Lateralization of bird song
Encyclopedia
Oscine songbirds produce song through the vocal organ, the syrinx
, which is composed of bilaterally symmetric halves located where the trachea
separates into the two bronchi
. Using endoscopic
techniques, it has been observed that song is produced by air passing between a set of medial and lateral labia on each side of the syrinx . Song is produced bilaterally, in both halves, through each separate set of labia unless air is prevented from flowing through one side of the syrinx. Birds regulate the airflow through the syrinx with muscle
s—M. syringealis dorsalis and M. tracheobronchialis dorsalis—that control the medial and lateral labia in the syrinx, whose action may close off airflow. Song may, hence, be produced unilaterally through one side of the syrinx when the labia are closed in the opposite side.
conveying messages from the brain
to the syrinx was first observed in the 1970s. This lateral dominance was determined in a breed of canary, the waterschlager canary, bred for its long and complex song, by lesion
ing the ipsilateral tracheosyringeal branch of the hypoglossal nerve, disabling either the left or right syrinx. The numbers of song elements in the birds’ repertoires were greatly attenuated when the left side was cut, but only modestly attenuated when the right side was disabled, indicating left syringeal dominance of song production in these canaries. Similar lateralized effects have been observed in other species such as the white-crowned sparrow
(Zonotrichia leucophrys), the Java sparrow
(Lonchura oryzivora) and the zebra finch
(Taeniopygia guttata), which is right-side dominant. However, denervation in these birds does not entirely silence the affected syllables but creates qualitative changes in phonology
and frequency
.
When bilateral airflow and subsyringeal air sac pressure were monitored along with electromyographic
activity of expiratory abdominal
muscles in brown thrasher
s (Toxostoma rufum), it was observed that during unilateral production of song, expiratory abdominal muscle activity was the same on both sides. This indicates that while inspiration and syringeal song control may be lateralized, motor control
of respiratory
muscles possibly remains bilateral.
Muscles of the syrinx are controlled by the tracheosyringeal branch of the hypoglossal nerve
. Each syringeal half is ipsilaterally innervated by the hypoglossal motor nucleus (XIIts) in the brain, which in turn receives projections—mainly ipsilateral—from nucleus robustus (RA), an important song control nucleus that also regulates respiratory muscles. Laterality of song control has been observed all the way into the higher vocal center (HVC) brain region; unilateral lesions to HVC produce lateralized effects in the temporal patterning of song in the zebra finch .
Also see Bird song: Neurophysiology
but has been inbred by humans for its beautiful song. The outbred domestic canary, however, does not exhibit the strong lateralization of the waterschlager canary. Possibly explaining their strong left lateralization, canaries of the waterschlager strain contain an inherited auditory defect that decreases their sensitivity by up to 40 dB to sounds higher than 2 kHz, which are produced mainly by the right side of the syrinx.
produces very rapid clusters of notes that alternate in frequency, with the right syrinx producing the high frequency notes and the left syrinx producing low frequency notes. The entire cluster is sung during a single respiratory expiration, called "pulsatile expiration", in which no inflow of air occurs between notes. By alternating note production successively between each side of the syrinx and without ceasing expiration, a cowbird is able to rapidly and abruptly switch the frequency of notes back and forth between high and low frequencies. To see a cartoon of how syllables are produced in alternate sides of the syrinx, click here
s contain FM
sweep syllables as part of their repertoire that begin around 6 or 7 kHz and sweep downward continuously to 2 kHz
. Each of these syllables is sung unilaterally. However, the cardinal switches mid-syllable from employing the right syrinx at the high frequency beginning of the sweep to the left syrinx at the lower frequency end. This switch usually occurs when the sweep reaches the 3.5 to 4.0 kHz range. The transition is abrupt yet timed so precisely that neither sonograms
nor audition
can detect the switch. To see a cartoon of how the syrinx produces cardinal song, click here.
has the ability to mimic the songs of other species, it has been useful in determining whether the vocal motor patterns employed by particular species in producing their unique song types are constrained by acoustic
properties or whether the unique song types may also be produced by different motor patterns generated by the same songbird vocal system. When juvenile mockingbirds were tutored with the recorded or synthesized song of a cardinal or cowbird, the mockingbirds employed the same respiratory and lateralized vocal pattern as the original species to produce its mimicked song. When the mockingbird motor pattern differed from the tutor motor pattern, the song output also differed, suggesting that the vocal motor pattern is largely determined by the acoustic restraints of the song type.
Even though the mockingbird was able to mimic the FM sweeps of cardinals by employing the same motor pattern—switching mid-syllable from right syrinx to left syrinx—the mockingbird did not perform the transition seamlessly. This indicates that precise unilateral control of song production in the syrinx of certain birds, such as cardinals, has allowed them to become unique vocal specialists.
to potential mates. Supporting this hypothesis, certain syllables called "sexy syllables" sung by male canaries at high frequency are more effective than others in eliciting sexual displays from females. These particular syllables all contain two notes that are sung alternately by each side of the syrinx. Thus, control of the rapid switching from one side of the syrinx to the other is required to produce these attractive syllables.
Lateralization also allows for rapid and abrupt frequency changes. Studies of mockingbirds mimicking tone
pairs in which the first tone was either higher or lower than a median tone of 2 kHz (either side is capable of producing this median tone) revealed that alternating sides of the syrinx for each note was necessary to reproduce them correctly.
. Correct mimicking was performed by singing the first syllable with the appropriate side of the syrinx—right for a high frequency tone and left for low frequency—and the second median tone with the opposite side. When the same side was used for both tones, the step-wise frequency change between the tones became slurred, suggesting that lateralization allows for abrupt frequency changes in song.
Syrinx (biology)
Syrinx is the name for the vocal organ of birds. Located at the base of a bird's trachea, it produces sounds without the vocal cords of mammals. The sound is produced by vibrations of some or all of the membrana tympaniformis and the pessulus caused by air flowing through the syrinx...
, which is composed of bilaterally symmetric halves located where the trachea
Vertebrate trachea
In tetrapod anatomy the trachea, or windpipe, is a tube that connects the pharynx or larynx to the lungs, allowing the passage of air. It is lined with pseudostratified ciliated columnar epithelium cells with goblet cells that produce mucus...
separates into the two bronchi
Bronchus
A bronchus is a passage of airway in the respiratory tract that conducts air into the lungs. The bronchus branches into smaller tubes, which in turn become bronchioles....
. Using endoscopic
Endoscopy
Endoscopy means looking inside and typically refers to looking inside the body for medical reasons using an endoscope , an instrument used to examine the interior of a hollow organ or cavity of the body. Unlike most other medical imaging devices, endoscopes are inserted directly into the organ...
techniques, it has been observed that song is produced by air passing between a set of medial and lateral labia on each side of the syrinx . Song is produced bilaterally, in both halves, through each separate set of labia unless air is prevented from flowing through one side of the syrinx. Birds regulate the airflow through the syrinx with muscle
Muscle
Muscle is a contractile tissue of animals and is derived from the mesodermal layer of embryonic germ cells. Muscle cells contain contractile filaments that move past each other and change the size of the cell. They are classified as skeletal, cardiac, or smooth muscles. Their function is to...
s—M. syringealis dorsalis and M. tracheobronchialis dorsalis—that control the medial and lateral labia in the syrinx, whose action may close off airflow. Song may, hence, be produced unilaterally through one side of the syrinx when the labia are closed in the opposite side.
Early experiments discover lateralization
Lateral dominance of the hypoglossal nerveHypoglossal nerve
The hypoglossal nerve is the twelfth cranial nerve , leading to the tongue. The nerve arises from the hypoglossal nucleus and emerges from the medulla oblongata in the preolivary sulcus separating the olive and the pyramid. It then passes through the hypoglossal canal...
conveying messages from the brain
Brain
The brain is the center of the nervous system in all vertebrate and most invertebrate animals—only a few primitive invertebrates such as sponges, jellyfish, sea squirts and starfishes do not have one. It is located in the head, usually close to primary sensory apparatus such as vision, hearing,...
to the syrinx was first observed in the 1970s. This lateral dominance was determined in a breed of canary, the waterschlager canary, bred for its long and complex song, by lesion
Lesion
A lesion is any abnormality in the tissue of an organism , usually caused by disease or trauma. Lesion is derived from the Latin word laesio which means injury.- Types :...
ing the ipsilateral tracheosyringeal branch of the hypoglossal nerve, disabling either the left or right syrinx. The numbers of song elements in the birds’ repertoires were greatly attenuated when the left side was cut, but only modestly attenuated when the right side was disabled, indicating left syringeal dominance of song production in these canaries. Similar lateralized effects have been observed in other species such as the white-crowned sparrow
White-crowned Sparrow
The White-crowned Sparrow is a medium-sized sparrow native to North America.- Description :Adults are long and have black and white stripes on their head, a grey face, brown streaked upper parts and a long tail. The wings are brown with bars and the underparts are grey. Their bill is pink or yellow...
(Zonotrichia leucophrys), the Java sparrow
Java Sparrow
The Java Sparrow, Padda oryzivora also known as Java Finch, Java Rice Sparrow or Java Rice Bird is a small passerine bird. This estrildid finch is a resident breeding bird in Java, Bali and Bawean in Indonesia. It is a popular cagebird, and has been introduced in a large number of other...
(Lonchura oryzivora) and the zebra finch
Zebra Finch
The Zebra Finch, Taeniopygia guttata, is the most common and familiar estrildid finch of Central Australia and ranges over most of the continent, avoiding only the cool moist south and the tropical far north. It also can be found natively in Indonesia and East Timor...
(Taeniopygia guttata), which is right-side dominant. However, denervation in these birds does not entirely silence the affected syllables but creates qualitative changes in phonology
Phonology
Phonology is, broadly speaking, the subdiscipline of linguistics concerned with the sounds of language. That is, it is the systematic use of sound to encode meaning in any spoken human language, or the field of linguistics studying this use...
and frequency
Frequency
Frequency is the number of occurrences of a repeating event per unit time. It is also referred to as temporal frequency.The period is the duration of one cycle in a repeating event, so the period is the reciprocal of the frequency...
.
Respiratory control and neurophysiology
In waterslager canaries, which produce most syllables using the left syrinx, as soon as a unilaterally produced syllable finishes, the right side opens briefly to allow inspiratory airflow through both bronchi before being closed again for left syrinx song production. During this “mini-breath” the left side may remain partially or fully adducted, allowing less inspiratory airflow than the right side while remaining ready to quickly resume singing.When bilateral airflow and subsyringeal air sac pressure were monitored along with electromyographic
Electromyography
Electromyography is a technique for evaluating and recording the electrical activity produced by skeletal muscles. EMG is performed using an instrument called an electromyograph, to produce a record called an electromyogram. An electromyograph detects the electrical potential generated by muscle...
activity of expiratory abdominal
Abdomen
In vertebrates such as mammals the abdomen constitutes the part of the body between the thorax and pelvis. The region enclosed by the abdomen is termed the abdominal cavity...
muscles in brown thrasher
Brown Thrasher
The Brown Thrasher , sometimes erroneously called the Brown Thrush, is a bird in the Mimidae family, a group that also includes the New World catbirds and mockingbirds.-Description:...
s (Toxostoma rufum), it was observed that during unilateral production of song, expiratory abdominal muscle activity was the same on both sides. This indicates that while inspiration and syringeal song control may be lateralized, motor control
Motor skill
A motor skill is a learned sequence of movements that combine to produce a smooth, efficient action in order to master a particular task. The development of motor skill occurs in the motor cortex, the region of the cerebral cortex that controls voluntary muscle groups.- Development of motor skills...
of respiratory
Respiratory system
The respiratory system is the anatomical system of an organism that introduces respiratory gases to the interior and performs gas exchange. In humans and other mammals, the anatomical features of the respiratory system include airways, lungs, and the respiratory muscles...
muscles possibly remains bilateral.
Muscles of the syrinx are controlled by the tracheosyringeal branch of the hypoglossal nerve
Hypoglossal nerve
The hypoglossal nerve is the twelfth cranial nerve , leading to the tongue. The nerve arises from the hypoglossal nucleus and emerges from the medulla oblongata in the preolivary sulcus separating the olive and the pyramid. It then passes through the hypoglossal canal...
. Each syringeal half is ipsilaterally innervated by the hypoglossal motor nucleus (XIIts) in the brain, which in turn receives projections—mainly ipsilateral—from nucleus robustus (RA), an important song control nucleus that also regulates respiratory muscles. Laterality of song control has been observed all the way into the higher vocal center (HVC) brain region; unilateral lesions to HVC produce lateralized effects in the temporal patterning of song in the zebra finch .
Also see Bird song: Neurophysiology
Canary (Serinus canaria)
The waterschlager canary is the most robust example of unilateral syringeal dominance, creating song of which 90% of the syllables are produced by the left syrinx, as determined by recording respiratory pressure and airflow through each side during singing. Waterschlager canaries with left tracheosyringeal nerve cuts are only able to produce up to 26% of the pre-operation syllable repertoire. The waterschlager canary strain is conspecific to the domestic canaryDomestic Canary
The Domestic Canary, often simply known as the canary, is a domesticated form of the wild Canary, a small songbird in the finch family originating from the Macaronesian Islands ....
but has been inbred by humans for its beautiful song. The outbred domestic canary, however, does not exhibit the strong lateralization of the waterschlager canary. Possibly explaining their strong left lateralization, canaries of the waterschlager strain contain an inherited auditory defect that decreases their sensitivity by up to 40 dB to sounds higher than 2 kHz, which are produced mainly by the right side of the syrinx.
Brown-headed cowbird (Molothrus ater)
The brown-headed cowbirdBrown-headed Cowbird
The Brown-headed Cowbird is a small brood parasitic icterid of temperate to subtropical North America. They are permanent residents in the southern parts of their range; northern birds migrate to the southern United States and Mexico in winter, returning to their summer habitat around March or...
produces very rapid clusters of notes that alternate in frequency, with the right syrinx producing the high frequency notes and the left syrinx producing low frequency notes. The entire cluster is sung during a single respiratory expiration, called "pulsatile expiration", in which no inflow of air occurs between notes. By alternating note production successively between each side of the syrinx and without ceasing expiration, a cowbird is able to rapidly and abruptly switch the frequency of notes back and forth between high and low frequencies. To see a cartoon of how syllables are produced in alternate sides of the syrinx, click here
Northern Cardinal (Cardinalis cardinalis)
Northern cardinalNorthern Cardinal
The Northern Cardinal or Redbird or Common Cardinal is a North American bird in the genus Cardinalis. It can be found in southern Canada, through the eastern United States from Maine to Texas and south through Mexico...
s contain FM
Frequency modulation
In telecommunications and signal processing, frequency modulation conveys information over a carrier wave by varying its instantaneous frequency. This contrasts with amplitude modulation, in which the amplitude of the carrier is varied while its frequency remains constant...
sweep syllables as part of their repertoire that begin around 6 or 7 kHz and sweep downward continuously to 2 kHz
Hertz
The hertz is the SI unit of frequency defined as the number of cycles per second of a periodic phenomenon. One of its most common uses is the description of the sine wave, particularly those used in radio and audio applications....
. Each of these syllables is sung unilaterally. However, the cardinal switches mid-syllable from employing the right syrinx at the high frequency beginning of the sweep to the left syrinx at the lower frequency end. This switch usually occurs when the sweep reaches the 3.5 to 4.0 kHz range. The transition is abrupt yet timed so precisely that neither sonograms
Spectrogram
A spectrogram is a time-varying spectral representation that shows how the spectral density of a signal varies with time. Also known as spectral waterfalls, sonograms, voiceprints, or voicegrams, spectrograms are used to identify phonetic sounds, to analyse the cries of animals; they were also...
nor audition
Hearing (sense)
Hearing is the ability to perceive sound by detecting vibrations through an organ such as the ear. It is one of the traditional five senses...
can detect the switch. To see a cartoon of how the syrinx produces cardinal song, click here.
Northern Mockingbird (Mimus polyglottus)
Because the mockingbirdNorthern Mockingbird
The Northern Mockingbird, Mimus polyglottos, is the only mockingbird commonly found in North America. This species was first described by Linnaeus in his Systema naturae in 1758 as Turdus polyglottos....
has the ability to mimic the songs of other species, it has been useful in determining whether the vocal motor patterns employed by particular species in producing their unique song types are constrained by acoustic
Acoustics
Acoustics is the interdisciplinary science that deals with the study of all mechanical waves in gases, liquids, and solids including vibration, sound, ultrasound and infrasound. A scientist who works in the field of acoustics is an acoustician while someone working in the field of acoustics...
properties or whether the unique song types may also be produced by different motor patterns generated by the same songbird vocal system. When juvenile mockingbirds were tutored with the recorded or synthesized song of a cardinal or cowbird, the mockingbirds employed the same respiratory and lateralized vocal pattern as the original species to produce its mimicked song. When the mockingbird motor pattern differed from the tutor motor pattern, the song output also differed, suggesting that the vocal motor pattern is largely determined by the acoustic restraints of the song type.
Even though the mockingbird was able to mimic the FM sweeps of cardinals by employing the same motor pattern—switching mid-syllable from right syrinx to left syrinx—the mockingbird did not perform the transition seamlessly. This indicates that precise unilateral control of song production in the syrinx of certain birds, such as cardinals, has allowed them to become unique vocal specialists.
Possible functions
Because the lateralized control of songs of certain species, such as cardinals, demands such precision in motor control, the ability to produce high-quality, seamless syllables may provide an indicator of fitnessFitness (biology)
Fitness is a central idea in evolutionary theory. It can be defined either with respect to a genotype or to a phenotype in a given environment...
to potential mates. Supporting this hypothesis, certain syllables called "sexy syllables" sung by male canaries at high frequency are more effective than others in eliciting sexual displays from females. These particular syllables all contain two notes that are sung alternately by each side of the syrinx. Thus, control of the rapid switching from one side of the syrinx to the other is required to produce these attractive syllables.
Lateralization also allows for rapid and abrupt frequency changes. Studies of mockingbirds mimicking tone
Pitch (music)
Pitch is an auditory perceptual property that allows the ordering of sounds on a frequency-related scale.Pitches are compared as "higher" and "lower" in the sense associated with musical melodies,...
pairs in which the first tone was either higher or lower than a median tone of 2 kHz (either side is capable of producing this median tone) revealed that alternating sides of the syrinx for each note was necessary to reproduce them correctly.
. Correct mimicking was performed by singing the first syllable with the appropriate side of the syrinx—right for a high frequency tone and left for low frequency—and the second median tone with the opposite side. When the same side was used for both tones, the step-wise frequency change between the tones became slurred, suggesting that lateralization allows for abrupt frequency changes in song.
See also
- Syrinx (biology)Syrinx (biology)Syrinx is the name for the vocal organ of birds. Located at the base of a bird's trachea, it produces sounds without the vocal cords of mammals. The sound is produced by vibrations of some or all of the membrana tympaniformis and the pessulus caused by air flowing through the syrinx...
- Bird songBird songBird vocalization includes both bird calls and bird songs. In non-technical use, bird songs are the bird sounds that are melodious to the human ear. In ornithology and birding, songs are distinguished by function from calls.-Definition:The distinction between songs and calls is based upon...
- Lateralization of brain functionLateralization of brain functionA longitudinal fissure separates the human brain into two distinct cerebral hemispheres, connected by the corpus callosum. The sides resemble each other and each hemisphere's structure is generally mirrored by the other side. Yet despite the strong anatomical similarities, the functions of each...
- Animal communicationAnimal communicationAnimal communication is any behavior on the part of one animal that has an effect on the current or future behaviour of another animal. The study of animal communication, is sometimes called Zoosemiotics has played an important part in the...
- BioacousticsBioacousticsBioacoustics is a cross-disciplinary science that combines biology and acoustics. Usually it refers to the investigation of sound production, dispersion through elastic media, and reception in animals, including humans. This involves neurophysiological and anatomical basis of sound production and...
External links
- X-ray video of a cardinal singing
- Macaulay Library at the Cornell Lab of Ornithology is the world's largest collection of animal sounds and associated video.
- xeno-canto a community database with ~20000 recordings of ~4000 bird species(July 2008).