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Vocal learning has evolved in only a few groups of mammals and birds. The key neuroanatomical and behavioural links bridging vocal learners and non-learners are still unknown. Here we show that a non-vocal-learning suboscine, the eastern phoebe, expresses neural and behavioural substrates that are associated with vocal learning in closely related oscine songbirds. In phoebes, a specialized forebrain region in the intermediate arcopallium seems homologous to the oscine song nucleus RA (robust nucleus of arcopallium) by its neural connections, expression of glutamate receptors and singing-dependent immediate-early gene expression. Lesion of this RA-like region induces subtle but consistent song changes. Moreover, the unlearned phoebe song unexpectedly develops through a protracted ontogeny. These features provide the first evidence of forebrain vocal-motor control in suboscines, which has not been encountered in other avian non-vocal-learners, and offer a potential configuration of brain and behaviour from which vocal learning might have evolved.

New neurons are added to the high vocal center (HVC) of adult males in seasonally breeding songbirds such as the canary (Serinus canaria) that learns new songs in adulthood, and the song sparrow (Melospiza melodia) that does not. In both cases, the new neurons numerically replace others that have died, resulting in a seasonal fluctuation in HVC volume and neuron number. Peaks in neuronal replacement in both species occur in the fall when breeding is over and song is variable. New neurons are added, too, to the HVC of zebra finches (Taeniopygia guttata) that do not learn new songs in adulthood and whose song remains stereotyped throughout the year. Here, we show that, in contrast to the observations in seasonal songbirds, neurons added to the zebra finch HVC are not part of a replacement process. Rather, they lead to a doubling in the number of neurons that project from HVC to the robust nucleus of the arcopallium (RA). As this happens, HVC volume remains constant and the packing density of its neurons increases. The HVC-RA neurons are part of a descending pathway that carries the pattern of learned song; some HVC-RA neurons are also responsive to song playback. The addition of HVC-RA neurons happens in zebra finches housed singly, but becomes more acute if the birds are housed communally. We speculate that new neurons added to the adult HVC may help with the production or perception of learned song, or both.

We do not know how vocal learning came to be, but it is such a salient trait in human evolution that many have tried to imagine it. In primates this is difficult because we are the only species known to possess this skill. Songbirds provide a richer and independent set of data. I use comparative data and ask broad questions: How does vocal learning emerge during ontogeny? In what contexts? What are its benefits? How did it evolve from unlearned vocal signals? How was brain anatomy altered to enable vocal learning? What is the relation of vocal learning to adult neurogenesis? No one has described yet a circuit or set of circuits that can master vocal learning, but this knowledge may soon be within reach. Moreover, as we uncover how birds encode their learned song, we may also come closer to understanding how we encode our thoughts., (Copyright © 2010. Published by Elsevier Inc.)

Vocal learning has evolved in only a few groups of mammals and birds. The developmental and evolutionary origins of vocal learning remain unclear. The imitation of a memorized sound is a clear example of vocal learning, but is that when vocal learning starts? Here we use an ontogenetic approach to examine how vocal learning emerges in a songbird, the chipping sparrow. The first vocalizations of songbirds, food begging calls, were thought to be innate, and vocal learning emerges later during subsong, a behavior reminiscent of infant babbling. Here we report that the food begging calls of male sparrows show several characteristics associated with learned song: male begging calls are highly variable between individuals and are altered by deafening; the production of food begging calls induces c-fos expression in a forebrain motor nucleus, RA, that is involved with the production of learned song. Electrolytic lesions of RA significantly reduce the variability of male calls. The male begging calls are subsequently incorporated into subsong, which in turn transitions into recognizable attempts at vocal imitation. Females do not sing and their begging calls are not affected by deafening or RA lesion. Our results suggest that, in chipping sparrows, intact hearing can influence the quality of male begging calls, auditory-sensitive vocal variability during food begging calls is the first step in a modification of vocal output that eventually culminates with vocal imitation.

Here we show how a migratory songbird, the chipping sparrow (Spizella passerina), achieves prompt and precise vocal imitation. Juvenile chipping sparrow males develop five to seven potential precursor songs; the normal development of these songs requires intact hearing but not imitation from external models. The potential precursor songs conform with general species-typical song parameters but differ from the song of wild, adult territorial males. As chipping sparrow males return from migration to start their first breeding season, they settle close to an older adult. The young male then stops producing all but one of its precursor songs, retaining the one that most resembles that of its neighbor. This single song then becomes more variable and, in a matter of days, is altered to closely match the neighbor's song. This elegant solution ensures species specificity and promptness of imitation.

Zebra finch males learn their song by imitation, a process influenced by social variables. The neural pathways for acquisition and production of learned song are known, but the cellular and molecular underpinnings are not. Here we describe a novel gene named "FnTm2" ("Phantom 2") that is predicted to encode a small protein (220 aa) with a single fibronectin type III domain and a single transmembrane domain. This gene shows great variability in its expression in song system neurons of the anterior forebrain pathway (AFP), a circuit that influences song discrimination and is necessary for normal song acquisition. AFP nuclei that express FnTm2 include the nucleus HVC (its Area X-projecting neurons), Area X, and LMAN (core and shell). FnTm2 expression does not correlate with singing behavior like the immediate early gene ZENK. It is expressed variably during sleeping hours and is not dependent on an intact song circuit. FnTm2's expression is sensitive to hearing, because in deafened birds its expression is substantially reduced in the core of LMAN. Furthermore, a comparison of FnTm2 expression between mice and zebra finches revealed a conserved pattern of expression in the "limbic system." We suggest that FnTm2 may be sensitive to affective and/or attentional states and thus may provide insights on how social variables influence the production and discrimination of learned vocalizations., ((c) 2007 Wiley-Liss, Inc.)

Socially reared zebra finch males imitate a song they hear during posthatching days 30-65; during this time, many new neurons are added to the high vocal center (HVC), a forebrain nucleus necessary for the production of learned song. New neuron addition drops sharply after day 65, and no new songs are imitated. In contrast, male zebra finches reared in isolation from other males have more variable songs at day 65 and thereafter can still imitate new sounds (Eales, 1985). We show that, in isolate birds, a greater number of new neurons continues to be added to HVC during the next 85 d, and this number correlates with syllable variability. We suggest that new neuron addition and turnover facilitate song change and that this effect lingers when an expected learning event is delayed.

Male zebra finches reared in family groups were housed initially in small indoors cages with three other companions. At 4-5 months of age these birds were treated with [(3)H]-thymidine and then placed in large outdoors aviaries by themselves or with other zebra finches. Counts of new neurons were made 40, 60 and 150 days after the change in housing. Recruitment of new neurons in nidopallium caudale (NC) was higher than in the hippocampal complex (HC); but in both brain regions it was higher in communally housed birds than in birds housed singly, suggesting that the complexity of the social setting affects new neuron survival. In addition, the new neurons lived longer in rostral NC than in its caudal counterpart, and neuronal turnover was faster and more significant in NC than in HC. Albeit indirect, this may be the first suggestion that different parts of the brain upgrade memories at different time intervals, yielding an anatomical representation of time.

The duration of songs and the intervals between these songs are more variable when wild, adult, free-ranging chipping sparrows sing at dawn than when they sing during the day. The more variable delivery is used to interact with males, and the stereotyped delivery is used to attract females. In captive birds, however, the variability observed at dawn persists during the day. We quantified the expression of an immediate early gene, ZENK, in wild and captive birds and found that the level of song-associated ZENK expression in two song nuclei, Area X and lMAN, was positively related to variability in song duration and intersong interval and could be dissociated from the social context in which the song occurred. Thus, a combination of field and laboratory approaches helped us identify nuclei, context, and behavioral features associated with a change in gene expression thought to be a marker of behavioral variability.

Canary song is hierarchically structured: Short stereotyped syllables are repeated to form phrases, which in turn are arranged to form songs. This structure occurs even in the songs of young isolates, which suggests that innate rules govern canary song development. However, juveniles that had never heard normal song imitated abnormal synthetic songs with great accuracy, even when the tutor songs lacked phrasing. As the birds matured, imitated songs were reprogrammed to form typical canary phrasing. Thus, imitation and innate song constraints are separate processes that can be segregated in time: freedom in youth, rules in adulthood.

Songbirds represent an excellent model system for understanding the neural mechanisms underlying learning.

Does the ontogeny of vocal imitation follow a set program that, given a target sound, unfolds in a predictable manner, or is it more like problem solving, with many possible solutions? We report that juvenile male zebra finches, Taeniopygia guttata, can master their imitation of the same song in various ways; these developmental trajectories are sensitive to the social setting in which the bird grows up. A variety of vocal developmental trajectories have also been described in infants. Are these many ways to learn unique to the vocal domain or a hallmark of advanced brain function?

Vocal learning in songbirds and humans is a complex learned skill with sensory, motor, and social aspects. It culminates in the imitation of sounds produced by other, usually older individuals. Song learning and language learning may differ in their cognitive content, but both require coordination of auditory feedback and fine motor control, which may be supported by similar brain structures. Vocal learning in birds as in humans requires the use of forebrain networks; in songbirds these networks are thought to be related, in part, to the frontal association cortex-basal ganglia loops that mature in humans at adolescence.

Neurons are constantly added to the telencephalon of songbirds. In the high vocal center (HVC), where this has been studied, new neurons replace older ones that died. Peaks in replacement are seasonal and affect some neuronal classes but not others. Peaks in replacement coincide with peaks in information acquisition. The new neurons are produced by division of cells in the wall of the lateral ventricle. Where studied closely, the neuronal stem cells proved to be radial glia. Life expectancy of the new neurons ranges from weeks to months. New neuron survival is regulated by vacancies, hormones, and activity. The immediate agent of new neuron survival is, in some cases, brain-derived neurotrophic factor (BDNF). The effect of BDNF is maximal 14-20 days after the cells are born, when they are establishing their connections. These observations are now being extended to other vertebrates and may apply, to varying degrees, to all of them. The function of neuronal replacement in healthy adult brain remains unclear. If synaptic number and efficacy sufficed as mechanisms for long-term memory storage and could be adjusted again and again to incorporate new memories, then neuronal replacement would seem unnecessary. Since it occurs, it seems reasonable to suppose that replacement serves to maintain learning potential in a way that could not be done just by synaptic change. Long-term memories may be encoded by long-term changes in gene expression akin to a last step in cell differentiation. If so, neuronal replacement may be the adult brain's way of striking a balance between limited memory space and the need to acquire new memories. The testing of this hypothesis remains in the future. This chapter tells how neuronal replacement was discovered in the adult songbird brain.

New neurons are constantly added to the high vocal center (HVC) of adult male canaries, Serinus canaria. Singing and testosterone (T) are known to promote this addition, but it is not known whether either variable can act on its own and what is their effect when acting together. We studied this question by castrating adult male canaries in late summer and quantifying their song in early fall. Intact birds served as controls. A 5 d systemic treatment of two daily injections of the cell birth marker 3H-thymidine started 10 d after surgery. Twenty days after the first 3H-thymidine injection and for a period of 1 month, we quantified the singing of all birds, which were then killed. Amount of singing, syllable diversity, and song stability were similar in intacts and castrates. When castrates and intacts that sang comparable amounts were compared, the number of 3H-labeled HVC neurons was 2.6 times higher in intacts than in castrates. In castrates with plasma T levels that were undetectable, the mean amount of singing was positively related to the number of new neurons. We suggest that singing and gonadal factors promote, separately, the recruitment of new neurons and that when they exert this effect together they do so in an additive manner.

It is not known whether the addition of new neurons to the high vocal center (HVC) of juvenile zebra finches permits vocal learning or is the consequence of it. To tease apart these two, we performed surgery on 26-d-old juveniles. The operations were removal of both cochleae and unilateral or bilateral denervation of the syrinx. Ability to imitate a tutor song was little affected by unilateral syringeal denervation but was severely hindered by bilateral denervation or deafening. Recruitment of new HVC neurons was studied by injecting BrdU, a cell birth marker, on post-hatching days 61-65 and killing the animals 30 d later. Deafening or bilateral denervation did not alter the number of BrdU-labeled neurons in HVC, but unilateral denervation nearly doubled this number in the intact side. This doubling was transient, was blocked by deafening, and was not seen in birds that received BrdU injections earlier or later in vocal ontogeny. The adult number of HVC neurons was not affected by any of our surgical procedures. Apparently experience does not affect the total number of neurons in adult HVC, but some kinds of experience can, during narrowly defined times, influence the recruitment of new HVC neurons.