Fernando Nottebohm

A procedure for an automated measurement of song similarity

Assessment of vocal imitation requires a widely accepted way of describing and measuring any similarities between the song of a tutor and that of its pupil. Quantifying the similarity between two songs, however, can be difficult and fraught with subjective bias. We present a fully automated procedure that measures parametrically the similarity between songs. We tested its performance on a large database of zebra finch, Taeniopygia guttata, songs. The procedure uses an analytical framework of modern spectral analysis to characterize the acoustic structure of a song. This analysis provides a superior sound spectrogram that is then reduced to a set of simple acoustic features. Based on these features, the procedure detects similar sections between songs automatically. In addition, the procedure can be used to examine: (1) imitation accuracy across acoustic features; (2) song development; (3) the effect of brain lesions on specific song features; and (4) variability across different renditions of a song or a call produced by the same individual, across individuals and across populations. By making the procedure available we hope to promote the adoption of a standard, automated method for measuring similarity between songs or calls. Copyright 2000 The Association for the Study of Animal Behaviour.

Auditory pathways of caudal telencephalon and their relation to the song system of adult male zebra finches (Taenopygia guttata)

Auditory information is critical for vocal imitation and other elements of social life in songbirds. In zebra finches, neural centers that are necessary for the acquisition and production of learned vocalizations are known, and they all respond to acoustic stimulation. However, the circuits by which conspecific auditory signals are perceived, processed, and stored in long‐term memory have not been well documented. In particular, no evidence exists of direct connections between auditory and vocal motor pathways, and two newly identified centers for auditory processing, caudomedial neostriatum (Ncm) and caudomedial hyperstriatum ventrale (cmHV), have no documented place among known auditory circuits. Our goal was to describe anatomically the auditory pathways in adult zebra finch males and, specifically, to show the projections by which Ncm and vocal motor centers may receive auditory input. By using injections of different kinds of neuroanatomical tracers (biotinylated dextran amines, rhodamine‐linked dextran amines, biocytin, fluorogold, and rhodamine‐linked latex beads), we have shown that, as in other avian groups, the neostriatal field L complex in caudal telencephalon is the primary forebrain relay for pathways originating in the auditory thalamus, i.e., the nucleus ovoidalis complex (Ov). In addition, Ncm and cmHV also receive input from the Ov complex. Ov has been broken down into two parts, the Ov “core” and “shell,” which project in parallel to different targets in the caudal telencephalon. Parts of the field L complex are connected among themselves and to Ncm, cmHV, and caudolateral HV (cIHV) through a complex web of largely reciprocal pathways. In addition, cIHV and parts of the field L complex project strongly to the “shelf” of neostriatum underneath the song control nucleus high vocal center (HVC) and to the “cup” of archistriatum rostrodorsal to another song‐control nucleus, the robust nucleus of the archistriatum (RA). We have documented two points at which the vocal motor pathway may pick up auditory signals: the HVC‐shelf interface and a projection from cIHV to the nucleus interfacialis (NIf), which projects to HVC. These data represent the most complete survey to date of auditory pathways in the adult male zebra finch brain, and of their projections to motor stations of the song system.

The Origins of Vocal Learning

Facts and theories on the evolution of vocal learning in mammals and birds are reviewed. An attempt is made to articulate principles of general heuristic importance. Different contexts in which vocal learning occurs are evaluated. It is concluded that maximal stimulation of females and benefits accruing from formation of vocal dialects have been selective pressures leading to vocal learning. Correlations between intense speciation and vocal learning, and between long-lasting pair bonds and filial song learning, need further study. In all cases where selective pressures leading to vocal learning have been identified, females are the selective agent. Use of vocal signals to attract females is much rarer in mammals, and this is correlated with a low incidence of vocal learning. The successive steps leading from genetically determined motor ontogenies to vocal learning are discussed.

Testosterone triggers growth of brain vocal control nuclei in adult female canaries.

Two vocal control nuclei of the canary telencephalon, hyperstriatum ventrale, pars caudale (HVc) and nucleus robustus archistriatalis (RA), are larger in males, that learn complex songs, than in females, that normally do not sing. HVc and RA can be induced to grow by 90% and 53%, respectively, in adult gonadectomized females under the influence of testosterone, as these birds acquire male-like song. The magnitude of this effect is comparable, though of reversed sign, to that following early castration in males. This system is unique in the extent to which gross neural plasticity normally associated with early development can be induced in adulthood.

Developmental and seasonal changes in canary song and their relation to changes in the anatomy of song-control nuclei

Young male canaries become sexually mature in late winter, 8-12 months after hatching. During the months between hatching and sexual maturity they develop adult song. The successive stages in the development of adult song are subsong, plastic song, and stable or full song. Once stable song is achieved it lasts for the duration of the breeding season. After the end of the breeding season there is a recurrence of song instability during summer and early fall. This plastic song is followed, once more, by stable song. New song syllables are added to the song of adult male canaries and some of the earlier syllables disappear. The song repertoire sung at 2 years of age is substantially larger, and different, from that sung during the first breeding season, when the birds were 1 year old. A comparable change occurs between the second and third breeding seasons. Most of the syllables acquired by adult males are formed during the summer-fall period of song instability. Developmental and seasonal changes in song are accompanied by anatomical changes in two forebrain nuclei known to be involved in song control, the hyperstriatum ventralis, pars caudalis (HVc), and the robust nucleus of the archistriatum (RA). HVc and RA grow during the subsong and plastic song periods of song development. These nuclei reach adult size by the time stable adult song is first produced, and retain this size during the breeding season. However, the size of HVc and RA diminishes by late summer, when it becomes comparable to that of a 3- to 4-month-old bird. This reduction in size is temporary and has been corrected by the following breeding season. It is suggested that these seasonal changes in volume reflect circuit changes which are under hormonal control, and that these changes are related to processes of learning and, possibly, forgetting. Despite earlier reports of left hemispheric dominance in canary song production, we failed to find any evidence of right-left systematic differences in the size of HVc and RA during development or in adulthood. Various hypotheses relating song learning to changes in the underlying anatomy are offered.

THE SONG OF THE CHINGOLO, ZOiVOTRICHlA CAPENSIS, IN ARGENTINA: DESCRIPTION AND EVALUATION OF A SYSTEM OF DIALECTS

Any intelligent statement about the role of dialects in bird song presupposes a knowledge of the functions of song. It has been suggested that song may subserve territorial advertisement, attracting unmated females and repelling other males. Less speculation has attended the possibility that song may stimulate the female to undergo hormonal changes leading towards ovulation or that it may affect other aspects of the integration of breeding behavior.

Targeted Neuronal Death Affects Neuronal Replacement and Vocal Behavior in Adult Songbirds

In the high vocal center (HVC) of adult songbirds, increases in spontaneous neuronal replacement correlate with song changes and with cell death. We experimentally induced death of specific HVC neuron types in adult male zebra finches using targeted photolysis. Induced death of a projection neuron type that normally turns over resulted in compensatory replacement of the same type. Induced death of the normally nonreplaced type did not stimulate their replacement. In juveniles, death of the latter type increased recruitment of the replaceable kind. We infer that neuronal death regulates the recruitment of replaceable neurons. Song deteriorated in some birds only after elimination of replaceable neurons. Behavioral deficits were transient and followed by variable degrees of recovery. This raises the possibility that induced neuronal replacement can restore a learned behavior.

Neuronal Replacement in Adulthood

My colleagues and I are interested in brain events that control learning. Our work, using canaries, has shown that brain cells can be replaced in adulthood. We suspect that neuronal replacement in adulthood is related to some kinds of learning; it is also a form of brain repair, though it happens in the absence of an external lesion. I will present the background to this work and our most recent findings.

BDNF Mediates the Effects of Testosterone on the Survival of New Neurons in an Adult Brain

New neurons are incorporated into the high vocal center (HVC), a nucleus of the adult canary (Serinus canaria) brain that plays a critical role in the acquisition and production of learned song. Recruitment of new neurons in the HVC is seasonally regulated and depends upon testosterone levels. We show here that brain-derived neurotrophic factor (BDNF) is present in the HVC of adult males but is not detectable in that of females, though the HVC of both sexes has BDNF receptors (TrkB). Testosterone treatment increases the levels of BDNF protein in the female HVC, and BDNF infused into the HVC of adult females triples the number of new neurons. Infusion of a neutralizing antibody to BDNF blocks the testosterone-induced increase in new neurons. Our results demonstrate that BDNF is involved in the regulation of neuronal replacement in the adult canary brain and suggest that the effects of testosterone are mediated through BDNF.

Brain space for a learned task.

Forty-six adult male and female canaries were sacrificed, their brains were weighed and the volume of several brain nuclei reconstructed from the cresyl violet-stained material. Two forebrain vocal control nuclei, hyperstriatum ventrale, pars caudale (HVc) and nucleus robustus archistriatalis (RA), were approximately 4 and 3 times larger, respectively, in males than in females, confirming previous findings. There was no consistent right-left asymmetry in the volume of these nuclei in males and females. Twenty-five male birds in this study had their song repertoire recorded during the peak of the singing season. They were sacrificed 3 to 4 months later. The size of the song repertoire, measured as number of different syllable types, showed a positive and significant correlation with the size of HVc and RA. There was no significant correlation between size of the syllable repertoire and age, brain weight or the volume of two brain nuclei not involved in song control. This is the first time that the amount of brain allotted to a specific learned skill has been shown to correlate positively with the amount of that skill that is learned. Interestingly, too, there was a positive and significant correlation between testis weight at the end of the breeding season and the volume of RA at that time, suggesting a hormone-mediated seasonal modulation of part of the brain space occupied by song control pathways. This material seems well suited for studying the relation between space and learning, and the manner in which this relation is influenced by gonadal hormones.