although the vocalizations of most animal 
 species constitute their innate behavior , some animal groups , such as mammals ( humans , 
 cetaceans , bats , elephants , and pinnipeds ) and birds ( oscine songbirds , parrots , and 
 hummingbirds ) develop a complex vocal pattern through vocal learning [ 23 , 24 ] . the songbird is an 
 attractive animal model for understanding the mechanisms underlying vocal learning because 
 non - human primates and rodents have a limited ability to modify their vocalization .
there are approximately 3,500 songbird species all 
 over the world , and their birdsong shows a readily quantifiable species - specific variation , 
 ideal to investigate the developmental changes of acoustic and sequential song structure 
 ( fig .
the zebra finch is known as a closed - ended learner , 
 meaning that once a stable species - specific song pattern  motif  is developed , the 
 song structure remains unchanged throughout life [ 8 , 22 , 74 ] .
this stereotypy of crystallized song enables precise 
 quantification of the similarities and differences in vocal development and song 
 patterns between experiments , allowing for examination of genetic and epigenetic 
 factors that contribute to the acquisition and maintenance of complex vocal patterns . 

( b , c ) examples of adult song patterns of two bengalese finches ( b ) and two java 
 sparrows ( c ) . )
. some species of birds such as the zebra finch and canary are easily bred under 
 laboratory conditions .
these features mean that 
 studies of songbirds can provide excellent insights into the evolution , function , 
 development , and mechanisms of vocal learning .
here we review vocal learning in songbirds , 
 with particular focus on auditory input as a developmental epigenetic factor of vocal 
 development .
first , we highlight the parallels between human speech and birdsong and 
 introduce the neural mechanisms involved in vocal production and learning .
we then provide 
 an overview of the contribution of auditory input during vocal development and 
 maintenance .
the zebra finch is known as a closed - ended learner , 
 meaning that once a stable species - specific song pattern  motif 
is developed , the 
 song structure remains unchanged throughout life [ 8 , 22 , 74 ] .
this stereotypy of crystallized song enables precise 
 quantification of the similarities and differences in vocal development and song 
 patterns between experiments , allowing for examination of genetic and epigenetic 
 factors that contribute to the acquisition and maintenance of complex vocal patterns . 

( b , c ) examples of adult song patterns of two bengalese finches ( b ) and two java 
 sparrows ( c ) .
although birds and mammals diverged from a common ancestor approximately three hundred 
 million years ago , birdsong broadly possesses 
 three behavioral traits similar to that of human speech .
first , sensory and sensorimotor learning is crucial for the development of both the 
 birdsong and human speech .
the sensorimotor learning 
 follows , and animals start vocalizing , gradually matching their vocalization to the 
 memorized template ( fig .
at the early stage 
 of sensorimotor learning , fledgling juvenile songbirds produce unstructured sounds .
juveniles compare these sounds with 
 the memorized template and achieve vocal imitation through a process of trial - and - error 
 vocalizations using auditory feedback ( fig .
thus , this reliance on tutor experience and auditory feedback means that birds raised in 
 complete social and acoustic isolation will develop abnormal song ( figs .
2.examples of song development and syllable scatter plots [ duration versus mean 
 frequency modulation ( fm ) ] in an intact , a socially isolated , an early - deafened , and 
 an adult - deafened bird .
( a , b ) colored portions ( blue and green ) highlight stable song 
 motifs . the intact and socially isolated birds exhibited song stability around dph 
 110 .
the crystallized song pattern of the socially isolated bird is similar to that of 
 the intact ( normal ) bird , except for a prolonged and variable syllable ( green 
 bracket ) .
[ 33 , 40 ] . examples of song development and syllable scatter plots [ duration versus mean 
 frequency modulation ( fm ) ] in an intact , a socially isolated , an early - deafened , and 
 an adult - deafened bird .
( a , b ) colored portions ( blue and green ) highlight stable song 
 motifs .
the crystallized song pattern of the socially isolated bird is similar to that of 
 the intact ( normal ) bird , except for a prolonged and variable syllable ( green 
 bracket ) .
second , learned vocalizations consist of a complex motor sequence , quantifiable at the 
 phonological and syntactical levels in both songbirds and humans . although the human speech 
 and birdsong share common features and their vocal patterns are defined as ordered strings 
 of sounds , they are different in a critical character .
human speech has the flexible 
 capacity to convey meaning associated with distinct sound ( phonology ) and word ( syntax ) 
 order , while songbirds use their songs for territorial advertisement and for mate 
 attraction , just conveying the information about the individual identity of the bird to 
 receivers .
third , vocal learning occurs within a critical period , usually at the early developmental 
 stage before adulthood .
both songbirds and humans are unable to learn vocalization equally 
 well throughout their life .
although it is critical that humans and birds are provided with 
 appropriate auditory and social conditions during the critical period to achieve vocal 
 learning , they are different with regard to the following point : humans are able to learn 
 new words and languages throughout their life .
some species of songbirds categorized as 
 closed - ended vocal learners , e.g. , the zebra finch and bengalese finch , which are commonly 
 used in research , are unable to learn new songs at the adult stage , while others categorized 
 as open - ended vocal learners , e.g. , the canary , have the ability to imitate new sounds to 
 some extent as adults .
this neurogenesis allows for replacement of 
 old neurons with new ones and results in a seasonal fluctuation in the neuron number that 
 correlates with the capacity of song plasticity . as outlined above , birdsong shares numerous behavioral traits with human speech . in 
 contrast , with regard to their vocal organs and respiratory systems , there are subtle 
 differences in the functional morphology . birds 
 generate sound using an organ named the syrinx , which is part of the respiratory system , 
 whereas humans generate sound using the larynx , which contains the vocal folds .
however , the 
 basic mechanism underlying sound generation in birds shows strong analogies to the human 
 source - filter mechanism . in both the cases
, vocalizations are generated by airflow - induced 
 oscillation of the vocal folds in the human larynx and elements in the wall of the syrinx , 
 followed by filtering and tuning of sound by the upper airway .
to generate vocal sounds , the 
 components of the peripheral vocal system , such as respiration organs , vocal organs and 
 vocal tract structures require to be precisely coordinated through the neural control of a 
 number of different muscles .
the following text 
 elaborates on the neural substrates involved in vocal development and how they contribute to 
 this process .
in vertebrates such as mammals and birds , the central nervous system is divided into five 
 basic regions : the hindbrain , the midbrain , the thalamus , the cerebellum , and the cerebrum . 
 across vertebrate species , there is similar structural organization throughout most of these 
 five brain regions , except the cerebrum . in birds ,
the cerebrum is organized into large cell 
 clusters ; on the other hand , in mammals , the cerebrum is divided into subcortical nuclei , 
 such as the basal ganglia , and the cerebral cortex , which consists of six main layers . 

however , recent studies have indicated that the avian striatal and pallidal domains are well 
 conserved in relation to their counterparts in the cerebrum of mammals ( fig . 3fig .
( modified from horita and wada , 2011 , and 
 pfenning et al . , 2014 ) . 

( a , b ) upper drawings illustrate a brain section from a male zebra finch ( a ) and a 
 human ( b ) .
solid black arrows denote connections within the posterior vocal motor 
 circuit ( from hvc to ra to brainstem motor nuclei ) .
white arrows denote connections 
 within the basal ganglia  forebrain circuit . dashed black arrows denote connections 
 between the two circuits .
red arrows show the direct connections found only in vocal 
 learners , which project from vocal motor cortex regions to brain stem vocal motor 
 neurons .
( c , d ) lower drawings illustrate comparative and simplified connectivity of 
 anterior and posterior vocal circuits in a songbird ( c ) and a human ( d ) .
dlm : dorsal 
 lateral medial nucleus of the thalamus , dm : dorsal medial nucleus of the midbrain , 
 hvc : a vocal nucleus ( no acronym ) , lman : lateral man , man : magnocellular nucleus of 
 the anterior nidopallium , nxiits : twelfth nucleus , tracheosyringeal part , ra : robust 
 nucleus of the arcopallium , ram / pam : nucleus retroambiguus / parambiguus . ) [ 25 , 26 ] .
both humans and songbirds have specific brain regions involved in vocal 
 learning and production .
humans have a specialized circuit that forms a network of brain 
 areas ( including broca s area and temporal areas ) devoted to speech perception and 
 production .
syntax - related networks are reported to exist in the opercular / triangular parts 
 of left inferior frontal gyrus and the left lateral premotor cortex .
in addition , the basal ganglia are considered to be involved in 
 prosodic modulation and language acquisition [ 1 , 12 ] .
several studies have indicated that compared with 
 the native language the basal ganglia showed different activity during speech production and 
 syntactic processing of a second language [ 11 , 31 ] .
the identity and function of the neural networks contributing to vocalization 
 have been particularly well studied in songbirds through a variety of neurophysiological and 
 molecular biology methods .
( modified from horita and wada , 2011 , and 
 pfenning et al . , 2014 ) . 

( a , b ) upper drawings illustrate a brain section from a male zebra finch ( a ) and a 
 human ( b ) .
solid black arrows denote connections within the posterior vocal motor 
 circuit ( from hvc to ra to brainstem motor nuclei ) .
red arrows show the direct connections found only in vocal 
 learners , which project from vocal motor cortex regions to brain stem vocal motor 
 neurons .
( c , d ) lower drawings illustrate comparative and simplified connectivity of 
 anterior and posterior vocal circuits in a songbird ( c ) and a human ( d ) .
dlm : dorsal 
 lateral medial nucleus of the thalamus , dm : dorsal medial nucleus of the midbrain , 
 hvc : a vocal nucleus ( no acronym ) , lman : lateral man , man : magnocellular nucleus of 
 the anterior nidopallium , nxiits : twelfth nucleus , tracheosyringeal part , ra : robust 
 nucleus of the arcopallium , ram / pam : nucleus retroambiguus / parambiguus . the brain areas associated with song learning and production , the song nuclei , are 
 organized into two major circuits : the posterior vocal motor circuit and the anterior basal 
 ganglia  forebrain circuit ( figs . 3a and c ) .
the 
 vocal motor circuit is involved in the generation of vocal patterns through a hierarchical 
 process of regulation of syllable sequence and acoustic features [ 17 , 73 ] .
furthermore , the premotor 
 hvc nucleus is the only song system nucleus that receives direct projections from auditory 
 areas , and it has a crucial role in encoding the 
 experience of the tutor song .
mirror neurons 
 have been reported in hvc of some songbirds [ 13 , 
 53 ] such as the swamp sparrow and bengalese 
 finches .
auditory mirroring in analogy to the 
 motor  visual ones found in human and nonhuman primate cortical motor areas .
this form of 
 sensorimotor correspondence is considered to be important for vocal learning and 
 communication .
in contrast , the basal 
 ganglia  forebrain circuit in both humans and songbirds is involved in motor and cognitive 
 processes , such as control of vocal movements and reinforcement - based learning . in 
 songbirds , this circuit plays a crucial role in song learning by supporting vocal 
 exploration with direct premotor bias in response to the vocal experience [ 3 , 6 , 27 , 61 ] , and it 
 also maintains learned vocalizations using auditory feedback .
variability in the sequence 
 and structure of syllables is reduced by the presence of a female .
physiological studies have indicated that this context - dependent 
 change in song variability is accompanied by changes in singing - related neural activity 
 within cortical nucleus lman [ 27 , 60 ] .
a recent study also revealed that the basal ganglia 
 nucleus area x is essential for singing - related patterned burst firing of lman , which is 
 critical for vocal plasticity and adjustment in response to auditory feedback .
together , these two premotor circuits are believed 
 to produce vocalizations at different stages of song development .
the poorly structured 
 subsong , akin to human babbling , is driven primarily by the basal ganglia  forebrain circuit , 
 whereas the adult song is highly stereotyped and is driven primarily by the motor circuit . 
 transferring control of song from the basal ganglia 
forebrain circuit to the motor circuit 
 is crucial for regulating vocal plasticity and stabilization .
human speech and birdsong result from the development of specialized brain regions for 
 vocal learning and production , which develop through interaction between genetic and 
 environmental factors .
overcoming this problem requires an appropriate model system whose 
 genomic information has been well understood and in which genetic manipulation can be 
 performed .
for example , foxp2 , a forkhead box family gene that encodes a 
 transcription factor , has been reported as the gene underlying a human developmental 
 language impairment caused by structural abnormalities in the striatum , cerebellum , and 
 cortex [ 35 , 69 ] .
similarly , in songbirds , foxp2 is expressed strongly in the 
 striatum and is regulated during vocal development [ 15 , 66 ] .
knockdown of 
 foxp2 in the songbird striatum impairs song learning , decreases spine 
 density of striatal spiny neurons , and disrupts the control of vocal variability by 
 interfering with dopamine - dependent modulation [ 16 , 
 62 ] .
other genes relevant to speech and other human 
 language disorders have been reported to be differentially expressed in the song nuclei of 
 songbirds , and investigation and manipulation of 
 these genes has become possible following the sequencing of the zebra finch genome   and through use of transgenesis and viral 
 transfection [ 2 , 16 , 43 ] .
in addition , targeting of viral 
 vectors to specific brain regions using microinjections can be used to regulate gene 
 expression with temporal and spatial precision in order to analyze the function of genes , 
 cells , and circuits [ 57 , 58 , 68 ] .
in addition to these genetic contributors , developmental factors that influence 
 epigenetics , such as social interaction   and 
 nutrition , are also important in the development 
 of vocalization and the brain regions that support it .
dysfunction of motor and auditory 
 ability causes speech disorders , such as aphasia and stuttering .
studies of vocal deficits by lesions to song 
 nuclei provide us with an animal model of aphasia .
for instance , an adult zebra finch 
 becomes unable to produce a learned vocal pattern after hvc lesions [ 4 , 63 , 67 ] .
stuttering is the most common disorder of speech motor control in 
 young children who are developing speech .
twin studies have 
 reported substantial genetic and epigenetic effects on stuttering [ 10 , 55 ] .
however , the 
 neurobiological basis of this disorder is poorly understood despite recent progress in 
 uncovering its genetic roots . from a comparative point of view
, song syllable repetitions of 
 the zebra finch resemble part - word repetitions , a common feature of stuttering .
song syllable repetitions can be induced by delays 
 or disruptions in auditory feedback during vocalization [ 19 , 36 ] , similar to those that can occur in 
 humans .
furthermore , auditory input is crucial 
 for the acquisition of birdsong and human speech and can influence epigenetic factors 
 contributing to sensorimotor learning [ 33 , 59 ] .
audition provides important information for vocal learning , both for learning templates and 
 for evaluation of one s own vocal output .
auditory feedback also plays an important role in 
 maintaining stable vocal output in adulthood [ 19 , 
 36 , 38 , 
 46 ] .
when songbirds are deprived of auditory input before the sensory learning phase of song , 
 they do not develop normal songs ( fig .
2c ) , similar to individuals with hearing loss that have 
 difficulty developing normal speech patterns . however , audition - deprived songbirds can still 
 develop a certain degree of species - specific song [ 41 , 54 ] and crystallize vocal patterns , 
 though they are noisy and amorphous ( fig .
developmental gene 
 expression is found to be conserved in an age - dependent manner even in deafened birds , indicating audition - independent robustness of gene 
 expression dynamics during vocal development in the song system .
although auditory 
 information is crucial for song development , auditory input is not the main driver of 
 developmental gene expression dynamics in motor circuit nuclei . in adult humans and songbirds , disruption of auditory feedback
2d ) [ 19 , 46 , 71 ] , and the rate of deterioration depends on age
. when deprived of auditory feedback , deterioration of 
 vocal patterns is much more severe at a younger age , and deterioration takes longer at an 
 older age .
delays or disruptions in auditory feedback during vocalization result in 
 stuttering , deletions , and distortion of syllables [ 19 , 36 ] .
furthermore , birds exhibit the 
 capacity to adjust pitch according to perceived errors in vocal production , and the speed and extent of vocal error correction 
 decreases markedly with age . the vocal 
 variability necessary for audition - dependent song plasticity
is generated by the basal 
 ganglia  forebrain circuit [ 3 , 27 , 49 ] .
however , expression of 
 the molecular markers of neural activity - dependent gene induction [ dual specificity 
 phosphatase 1 ( dusp1 ) , c - fos , and arc ] is 
 similar throughout development in the nuclei of the basal ganglia  forebrain circuit .
this suggests that molecular signaling cascades are 
 consistently regulated regardless of age in the basal ganglia 
therefore , during vocal learning , inherited genetic programs 
 contribute to vocal development and auditory - dependent vocal plasticity , which are directly 
 or indirectly regulated by age or activation of vocalization ( motor)-dependent epigenetic 
 factors .
it is a complex form of 
 sensorimotor learning that requires coordination of sensory input and motor output to guide 
 one s own vocalization .
hearing impairment and developmental disabilities lead to deficits in acquired vocal 
 patterns and maintenance during vocal development , including speech disorders , such as 
 aphasias , and stuttering .
songbirds that have had auditory input disrupted are useful animal 
 models for understanding how hearing impairment affects the development of brain regions for 
 vocal learning and production ( fig .
4.a schematic highlighting the use of songbirds as a research model for disorders of 
 vocal development and communication . ) . a schematic highlighting the use of songbirds as a research model for disorders of 
 vocal development and communication . as we have described , audition - independent robustness of gene expression is present in the 
 songbird motor circuit , which indicates that volitional vocalization itself may have a 
 crucial influence on epigenetic factors that activate the genetic programs necessary for 
 regulating vocal plasticity and development of vocal patterns .
in fact , a large set of 
 neural plasticity - related genes are regulated by singing in song nuclei [ 37 , 51 , 70 ] . although variability in the accuracy of 
 syllable / word structures in human children and adults with hearing impairments has been 
 observed ,
language outcomes may 
 vary by the overall hearing level , age of onset of hearing loss , and therapeutic 
 interventions , such as hearing aids or cochlear implants .
in addition , vocal development may 
 rely not only on how good one s hearing is but also how much vocalization they produce .
this 
 suggests that interventions , such as hearing aids or cochlear implant , performed at an early 
 stage of word production may have a more positive effect on language development in children 
 with congenital hearing impairment .
studies on birdsong using behavioral manipulation and genetic and neurophysiological tools 
 have shed light on the specialized neural networks that underlie vocal learning .
further 
 research is needed to understand how auditory input , motor activity , and aging affect the 
 development of brain areas involved in vocal learning and production .
 like humans , songbirds are one of the few animal groups that learn vocalization . 
 vocal 
 learning requires coordination of auditory input and vocal output using auditory feedback 
 to guide one s own vocalizations during a specific developmental stage known as the 
 critical period . 
 songbirds are good animal models for understand the neural basis of vocal 
 learning , a complex form of imitation , because they have many parallels to humans with 
 regard to the features of vocal behavior and neural circuits dedicated to vocal learning . 
 in this review 
 , we will summarize the behavioral , neural , and genetic traits of birdsong . 
 
 we will also discuss how studies of birdsong can help us understand how the development of 
 neural circuits for vocal learning and production is driven by sensory input ( auditory 
 information ) and motor output ( vocalization ) . 
Introduction
Human Speech and Birdsong
Neural Substrates of Vocal Learning and Production
Audition for Vocal Learning and Maintenance
Conclusions and Future Directions