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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 larynx or avian syrinx) as opposed to by the lips, teeth, and tongue, which require substantially less motor control. A rare trait, vocal learning is a critical substrate for spoken language and has only been detected in eight animal groups despite the wide array of vocalizing species; these include humans, bats, cetaceans, pinnipeds (Pinniped and sea lions), elephants, and three distantly related bird groups including songbirds, parrots, and hummingbirds. Vocal learning is distinct from auditory learning, or the ability to form memories of sounds heard, a relatively common trait which is present in all vertebrates tested. For example, dogs can be trained to understand the word "sit" even though the human word is not in its innate auditory repertoire (auditory learning). However, the dog cannot imitate and produce the word "sit" itself as vocal learners can.
Vocal learning phenotype also differ within groups and closely related species will not display the same abilities. Within avian vocal learners, for example, zebra finch songs only contain strictly linear transitions that go through different syllables in a motif from beginning to end, yet mockingbird and nightingale songs show element repetition within a range of legal repetitions, non-adjacent relationships between distant song elements, and forward and backward branching in song element transitions. Parrots are even more complex as they can imitate the speech of heterospecifics like humans and synchronize their movements to a rhythmic beat.
Further evidence for vocal learning in bats appeared in 1998 when Janette Wenrick Boughman studied female greater spear-nosed bats ( Phyllostomus hastatus). These bats live in unrelated groups and use group contact calls that differ among social groups. Each social group has a single call, which differs in frequency and temporal characteristics. When individual bats were introduced to a new social group, the group call began to morph, taking on new frequency and temporal characteristics, and over time, calls of transfer and resident bats in the same group more closely resembled their new modified call than their old calls.
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.
Vocal learning has also been seen in ( Orcinus orca). Two juvenile killer whales, separated from their natal pods, were seen mimicking cries of California sea lions ( Zalophus californianus) that were near the region they lived in. The composition of the calls of these two juveniles were also different from their natal groups, reflecting more of the sea lion calls than that of the whales.
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.
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 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. 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. 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.
More evidence of vocal learning in seals occurs in southern elephant seals ( Mirounga leonine). Young males imitate the vocal cries of successful older males during their breeding season. northern and southern elephant seals have a highly polygynous mating system with a vast disparity in mating success. In other words, few males guard huge harems of females, eliciting intense male-male competition. Antagonistic vocal cries play an important role in inter-male competitions and are hypothesized to demonstrate the resource-holding potential of the emitter. In both species, antagonistic vocal cries vary geographically and are structurally complex and individually distinct. Males displays unique calls, which can be identified by the specific arrangement of syllable and syllable parts.
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.
Other evidence of vocal learning in elephants occurred in a cross-fostering situation with a captive African elephant. At the Basel Zoo in Switzerland, Calimero, a male African elephant, was kept with two female Asian elephants. Recordings of his cries shows evidence of chirping noises, typically only produced by Asian elephants. The duration and frequency of these calls differs from recorded instances of chirping calls from other African elephants and more closely resembles the chirping calls of Asian elephants.
Other studies argue that non-human primates do have some limited vocal learning ability, demonstrating that they can modify their vocalizations in a limited fashion through laryngeal control and lip movements. For example, chimpanzees in both captivity and in the wild have been recorded producing novel sounds to attract attention. By puckering their lips and making a vibrating sounds, they can make a "raspberry" call, which has been imitated by both naïve captive and wild individuals. There is also evidence of an orangutan learning to whistle by copying a human, an ability previously unseen in the species. A cross-fostering experiment with and showed convergence in pitch and other acoustic features in their supposedly innate calls, demonstrating the ability, albeit limited, for vocal learning.
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 phenotypes and discovered that strain-specific characteristics of each song persisted in the offspring, indicating that these vocalizations are innate. However, a year later work by Arriaga et al. contradicted these results as their study found a motor cortex region active during singing, which projects directly to brainstem motor neurons and is also important for keeping songs stereotyped and on pitch. Vocal control by forebrain motor areas and direct cortical projections to vocal motor neurons are both features of vocal learning. Furthermore, male mice were shown to depend on auditory feedback to maintain some ultrasonic song features, and sub-strains with differences in their songs were able to match each other's pitch when cross-housed under competitive social conditions.
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.
With this conflicting evidence, it remains unclear whether mice are vocal non-learners or limited vocal learners.
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. Although these studies are promising, more research is needed in this area to compare predation rates across vocal learners and non-learners.
Currently, it remains unclear as to which of these hypotheses is the most accurate.
| VLN: vocal nucleus of the lateral nidopallium |
| VA: vocal nucleus of the arcopallium |
Vocal nuclei are found in two separate brain pathways, which will be described in songbirds as most research has been conducted in this group, yet connections are similar in parrots and hummingbirds. Projections of the anterior vocal pathway in the hummingbird remain unclear and so are not listed in the table above.
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 HVC in songbirds. The HVC then projects to the robust nucleus of the arcopallium (RA). The RA connects to the midbrain vocal center DM (dorsal medial nucleus of the midbrain) and the brainstem (nXIIts) vocal motor neurons that control the muscles of the syrinx, a direct projection similar to the projection from LMC to the nucleus ambiguus in humans. The HVC is considered the syntax generator while the RA modulates the acoustic structure of syllables. Vocal non-learners do possess the DM and twelfth motor neurons (nXIIts), but lack the connections to the arcopallium. As a result, they can produce vocalizations, but not learned vocalizations.
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. 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.
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 songbirds, the posterior pathway communicates with the anterior pathway via projections from the HVC to Area X; the anterior pathway sends output to the posterior pathway via connections from LMAN to RA and medial MAN (MMAN) to HVC. Parrots, on the other hand, have projections from the ventral part of the AAC (AACv), the parallel of the songbird RA, to the NAOc, parallel of the songbird MAN, and the oval nucleus of the mesopallium (MO). The anterior pathway in parrots connects to the posterior pathway via NAOc projections to the NLC, parallel of the songbird HVC, and AAC. Thus, parrots do not send projections to the striatum nucleus of the anterior pathway from their posterior pathway as do songbirds. Another crucial difference is the location of the posterior vocal nuclei among species. Posterior nuclei are located in auditory regions for songbirds, laterally adjacent to auditory regions in hummingbirds, and are physically separate from auditory regions in parrots. Axons must therefore take different routes to connect nuclei in different vocal learning species. Exactly how these connectivity differences affect song production and/or vocal learning ability remains unclear.
An auditory pathway that is used for auditory learning brings auditory information into the vocal pathway, but the auditory pathway is not unique to vocal learners. Ear hair cells project to cochlear ganglia neurons to auditory pontine nuclei to midbrain and thalamus nuclei and to primary and secondary pallial areas. A descending auditory feedback pathway exists projecting from the dorsal nidopallium to the intermediate arcopallium to shell regions around the thalamus and midbrain auditory nuclei. Remaining unclear is the source of auditory input into the vocal pathways described above. It is hypothesized that songs are processed in these areas in a hierarchical manner, with the primary pallial area responsible for acoustic features (field L2), the secondary pallial area (fields L1 and L3 as well as the caudal medial nidopallium or NCM) determining sequencing and discrimination, and the highest station, the caudal mesopallium (CM), modulating fine discrimination of sounds. Secondary pallial areas including the NCM and CM are also thought to be involved in auditory memory formation of songs used for vocal learning, but more evidence is needed to substantiate this hypothesis.
In the male zebra finch, vocal learning begins with a period of sensory acquisition or auditory learning where juveniles are exposed to the song of an adult male "tutor" at about posthatch day 30 to 60. During this stage, juveniles listen and memorize the song pattern of their tutor and produce subsong, characterized by the production of highly variable syllables and syllable sequences. Subsong is thought to be analogous to babbling in human infants. Subsequently during the sensorimotor learning phase at posthatch day 35 to 90, juveniles practice the motor commands required for song production and use auditory feedback to alter vocalizations to match the song template. Songs during this period are plastic as specific syllables begin to emerge but are frequently in the wrong sequence, errors that are similar to phonological mistakes made by young children when learning a language. As the bird ages, its song becomes more stereotyped until at posthatch day 120 the song syllables and sequence are crystallized or fixed. At this point, the zebra finch can no longer learn new songs and thus sings this single song for the duration of its life.
The neural mechanisms behind the closing of the critical period remain unclear, but early deprivation of juveniles from their adult tutors has been shown to extend the critical period of song acquisition "Synapse selection" theories hypothesize that synaptic plasticity during the critical period is gradually reduced as dendritic spines are pruned through activity-dependent synaptic rearrangement The pruning of dendritic spines in the LMAN song nucleus was delayed in isolated zebra finches with extended critical periods, suggesting that this form of synaptic reorganization may be important in closing the critical period. However, other studies have shown that birds reared normally as well as isolated juveniles have similar levels of dendritic pruning despite an extended critical period in the latter group, demonstrating that this theory does not completely explain critical period modulation.
Previous research has suggested that the length of the critical period may be linked to differential gene expression within song nuclei, thought to be caused by neurotransmitter binding of receptors during neural activation. One key area is the LMAN song nucleus, part of the specialized cortical-basal-ganglia-thalamo-cortical loop in the anterior forebrain pathway, which is essential for vocal plasticity. While inducing deafness in songbirds usually disrupts the sensory phase of learning and leads to production of highly abnormal song structures, lesioning of LMAN in zebra finches prevents this song deterioration, leading to the earlier development of stable song. One of the neurotransmitter receptors shown to affect LMAN is the NMDA receptor (NMDAR), which is required for learning and activity-dependent gene regulation in the post-synaptic neuron. Infusions of the NMDAR antagonist APV (R-2-amino-5-phosphonopentanoate) into the LMAN song nucleus disrupts the critical period in the zebra finch. NMDAR density and mRNA levels of the NR1 subunit also decrease in LMAN during early song development. When the song becomes crystallized, expression of the NR2B subunit decreases in LMAN and NMDAR-mediated synaptic currents shorten. It has been hypothesized that LMAN actively maintains RA microcircuitry in a state permissive for song plasticity and in a process of normal development it regulates HVC-RA synapses.
Orthologues of FOXP2 are found in a number of vertebrates including mice and songbirds, and have been implicated in modulating Neuroplasticity of neural circuits. In fact, although mammals and birds are very distant relatives and diverged more than 300 million years ago, the FOXP2 gene in zebra finches and mice differs at only five amino acid positions, and differs between zebra finches and humans at only eight amino acid positions. In addition, researchers have found that patterns of expression of FOXP1 and FOXP2 are amazingly similar in the human fetal brain and the songbird.
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 striatum during the critical period of song plasticity in songbirds. In humans, FOXP2 is highly expressed in the basal ganglia, frontal cortex, and insular cortex, all thought to be important nodes in the human vocal pathway. Thus, mutations in the FOXP2 gene are proposed to have detrimental effects on human speech and language, such as grammar, language processing, and impaired movement of the mouth, lips, and tongue, as well as potential detrimental effects on song learning in songbirds. Indeed, FOXP2 was the first gene to be implicated in the cognition of speech and language in a family of individuals with a severe speech and language disorder.
Additionally, it has been suggested that due to the overlap of FOXP1 and FOXP2 expression in songbirds and humans, mutations in FOXP1 may also result in speech and language abnormalities seen in individuals with mutations in FOXP2.
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.
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