Vocal learning
Vocal learning is the ability to modify acoustic and syntactic sounds, acquire new sounds via imitation, and produce vocalizations. "Vocalizations" in this case refers only to sounds generated by the vocal organ (mammalian
Classification
Historically, species have been classified into the binary categories of vocal learner or vocal non-learner based on their ability to produce novel vocalizations or imitate other species, with evidence from
Vocal learning phenotype also differ within groups and closely related species will not display the same abilities. Within avian vocal learners, for example,
Continuum hypothesis
Even further complicating the original binary classification is evidence from recent studies that suggests that there is greater variability in a non-learner's ability to modify vocalizations based on experience than previously thought. Findings in suboscine
Evidence of vocal learning in various species
Known vocal learners
Birds
The most extensively studied
Bats
The first evidence for audio-vocal learning in a non-human mammal was produced by Karl-Heinz Esser in 1994. Hand-reared infant lesser spear-nosed bats (Phyllostomos discolor) were able to adapt their isolation calls to an external reference signal. Isolation calls in a control group that had no reference signal did not show the same adaptation.[8]
Further evidence for vocal learning in bats appeared in 1998 when Janette Wenrick Boughman studied female
Cetaceans
Whales
Male
Whale songs recorded along the east coast of Australia in 1996 showed introduction of a novel song by two foreign whales who had migrated from the west Australian coast to the east Australian coast. In just two years, all members of the population had switched songs. This new song was nearly identical to ones sung by migrating humpback whales on the west Australian Coast, and the two new singers who introduced the song are hypothesized to have introduced the new "foreign" song to the population on the east Australian coast.[10]
Vocal learning has also been seen in
Dolphins
Captive bottlenose dolphins (Tursiops truncatus) can be trained to emit sounds through their blowhole in open air. Through training, these vocal emissions can be altered from natural patterns to resemble sounds like the human voice, measurable through the number of bursts of sound emitted by the dolphin. In 92% of exchanges between humans and dolphins, the number of bursts equaled ±1 of the number of syllables spoken by a human.[12] Another study used an underwater keyboard to demonstrate that dolphins are able to learn various whistles in order to do an activity or obtain an object. Complete mimicry occurred within ten attempts for these trained dolphins.[13] Other studies of dolphins have given even more evidence of spontaneous mimicry of species-specific whistles and other biological and computer-generated signals.[14]
Such vocal learning has also been identified in wild bottlenose dolphins. Bottlenose dolphins develop a distinct signature whistle in the first few months of life, which is used to identify and distinguish itself from other individuals. This individual distinctiveness could have been a driving force for evolution by providing higher species fitness since complex communication is largely correlated with increased intelligence. However, vocal identification is present in vocal non-learners as well. Therefore, it is unlikely that individual identification was a primary driving force for the evolution of vocal learning. Each signature whistle can be learned by other individuals for identification purposes and are used primarily when the dolphin in question is out of sight. Bottlenose dolphins use their learned whistles in matching interactions, which are likely to be used while addressing each other, signalling alliance membership to a third party, or preventing deception by an imitating dolphin.[15]
Mate attraction and territory defense have also been seen as possible contributors to vocal learning evolution. Studies on this topic point out that while both vocal learners and non-learners use vocalizations to attract mates or defend territories, there is one key difference: variability. Vocal learners can produce a more varied arrangement of vocalizations and frequencies, which studies show may be more preferred by females. For example, Caldwell[16] observed that male Atlantic bottlenose dolphins may initiate a challenge by facing another dolphin, opening its mouth, thereby exposing its teeth, or arching its back slightly and holding its head downward. This behavior is more along the lines of visual communication but still may or may not be accompanied by vocalizations such as burst-pulsed sounds. The burst-pulsed sounds, which are more complex and varied than the whistles, are often utilized to convey excitement, dominance or aggression such as when they are competing for the same piece of food.[17] The dolphins also produce these forceful sounds when in the presence of other individuals moving towards the same prey. On the sexual side, Caldwell saw that dolphins may solicit a sexual response from another by swimming in front of it, looking back, and rolling on its side to display the genital region.[18] These observations provide yet another example of visual communication where dolphins exhibit different postures and non-vocal behaviors to communicate with others that also may or may not be accompanied by vocalizations. Sexual selection for greater variability, and thus in turn vocal learning, may then be a major driving force for the evolution of vocal learning.
Seals
Captive harbor seals (Phoca vitulina) were recorded mimicking human words such as "hello", "Hoover" (the seal's own name) and producing other speech-like sounds. Most of the vocalizations occurred during the reproductive season.[19]
More evidence of vocal learning in seals occurs in
Harem holders frequently vocalize to keep peripheral males away from females, and these vocalizations are the dominant component in a young juvenile's acoustic habitat. Successful vocalizations are heard by juveniles, who then imitate these calls as they get older in an attempt to obtain a harem for themselves. Novel vocal types expressed by dominant males spread quickly through populations of breeding elephant seals and are even imitated by juveniles in the same season.
Genetic analysis indicated that successful vocal patterns were not passed down hereditarily, indicating that this behavior is learned. Progeny of successful harem holders do not display their father's vocal calls and the call that makes one male successful often disappears entirely from the population.[20]
Elephants
Mlaika, a ten-year-old adolescent female African elephant, has been recorded imitating truck sounds coming from the Nairobi-Mombasa highway three miles away. Analysis of Mlaika's truck-like calls show that they are different from the normal calls of African elephants, and that her calls are a general model of truck sounds, not copies of the sounds of trucks recorded at the same time of the calls. In other words, Mlaika's truck calls are not imitations of the trucks that she hears, but rather, a generalized model she developed over time.
Other evidence of vocal learning in elephants occurred in a cross-fostering situation with a captive African elephant. At the
Controversial or limited vocal learners
The following species are not formally considered vocal learners, but some evidence has suggested they may have limited abilities to modify their vocalizations. Further research is needed in these species to fully understand their learning abilities.
Non-human primates
Early research asserted that primate calls are fully formed at an early age in development, yet recently some studies have suggested these calls are modified later in life.
Other studies argue that
Mice
There has been intense debate on whether these songs are innate or learned. In 2011, Kikusui et al. cross-fostered two strains of mice with distinct song
In 2013, Mahrt et al. showed that genetically deafened mice produce calls of the same types, number, duration, frequency as normal hearing mice. This finding shows that mice do not require auditory experience to produce normal vocalizations, suggesting that mice are not vocal learners.[31]
With this conflicting evidence, it remains unclear whether mice are vocal non-learners or limited vocal learners.
Goats
When
Evolution
As vocal learning is such a rare trait that evolved in distant groups, there are many theories to explain the striking similarities between vocal learners, especially within avian vocal learners.
Adaptive advantage
There are several proposed hypotheses that explain the selection for vocal learning based on environment and behavior. These include:[32]
- Individual identification: In most vocal-learning species, individuals have their own songs which serve as a unique signature to differentiate themselves from others in the population, which some suggest has driven selection of vocal learning. However, identification by voice, rather than by song or name, is present in vocal non-learners as well. Among vocal learners, only bottlenose dolphins actually use unique names. Therefore, it is unlikely that individual identification was a primary driving force for the evolutionof vocal learning.
- Semantic communication: Semantic vocal communication associates specific vocalizations with animate or inanimate objects to convey a factual message. This hypothesis asserts that vocal learning evolved to facilitate enhanced communication of these specific messages as opposed to affective communication, which conveys emotional content. For example, humans are able to shout "watch out for that car!" when another is in danger while crossing the street instead of just making a noise to indicate urgency, which is less effective at conveying the exact danger at hand. However, many vocal non-learners, including chickens and velvet monkeys, have been shown to use their innate calls to communicate semantic information such as ‘a food source’ or 'predator.' Further discrediting this hypothesis is the fact that vocal learning birds also use innate calls for this purpose and only rarely use their learned vocalizations for semantic communication (for example, the grey parrotcan mimic human speech and the black-capped chickadee uses calls to indicate predator size). As learned vocalizations rarely convey semantic information, this hypothesis also does not fully explain the evolution of vocal learning.
- Mate attraction and territory defense: While both vocal learners and non-learners use vocalizations to attract mates or defend territories, there is one key difference: variability. Vocal learners can produce more varied songbirds. For example, canaries use two voices to produce large frequency modulation variations called "sexy syllables" or "sexy songs", which are thought to stimulate estrogen production in females. When vocal non-learner females were presented with artificially increased frequency modulations in their innate vocalizations, more mating was stimulated. Sexual selectionfor greater variability, and thus in turn vocal learning, may then be a major driving force for the evolution of vocal learning.
- Rapid adaptation to sound propagation in different environments: Vocal non-learners produce their sounds best in specific habitats, making them more susceptible to changes in the environment. For example, pigeons' low-frequency calls travel best near the ground, and so communication higher in the air is much less effective. In contrast, vocal learners can change voice characteristics to suit their current environment, which presumably allows for better group communication.
Predatory pressure
With the many possible advantages outlined above, it still remains unclear as to why vocal learning is so rare. One proposed explanation is that predatory pressure applies a strong selective force against vocal learning.
While little research has been done in this area, some studies have supported the predation hypothesis. One study showed that Bengalese finches bred in captivity for 250 years without predation or human selection for singing behavior show increased variability in syntax than their conspecifics in the wild. A similar experiment with captive zebra finches demonstrated the same result as captive birds had increased song variability, which was then preferred by females.[33] Although these studies are promising, more research is needed in this area to compare predation rates across vocal learners and non-learners.
Phylogeny
Birds
Modern birds supposedly evolved from a common ancestor around the
- Independent convergent evolution: All three avian groups evolved vocal learning and similar neural pathways independently (not through a common ancestor). This suggests that there are strong epigeneticconstraints imposed by the environment or morphological needs, and so this hypothesis predicts that groups that newly evolve vocal learning will also develop similar neural circuits.
- Common ancestor: This alternative hypothesis suggests that vocal learning birds evolved the trait from a distant common ancestor, which was then lost four independent times in interrelated vocal non-learners. Possible causes include high survival costs of vocal learning (predation) or weak adaptive benefits that did not induce strong selection for the trait for organisms in other environments.
- Rudimentary structures in non-learners: This alternative hypothesis states that avian non-learners actually do possess rudimentary or undeveloped brain structures necessary for song learning, which were enlarged in vocal learning species. Significantly, this concept challenges the current assumption that vocal nuclei are unique to vocal learners, suggesting that these structures are universal even in other groups such as mammals.
- Motor theory: This hypothesis suggests that cerebral systems that control vocal learning in distantly related animals evolved as specializations of a pre-existing motor system inherited from a common ancestor. Thus in avian vocal learners, each of the three groups of vocal learning birds evolved cerebral vocal systems independently, but the systems were constrained by a previous genetically determined motor system inherited from the common ancestor that controls learned movement sequencing. Evidence for this hypothesis was provided by Feenders and colleagues in 2008 as they found that EGR1, an immediate early gene associated with increases in neuronal activity, was expressed in forebrain regions surrounding or directly adjacent to song nuclei when vocal learning birds performed non-vocal movement behaviors such as hopping and flying. In non-learners, comparable areas were activated, but without the adjacent presence of song nuclei.[34] EGR1 expression patterns were correlated with the amount of movement, just as its expression typically correlates with the amount of singing performed in vocal birds. These finding suggest that vocal learning brain regions developed from the same cell lineages that gave rise to the motor pathway, which then formed a direct projection onto the brainstem vocal motor neurons to provide greater control.[1]
Currently, it remains unclear as to which of these hypotheses is the most accurate.
Primates
In
Neurobiology
Neural pathways in avian vocal learners
As avian vocal learners are the most amenable to experimental manipulations, the vast majority of work to elucidate the neurobiological mechanisms of vocal learning has been conducted with zebra finches, with a few studies focusing on
Parallel Song Nuclei in Avian Vocal Learners | ||
---|---|---|
Songbirds | Parrots | Hummingbirds |
HVC: a letter based name | NLC: central nucleus of the lateral nidopallium | VLN: vocal nucleus of the lateral nidopallium |
RA: robust nucleus of the arcopallium | AAC: central nucleus of the anterior arcopallium | VA: vocal nucleus of the arcopallium |
MAN: magnocellular nucleus of anterior nidopallium | NAOc: oval nucleus of the anterior nidopallium complex | |
Area X: area X of the striatum | MMSt: magnocellular nucleus of the anterior striatum | |
DLM: medial nucleus of dorsolateral thalamus | DMM: magnocellular nucleus of the dorsomedial thalamus | |
MO: oval nucleus of the mesopallium | MOc: oval nucleus of the mesopallium complex |
Vocal nuclei are found in two separate brain pathways, which will be described in
The posterior vocal pathway (also known as vocal motor pathway), involved in the production of learned vocalizations, begins with projections from a nidopallial nucleus, the
The anterior vocal pathway (also known as vocal learning pathway) is associated with learning, syntax, and social contexts, starting with projections from the magnocellular nucleus of the anterior nidopallium (MAN) to the striatal nucleus Area X. Area X then projects to the medial nucleus of dorsolateral thalamus (DLM), which ultimately projects back to MAN in a loop[38] The lateral part of MAN (LMAN) generates variability in song, while Area X is responsible for stereotypy, or the generation of low variability in syllable production and order after song crystallization.[32]
Despite the similarities in vocal learning neural circuits, there are some major connectivity differences between the posterior and anterior pathways among avian vocal learners. In
An auditory pathway that is used for
Critical period
The development of the sensory modalities necessary for song learning occurs within a “critical period” of development that varies among avian vocal learners. Closed-ended learners such as the zebra finch and aphantochroa hummingbird can only learn during a limited time period and subsequently produce highly stereotyped or non-variable vocalizations consisting of a single, fixed song which they repeat their entire lives. In contrast, open-ended learners, including canaries and various parrot species, display significant plasticity and continue to learn new songs throughout the course of their lives.[40]
In the male zebra finch, vocal learning begins with a period of sensory acquisition or
The neural mechanisms behind the closing of the
Previous research has suggested that the length of the
In humans
Humans seem to have analogous anterior and posterior vocal pathways which are implicated in speech production and learning. Parallel to the avian posterior vocal pathway mentioned above is the motor cortico-brainstem pathway. Within this pathway, the face motor cortex projects to the nucleus ambiguous of the medulla, which then projects to the muscles of the larynx. Humans also have a vocal pathway that is analogous to the avian anterior pathway. This pathway is a cortico-basal ganglia-thalamic-cortico loop which begins at a strip of the premotor cortex, called the cortical strip, which is responsible for speech learning and syntax production. The cortical strip includes spans across five brain regions: the anterior insula, Broca's area, the anterior dorsal lateral prefrontal cortex, the anterior pre-supplementary motor area, and the anterior cingulate cortex. This cortical strip has projections to the anterior striatum which projects to the globus pallidus to the anterior dorsal thalamus back to the cortical strip. All of these regions are also involved in syntax and speech learning.[52]
Genetic applications to humans
In addition to the similarities in the neurobiological circuits necessary for vocalizations between animal vocal learners and humans, there are also a few genetic similarities. The most prominent of these genetic links are the
These similarities are especially interesting in the context of the aforementioned avian song circuit. FOXP2 is expressed in the avian Area X, and is especially highly expressed in the
Additionally, it has been suggested that due to the overlap of FOXP1 and FOXP2 expression in
These genetic links have important implications for studying the origin of language because FOXP2 is so similar among vocal learners and humans, as well as important implications for understanding the etiology of certain speech and language disorders in humans.
Currently, no other genes have been linked as compellingly to vocal learning in animals or humans.
See also
- Animal cognition
- Bioacoustics
- Biolinguistics
- Biomusic
- Birdsong
- Entrainment
- Evolution of language
- Evolution of music
- Evolutionary linguistics
- Evolutionary psychology
- Human voice
- Phonation
- Social learning
- Speech repetition
- Talking animal
- Whale song
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