Rudimentary substrates for vocal learning in a suboscine.

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.

The zebra finch paradox: song is little changed, but number of neurons doubles.

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.

The origins of vocal learning: New sounds, new circuits, new cells.

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.

Variable food begging calls are harbingers of vocal learning.

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 relationship between nature of social change, age, and position of new neurons and their survival in adult zebra finch brain.

Some kinds of neurons are spontaneously recruited in the intact, healthy adult brain, but the variables that affect their survival are not always clear. We show that in caudal nidopallium of adult male zebra finches, the rostrocaudal position of newly recruited neurons, their age (1 vs 3 months), and the nature of social change (complex vs simple) after the neurons were born affect their survival. Greater social complexity promoted the survival of younger new neurons, and the demise of older ones; a less marked social change promoted the survival of older new neurons.

A learning program that ensures prompt and versatile 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.

FnTm2, a novel brain-specific transcript, is dynamically expressed in the song learning circuit of the zebra finch.

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.

Neuronal recruitment in adult zebra finch brain during a reproductive cycle.

Previous studies suggest that adult neurogenesis and neuronal replacement are related to the acquisition of new information. The present study supports this hypothesis by showing that there is an increase in new neuron recruitment in brains of adult male and female zebra finches that coincides with the need to memorize vocalizations of nestlings before they fledge. We counted [(3)H]-Thymidine labeled neurons 40 days after [(3)H]-Thymidine injections.

Genomic resources for songbird research and their use in characterizing gene expression during brain development.

Vocal learning and neuronal replacement have been studied extensively in songbirds, but until recently, few molecular and genomic tools for songbird research existed. Here we describe new molecular/genomic resources developed in our laboratory. We made cDNA libraries from zebra finch (Taeniopygia guttata) brains at different developmental stages.

High levels of new neuron addition persist when the sensitive period for song learning is experimentally prolonged.

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).

Expression profiling of intermingled long-range projection neurons harvested by laser capture microdissection.

Gene expression data are most useful if they can be associated with specific cell types. This is particularly so in an organ such as the brain, where many different cell types lie in close proximity to each other. We used zebra finches (Taeniopygia guttata), fluorescent tracers and laser capture microdissection (LCM) to collect projection neurons and their RNAs from two interspersed populations from the same animal.

Social and spatial changes induce multiple survival regimes for new neurons in two regions of the adult brain: An anatomical representation of time?

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.

Variable rate of singing and variable song duration are associated with high immediate early gene expression in two anterior forebrain song nuclei.

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.

Replaceable neurons and neurodegenerative disease share depressed UCHL1 levels.

Might there be systematic differences in gene expression between neurons that undergo spontaneous replacement in the adult brain and those that do not? We first explored this possibility in the high vocal center (HVC) of male zebra finches by using a combination of neuronal tracers, laser capture microdissection, and RNA profiling. HVC has two kinds of projection neurons, one of which continues to be produced and replaced in adulthood. HVC neurons of the replaceable kind showed a consistent and robust underexpression of the deubiquitination gene ubiquitin carboxyl-terminal hydrolase (UCHL1) that is involved with protein degradation.

Freedom and rules: the acquisition and reprogramming of a bird's learned song.

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.

The neural basis of birdsong.

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

Juvenile zebra finches can use multiple strategies to learn the same song.

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?

The road we travelled: discovery, choreography, and significance of brain replaceable neurons.

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.

Age and experience affect the recruitment of new neurons to the song system of zebra finches during the sensitive period for song learning: ditto for vocal learning in humans?

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.

A conversation with Fernando Nottebohm, PhD. Interviewed by Michael Eisenstein.

During the last 30 years, a number of revolutionary discoveries in the field of neuroscience have come from what was, at first, an unexpected direction: songbird research. Investigations into seasonal and sex-specific differences in birdsong development have led to important revelations about the impact of sex hormones on brain development and the hormonally controlled plasticity of brain structure, as well as the particularly surprising discovery that neurogenesis continues to occur in the adult brain (see Harding, p. 28).

Timing of brain-derived neurotrophic factor exposure affects life expectancy of new neurons.

The high vocal center (HVC) of adult male canaries, Serinus canaria, is necessary for the production of learned song. New neurons are added to HVC every day, where they replace older neurons that have died, but the length of their survival depends on the time of year when they are born. A great number of HVC neurons born in the fall, when adult canaries learn a new song, are still present 8 mo later, when this song is used during the breeding season.

Vocal learning in birds and humans.

Vocal learning is the modification of vocal output by reference to auditory information. It allows for the imitation and improvisation of sounds that otherwise would not occur. The emergence of this skill may have been a primary step in the evolution of human language, but vocal learning is not unique to humans.

Gonads and singing play separate, additive roles in new neuron recruitment in adult canary 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.