Song recognition in zebra finches: Are there sensitive periods for song memorization?

Male zebra finches learn to sing songs that they hear between 25 and 65 days of age, the sensitive period for song learning. In this experiment, male and female zebra finches were exposed to zebra finch songs either before (n = 9) or during (n = 4) the sensitive period. Following song exposure, recognition memory for the songs was assessed with an operant discrimination between familiar and novel songs. Zebra finches that were exposed to songs between 22 and 30 days of age discriminated between familiar and novel songs; zebra finches exposed to songs from 9 to 17 days of age did not. Failure to memorize songs heard prior to the sensitive period may contribute to the exclusion of those songs from the repertoire of songbirds.     

Vocal syntax development in the white-crowned sparrow (Zonotrichia leucophrys).

Birdsong development exemplifies the interplay between experience and predisposition that occurs during behavioral ontogeny. Songbirds must hear song models to develop normal song, yet they preferentially learn conspecific song when given a choice in the laboratory. To the extent that features guiding this selective learning are pre-encoded in the brain, such features should also develop in the song of young birds not exposed to them in tutor models. To investigate whether song syntax-phrase number and order--is such a feature in the white-crowned sparrow (Zonotrichia leucophrys), the authors tutored males of this species with separate phrase models. Birds learned and assembled these into songs of species-typical sequence, suggesting that syntax is to some degree pre-encoded in white-crowned sparrows. Birds also learned heterospecific phrases, confirming previous evidence that note phonology is not the primary cue for selective song learning in this species.     

Hippocampal activation of immediate early genes Zenk and c-Fos in zebra finches (Taeniopygia guttata) during learning and recall of a spatial memory task

Zebra finches (Taeniopygia guttata) are able to learn the position of food by orienting on spatial cues in a ‘dry water maze’. In the course of spatial learning, the hippocampus shows high expression of the immediate early genes (IEGs) Zenk and c-Fos, indicating high activation of this area during learning. In contrast, the IEG activity is nearly absent if the birds do not have to rely on spatial cues. In the present experiment it was investigated whether hippocampal activation can also be observed if the learned spatial task is recalled. For this purpose, the hippocampal Zenk and c-Fos activation of birds in an early learning stage was compared with that of others having well reached their maximal performance. The results show that the avian hippocampus is also active during recall of a learned spatial task, but the activation is significantly lower than in animals learning actually. As in previous experiments, hippocampal IEG expression showed strong variation not only in the position of the active patches of neurons, but also in size and cell density. The observed difference contributes to the view that immediate early genes may not be indicators of activation alone, but may be due to a combination of activation and plastic changes.     

Direct social contacts override auditory information in the song-learning process in starlings (Sturnus vulgaris)

Social influence on song acquisition was studied in 3 groups of young European starlings raised under different social conditions but with the same auditory experience of adult song. Attentional focusing on preferred partners appears the most likely explanation for differences found in song acquisition in relation to experience, sex, and song categories. Thus, pair-isolated birds learned from each other and not from broadcast live songs, females did not learn from the adult male tutors, and sharing occurred more between socially associated peers. On the contrary, single-isolated birds clearly copied the adult songs that may have been the only source of attention stimulation. Therefore, social preference appears as both a motor for song learning and a potential obstacle for acquisition from nonpreferred partners, including adults.     

Behavioral consequences of song learning: Discrimination of song types by male white-crowned sparrows

The functional significance of learned population differences in male song in the white-crowned sparrow was explored in natural populations using playback tests. Laboratory results have shown that learning of the population-specific song seems to take place in early life and is strongly dependent upon the nature of the auditory experience at that time. However, the varied results of recent studies make it difficult to reach a confident conclusion about the ecological functions of song learning. The present research took advantage of naturally occurring variation in the differences between songs of adjacent populations to determine a function relating degree of difference in song to intensity of territorial singing elicited. Applying a typological evaluation of syllable structure to the four segments of the song allowed a crude quantitative ranking of the differences between local songs and playback stimuli. These results, together with those of other studies, suggest a unimodal aggressive response function of males to songs of other males. A maximum response to songs slightly different from the local song environment suggests that male exclusion based upon acquired song components may contribute to the maintenance of discrete and stable song dialects.     

Shared musical knowledge in 11‐month‐old infants

Five‐month‐old infants selectively attend to novel people who sing melodies originally learned from a parent, but not melodies learned from a musical toy or from an unfamiliar singing adult, suggesting that music conveys social information to infant listeners. Here, we test this interpretation further in older infants with a more direct measure of social preferences. We randomly assigned 64 11‐month‐old infants to 1–2 weeks’ exposure to one of two novel play songs that a parent either sang or produced by activating a recording inside a toy. Infants then viewed videos of two new people, each singing one song. When the people, now silent, each presented the infant with an object, infants in both conditions preferentially chose the object endorsed by the singer of the familiar song. Nevertheless, infants’ visual attention to that object was predicted by the degree of song exposure only for infants who learned from the singing of a parent. Eleven‐month‐olds thus garner social information from songs, whether learned from singing people or from social play with musical toys, but parental singing has distinctive effects on infants’ responses to new singers. Both findings support the hypothesis that infants endow music with social meaning. These findings raise questions concerning the types of music and behavioral contexts that elicit infants’ social responses to those who share music with them, and they support suggestions concerning the psychological functions of music both in contemporary environments and in the environments in which humans evolved.     

Factors influencing song development in the white-crowned sparrow (Zonotrichia leucophrys)

Nestling white-crowned sparrows (Zonotrichia leucophrys nuttalli) were hand-reared in sound-isolation chambers under a variety of conditions. The songs of total isolates were compared with songs of birds tutored with song, and the number of inputs sufficient for a bird to produce a normal song was explored. The flexibility of the song learning system was investigated with a range of tape-recorded tutor songs: alien dialects, alien subspecies, alien species, alternating alien dialects, and an aberrant song. Adult songs were obtained for 40 males and 7 testosterone-injected females. All of the tutor songs could be learned. Also, some birds learned elements of an alien species' song. Birds tutored with two songs copied one or the other, were bilingual, or sang a hybrid of the two. No bird presented with fewer than 120 songs learned the tutor song; 2 birds tutored with 252 songs copied the tutor song. It is concluded that the song learning system is quite flexible, hat the results obtained with tape-tutors are very different from those with social tutors, and that there may be an interaction between total number of song inputs and the number presented on a single day. Some implications of these data for physiological mechanisms and the possible functional significance of the acquisition system are discussed.     

Song learning and cognitive ability are not consistently related in a songbird

Learned aspects of song have been hypothesized to signal cognitive ability in songbirds. We tested this hypothesis in hand-reared song sparrows (Melospiza melodia) that were tutored with playback of adult songs during the critical period for song learning. The songs developed by the 19 male subjects were compared to the model songs to produce two measures of song learning: the proportion of notes copied from models and the average spectrogram cross-correlation between copied notes and model notes. Song repertoire size, which reflects song complexity, was also measured. At 1 year of age, subjects were given a battery of five cognitive tests that measured speed of learning in the context of a novel foraging task, color association, color reversal, detour-reaching, and spatial learning. Bivariate correlations between the three song measures and the five cognitive measures revealed no significant associations. As in other studies of avian cognition, different cognitive measures were for the most part not correlated with each other, and this result remained true when 22 hand-reared female song sparrows were added to the analysis. General linear mixed models controlling for effects of neophobia and nest of origin indicated that all three song measures were associated with better performance on color reversal and spatial learning but were associated with worse performance on novel foraging and detour-reaching. Overall, the results do not support the hypothesis that learned aspects of song signal cognitive ability.     

Sequential learning and rule abstraction in Bengalese finches

The Bengalese finch (Lonchura striata var. domestica) is a species of songbird. Males sing courtship songs with complex note-to-note transition rules, while females discriminate these songs when choosing their mate. The present study uses serial reaction time (RT) to examine the characteristics of the Bengalese finches’ sequential behaviours beyond song production. The birds were trained to produce the sequence with an “A–B–A” structure. After the RT to each key position was determined to be stable, we tested the acquisition of the trained sequential response by presenting novel and random three-term sequences (random test). We also examined whether they could abstract the embedded rule in the trained sequence and apply it to the novel test sequence (abstract test). Additionally, we examined rule abstraction through example training by increasing the number of examples in baseline training from 1 to 5. When considered as (gender) groups, training with 5 examples resulted in no statistically significant differences in the abstract tests, while statistically significant differences were observed in the random tests, suggesting that the male birds learned the trained sequences and transferred the abstract structure they had learned during the training trials. Individual data indicated that males, as opposed to females, were likely to learn the motor pattern of the sequence. The results are consistent with observations that males learn to produce songs with complex sequential rules, whereas females do not.     

Early tutoring and adult reproductive behaviour in female domestic canary (Serinus canaria)

We studied the effect of early tutoring on the subsequent sexual preferences and reproductive activity of female domestic canaries (Serinus canaria). Young female canaries were exposed during the first 4 months of life to songs of either domestic or wild canaries. When adult, these females were again exposed to domestic or wild songs. In the first experiment, the sexual responses of the females to unfamiliar domestic and wild songs were quantified with the copulation solicitation display (CSD) assay. In the second experiment, the same females were tested again with modified tutoring songs. In the third experiment, song stimulation of nest-building and egg-laying was studied. Domestic-strain-tutored females gave more CSDs to domestic than to wild songs. In contrast, wild-strain-tutored females showed no sexual preference. We propose that the sexual preference of adult domestic-strain-tutored female canaries for domestic songs is the consequence of learning and categorisation processes. The discrepancy between the results of the domestic-strain-tutored females and those of the wild-strain-tutored females suggests that female canaries have a predisposition to learn songs of their own strain rather than songs of an alien strain. In the third experiment nest-building and egg-laying activities appeared to be unaffected by early tutoring conditions: there was no significant differential effect of the different tutoring and exposure conditions on nest-building and egg-laying scores. Mate attraction and stimulation of females’ reproductive activity appear to be two separate functions of male song, which may have been shaped by different evolutionary constraints. Received: 24 July 1999 / Accepted after revision: 22 February 2000     

Rapidly learned song-discrimination without behavioral reinforcement in adult male zebra finches (Taeniopygia guttata)

Zebra finches communicate via several distinct vocalizations, of which song is the most studied. Behavioral observations indicate that adults are able to discriminate among the songs of different conspecific individuals. In the wild, zebra finches live in structured but mobile colonies, and encounter new individuals on a frequent basis. Thus it seems plausible that adult finches might have the capacity to recognize and remember new songs they encounter on a single day, but this has never been directly tested. Here we devised a simple observational assay to determine whether adult male zebra finches show recognition of a song they have heard repeatedly from taped playbacks, over a single three hour period the day before. We quantified the rate of production of six discrete behaviors (short calls, contact calls, singing, short hops, long hops, and beak swipes) made by adult male zebra finches as they listened to the playbacks. At the onset of song playback, all birds suspended these behaviors and sat silently-occasionally moving their heads. Then, after a measurable period ("response latency"), the birds resumed these activities. We observed that the response latency was long (approximately 10 min) when birds were hearing a particular song for the first time. The response latency was much shorter (approximately 1-2 min) when the birds had heard the same song the day before. Thus, functional song memories must result from as little as 3 h of passive song-exposure. These results suggest that ongoing song learning may play a natural role in the daily life of adult zebra finches, and provide a behavioral reference point for studies of molecular and physiological plasticity in the adult auditory system.     

Influence of social conditions in song sharing in the adult canary

In songbirds, experience of social and environmental cues during a discrete period after birth may dramatically influence song learning. In the canary, the ability to learn new songs is assumed to persist throughout life. The aim of the present study was to investigate whether social context could guide changes in adult song. Three groups of canaries were kept in different social and temporal conditions. Results showed that the multiple hierarchical levels of the canary song structure were affected by social environment: songs of males housed together for 2 years were more similar than those of males that spent the same time in individual cages in regard to acoustic parameters, syllable repertoire and repertoire of sequences of two-syllable types. However, social housing did not result in the emergence of a group-specific vocal signature within songs. In conclusion, these results suggested that under the influence of social factors, a copying process could allow adult canaries to adjust, at least in part, their songs to those of other individuals.     

Song copying by humpback whales: themes and variations

Male humpback whales (Megaptera novaeangliae) produce long, structured sequences of sound underwater, commonly called songs. Humpbacks progressively modify their songs over time in ways that suggest that individuals are copying song elements that they hear being used by other singers. Little is known about the factors that determine how whales learn from their auditory experiences. Song learning in birds is better understood and appears to be constrained by stable core attributes such as species-specific sound repertoires and song syntax. To clarify whether similar constraints exist for song learning by humpbacks, we analyzed changes over 14 years in the sounds used by humpback whales singing in Hawaiian waters. We found that although the properties of individual sounds within songs are quite variable over time, the overall distribution of certain acoustic features within the repertoire appears to be stable. In particular, our findings suggest that species-specific constraints on temporal features of song sounds determine song form, whereas spectral variability allows whales to flexibly adapt song elements.Electronic Supplementary Material Supplementary material is available for this article at .     

Perinatal exposure to diethylstilbestrol improves olfactory discrimination learning in male and female Swiss-Webster mice

During late prenatal and early postnatal brain development, estrogen induces structural sex differences that correspond to behavioral differences in certain domains such as learning and memory. The typically superior performance of males is attributed to the action of elevated concentrations of estrogen, derived inside neurons from the aromatization of testosterone. In contrast, female performance appears dependent on minimal estrogenic activity. Rat models of the relationship between hormones and cognitive behavior predominate the field, but the advent of genetically modified mice as research tools necessitates development of analogous mouse models. This study examined how early postnatal exposure to the synthetic estrogen diethylstilbestrol (DES) affected the ability of male and female Swiss-Webster mice to learn a two-choice olfactory discrimination and three repeated reversals. Mice treated with subcutaneous injections of DES from postnatal days 1-10 learned reversals more readily than oil-treated controls, a difference that became evident after repeated testing. DES-exposed males and females learned reversals at a comparable rate, suggesting that early postnatal estrogen exposure does not influence this mode of learning through a sexually differentiated mechanism in mice. An analysis of response patterns during qualitatively different phases of reversal learning revealed that DES-induced improvements probably were not due to greater inhibitory control. Instead, DES appeared to enhance associative ability. Early postnatal estrogen exposure may have the potential to preserve certain cognitive skills in adulthood.     

Two-year-olds learn novel nouns,verbs, and conventional actions from massed or distributed exposures

Two-year-old children were taught either 6 novel nouns, 6 novel verbs, or 6 novel actions over 1 month. In each condition, children were exposed to some items in massed presentations (on a single day) and some in distributed presentations (over the 2 weeks). Children's comprehension and production was tested at 3 intervals after training. In comprehension, children learned all types of items in all training conditions at all retention intervals. For production, the main findings were that (a) production was better for nonverbal actions than for either word type, (b) children produced more new nouns than verbs, (c) production of words was better following distributed than massed exposure, and (d) time to testing (immediate, 1 day, 1 week) did not affect retention. A follow-up study showed that the most important timing variable was the number of different days of exposure, with more days facilitating production. Results are discussed in terms of 2 key issues: (a) the domain-generality versus domain-specificity of processes of word learning and (b) the relative ease with which children learn nouns versus verbs.     

NR2B downregulation in a forebrain region required for avian vocal learning is not sufficient to close the sensitive period for song learning

The neural changes that limit the sensitive period for avian song development are unknown, but neurons in a forebrain region critical for song learning, the lMAN, exhibit experience-driven changes in NMDAR subunit expression that could regulate sensitive period closure. Specifically, NR2B levels in lMAN decrease during song acquisition, potentially reducing synaptic plasticity by decreasing NMDAR EPSC duration and/or affecting NMDAR-coupled intracellular cascades. While rearing birds in isolation extends the sensitive period and also delays the developmental changes in NR2B expression and NMDAR physiology, recent work indicates that a transition to faster NMDAR currents does not preclude further song learning. However, NR2B mRNA expression in isolates remains elevated beyond the age at which NMDAR currents shorten, leaving open the possibility that NR2B levels regulate closure of the sensitive period through effects other than those mediated by NMDAR current duration. To determine whether the experience-driven decrease in NR2B expression in lMAN closes the sensitive period, we promoted this change in gene expression either by treating isolation-reared zebra finches briefly with testosterone (T-isolates) or by allowing males limited access to conspecific song (pre-exposed isolates). We then assessed if these birds could acquire song from tutors after the normal close of the sensitive period. Despite a normal decline in NR2B expression, T-isolate and pre-exposed isolate birds learned tutor songs heard from d65-90, while normally reared birds did not. These findings suggest that the normal decline in NR2B expression with lMAN is not sufficient for sensitive period closure.     

Auditory scene analysis in estrildid finches (Taeniopygia guttata and Lonchura striata domestica): a species advantage for detection of conspecific song

Operant-conditioning techniques were used to investigate the ability of zebra finches (Taeniopygia guttata) and Bengalese finches (Lonchura striata domestica) to detect a zebra finch or a Bengalese finch target song intermixed with other birdsongs. Sixteen birds were trained to respond to the presence of a particular target song, either of their own species (n = 8) or of another species (n = 8). The birds were able to learn a discrimination between song mixtures that contained a target song and song mixtures that did not, and they were able to maintain their response to the target song when it was mixed with novel songs. Zebra finches, but not Bengalese finches, learned the discrimination with a conspecific target more quickly and were worse at detecting a Bengalese finch in the presence of a conspecific song. The results indicate that selective attention to birdsongs within an auditory scene is related to their biological relevance.     

Does zebra finch (Taeniopygia guttata) preference for the (familiar) father's song generalize to the songs of unfamiliar brothers?

Several studies have demonstrated that zebra finches (Taeniopygia guttata) prefer their fathers' songs over unfamiliar songs. Songs of tutors (i.e., fathers) and tutees (i.e., sons) resemble each other as a result of cultural transmission. Subjects (N = 18) with a previously established preference for the father's song could choose between the song of an unfamiliar brother or a random unfamiliar song in an operant task. Most subjects showed a significant preference for either category of song, but overall, the songs of unfamiliar brothers were not preferred, although they were more similar to the father's song than were the unfamiliar songs. This suggests that subjects did not generalize their learned preference for a song of a particular tutor to the songs of his tutees.     

Children's memory for new songs: integration or independent storage of words and tunes?

The present study investigated how young children encode a song in memory, specifically, whether they integrate or store independently in memory the text and the tune of a song. Preschool children and, for purposes of comparison, adults, each participated in two test sessions: in one they were presented three novel tunes each with rhyming text and in the other they heard the same three tunes but with nonrhyming text. Following this familiarization phase they received a recognition test. On each trial, they heard one of five types of songs; the original song, a completely new song (new words, new tune), a mismatch of the tune of one song with the words of another, old words with a new tune, and new words with an old tune. The subject's task was to decide if each test song was "exactly the same," "somewhat the same," or "not at all the same" as any one of the three original songs. At both ages the proportion of "same" responses was significantly greater for the original than mismatch songs, indicating that listeners were more likely to remember the exact pairing of text and tune than to retain the components independently. However, integration was significantly greater for adults than children. At both ages, for songs judged as similar to the original songs, the words more often than the tune proved to be the most salient feature, particularly for children. There were no significant effects of rhyme on performance at either age. The results are discussed in terms of Serafine, Crowder, and Repp's (1984) hypothesis that one integrates the tune and text of a song in memory, rather than storing components separately.     

Awareness of Recognition Memory for Polish and English Folk Songs in Polish and English Folk

Polish and English people listened either once or three times to excerpts from Polish and English folk songs before being given a recognition test in which, when recognising an excerpt, they had to report whether they remembered hearing it, knew they had heard it, or guessed they had heard it. Both Polish and English people remembered more of the excerpts from their own folk songs, and they remembered more of the excerpts they heard three times rather than once, regardless of the national background of the songs. They also knew they had heard more of the excerpts they heard three times, but only if they were from the other folk's songs. Repetition did not affect knowing songs from one's own national background. These findings confirm and extend previous findings suggesting that remembering and knowing are functionally independent states of awareness.