathways towards a common response generation site, the winning sensory signal will get to trigger the response.  If both sensory stimuli have an equal chance, the race model predicts that on average a multisensory scheme will be faster than a unisensory reaction time. (Whitchurch et al. 2006)  This suggests that by employing both auditory and visual inputs an animal can increase the probability of identifying the source of a weak stimulus.  The chances of accomplishing this are greater than if only one pathway existed.  According to the race model, although both potential pathways for sensory inputs exist, only one is chosen in the end as the primary sense used to track the prey.  The data found by the research actually disproves this.  When owls were presented with stimulation that evoked a shorter response time from head saccades that would typically yield an accurate visual response, the audio visual saccade occurred just as fast as the purely auditory response. (Whitchurch et al. 2006)  This implies that rather than a “one or the other” type response, neuronal responses to stimuli might instead favor a mixed usage of both auditory and visual stimuli to help locate prey.

Section 4: The neurological explanations of the owl’s abilities.

Although researchers have been able to identify and pinpoint how auditory specialization occurs on the part of the owl’s ears and head saccades themselves, there is more research which looks at the owl’s brain itself and tries to identify how the spatial mapping occurs on a neurological level.  Winkowski et al. 2006 took research like Whitchurch et al. performed and looked further into the process of visual and auditory cues.  Winkowski et al. were interested in the interaction between areas of the brain responsible for vision and how those areas are integrated with other particular areas of the brain.  When micro stimulation was placed onto the gaze control area of the barn owl’s forebrain, there was an activation of the auditory midbrain and they became more spatially selective.  This meant that the owl’s direction of their gaze was more selective for sounds that it might hear.  This was able to be measured by looking at electrical activity of the gaze center of the owls forebrain when microstimulation was placed on the corresponding auditory center of the midbrain. Other areas of the midbrain responsible for auditory processing which were not being stimulated by the forebrain area were not activated during stimulation of the forebrain.  The forebrain area known as the optic tectum is responsible for processing visual information.  The area specific stimulation of the midbrain by the forebrain shows a clear integration between visual information and its conversion into auditory spatial information.  When stimulation occurs, sensitivity to interaural timing differences (a measured difference in the rates of the arrival times of sounds) increases in various areas of the midbrain.  This increase in sensitivity showed that the owl’s midbrain was being regulated by the forebrain of Tyto alba (Winkowski et al 2006).  This helps to confirm that the owl’s vision and hearing not only work together in symposium but enhance one another’s functioning as well.

The mesencephalicus lateralis pars dorsalis (MLd) is a region of the midbrain nucleus found in birds that is responsible for the processing of acoustic behavior.  All birds have acoustic behaviors, including the echolocators, the song birds, the vocal learners and the auditory specialists like the owls.  The researchers decided to look at whether or not the variation in the size and volume of the MLd corresponded to the complexity of the tasks the animals had to accomplish.  This was done by dissecting the brains from 72 different species of birds and taking measurements of the brains overall volume, the volume of the optic tectum, and the mesencephalicus lateralis pars dorsalis.  The ratios of volumes of these structures were then compared to each other and log plots of the correlation of these values across the 72 species were identified.  When this was combined with the already published knowledge about the behavior of these animals in terms of whether they echolocate, or hunt via auditory specialization like the barn owl for example, they found a direct correlation to the size of the birds midbrains relative to the task that was required of them.  Owls, the auditory specialists all had a significantly larger midbrain nucleus than all the other types of birds.  This would logically correspond to the fact that owls hunt using special maps made via hearing.  Researchers also looked more closely at the relationship of asymmetrically eared owls vs. symmetrically eared owls.  They found that asymmetrically eared owls have an even larger volume midbrain than the symmetrically eared owls. (Iwaniuk et. Al. 2006) This logically made sense to the fact that most symmetrically eared owls do not rely mainly on hearing to hunt their prey.  Although Tyto alba uses vision as Winkowski et al pointed out, this still makes the asymmetrically eared owls like Tyto alba true auditory specialists.

As many of the investigations on Tyto alba have shown, the midbrain is part of the brain that allows Tyto alba to have its amazing auditory abilities.  Because of this midbrain specialization, McBride et. al used the owl’s middle brain as testing ground for the neurological model of learning.   Young juvenile owls were raised with a prism over their eyes that shifted the visual field 19 degrees.  After one year the dendritic numbers and spatial layouts of owls with prisms vs. owls without, were measured to see if there were any differences.  By  using a fluorescently labeled tracer, the tissue samples taken from juvenile barn owls raised with prismatic lenses over their eyes, showed that the owls exhibited a different and more complex set of dendritic neurons. It was observed that dendritic clusters that were spaced closer than 20 µm where shown to have higher rates of contact where as dendritic clusters that were spaced greater than 20 µm apart had less contact and there for implied a lack of neurological learning.  (McBride et al 2008)  This is the first time that a study has demonstrated that there is a change in the patterns of dendrites in the brain that correlates directly to an animal’s ability to adjust and learn.  However, generalizations and an unequal sample pool might cause this data to come under some scrutiny.  If this research is accurate it would paints a picture of the owl’s midbrains as being plastic and flexible.  It would also show on a neurological level a direct correlation between learning and neurological spacing.

Conclusions

Barn owls are amazing creatures with an amazing ability to locate prey based on sounds. The barn owls midbrain processes the timing differences between sounds heard on either side of the owl’s asymmetrical ears.  The owl’s forebrain stimulates the midbrain and helps to cue it’s visual system to gaze in a particular area.  Once gazing the owl can track its prey’s motion using head saccades and predict where the prey will be in order to intercept it.  It then takes off and attacks its prey with great speed being able to generally adjust its flight path accordingly.  All of this is done in pitch darkness in a matter of seconds.  Tyto alba research is important to understanding how we as humans process complex sounds and how our own brains are tuned to focus and pay attention to our surroundings.  Audio spatial mapping might have huge potential in military applications in activites such as tracking and espionage or even in planes, shipping or mining applications.  Spitzer and Takahashi’s research in particular helps us to understand how we are able to identify and pinpoint specific sounds in a loud and echoic environment.  Future research should look more into claims of Tyto alba being able to fly silently, as well as the owl’s midbrain nucleus and potential abilities for this area of the brain to learn and adapt to different sensory stimuli. For example, some research by Terry Takahashi, a major contributor of auditory research in Tyto alba, might look into the owls complete sensory fields and attempt to map the effects on the gaze center over a broad range of stimuli rather than a set few.  Other future research might test the pathways of control from the forebrain to the midbrain itself, paying special attention to a neurological ability to create new pathways, how different stimuli inputs map across the regions of the brains and how the owls respond to having modified sounds as stimuli inputs.  Regardless of the future research, current research shows us that Tyto alba is indeed one of the best audio locators in the animal kingdom.

Bibliography

1. http://www.allaboutbirds.org (Cornell Universities Bird Website)

2. http://en.wikipedia.org/wiki/Haas_effect (Wikipedia entry on Helmut Haas and his discovery of the Precedence Effect)

3. Fux M, Eilam, D (2009) How barn owls (Tyto alba) visually follow moving voles (Microtus socialis) before attacking them, Physiology & Behavior 98:359-366

4. Hausmann, L., Plachta, D. T.T., Singheiser, M., Brill, S., Wagner, H., (2008) In-flight corrections in free-flying barn owls (Tyto alba) during sound localization tasks, The Journal of Experimental Biology 211:2976-2988

5. Ilany, A., Eilam D., (2008) Wait before running for your life: defensive tactics of spiny mice (Acomys cahirinus) in evading barn owl (Tyto alba) attack, Behavioral Ecology and Sociobiology 62:923-933

6. Iwaniuk, A. N., Clayton, D. H., Wylie, D. R. W., (2006) Echolocation, vocal learning, auditory localization and the relative size of the avian auditory midbrain nucleus (MLd), Behavioural Brain Research, 167:305-317.

7. Koppl, C., Gleich, O., (2007) Evoked cochlear potentials in the barn owl,  Journal of Comparative Physiology 193:601-612.

8. Koppl, C., Nickel, R., (2007) Prolonged maturation of cochlear function in the barn owl after hatching, Journal of Comparative Physiology 193:613-624.

9. McBride, T. J., Rodriguez-Contreras, A., Trinh, A., Bailey, R., Debello, W. M., (2008) Learning Drives Differential Clustering of Axodendritic Contacts in the Barn Owl Auditory System, Journal of Neuroscience 28:6960-6973

10. Spitzer, M. W., Takahashi, T. T., (2006) Sound Localization by Barn Owls in a Simulated Echoic Environment, Journal of Neurophysiology 95:3571-3584

11. Whitchurch, E. A., Takahashi T. T.,(2006) Combined Auditory and Visual Stimuli Facilitate Head Saccades in the Barn Owl (Tyto alba) Journal of Neurophysiology 96:730-745

12. Winkowski, D. E., Knudsen, E. I., (2006) Top-down gain control of the auditory space map by gaze control circuitry in the barn owl Nature 439:336-339

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Posted on December 14, 2009, in Scientific Research and tagged , , , , , , , , , , , , . Bookmark the permalink. 2 Comments.

  1. The barn owl (Tyto alba) an auditory specalist .Thanks for nice post.I added to my twitter.

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