Expression of oxytocin receptors in the zebra finch brain during vocal development

AbstractJuvenile male zebra finches memorize and learn to sing the song of a male caregiver, or “tutor”, during a complex vocal learning process. Juveniles are highly motivated to interact socially with their tutor, and these interactions are required for effective vocal learning. It is currently unknown what neurological mechanisms underlie attraction to tutors, but social motivation and affiliation in this and other species may be mediated by oxytocin and related nonapeptides. Here, we used qPCR to quantify expression of oxytocin receptor (OTR) mRNA in the lateral septum, auditory forebrain, and regions of the song control system in zebra finches throughout post-hatch development and vocal learning. We found that zebra finches express OTR mRNA in these regions from post-hatch day 5 to adulthood, encompassing the entire period of auditory and sensorimotor learning. We also mapped the binding of 125I-ornithine vasotocin, an oxytocin receptor antagonist that binds to oxytocin receptors in songbird brain, to understand the neuroanatomical distribution of oxytocin-like action during vocal development. This study provides the groundwork for the use of zebra finches as a model for understanding the mechanisms underlying social motivation and its role in vocal development.

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Oxytocin receptor antagonism during song tutoring in zebra finches reduces preference for and learning of the tutor's song

10.1101/2021.06.16.448133 ◽

2021 ◽

Author(s):

Natalie R. Pilgeram ◽

Nicole M. Baran ◽

Aditya Bhise ◽

Matthew T. Davis ◽

Emily Kim ◽

...

Keyword(s):

Social Interactions ◽

Vocal Learning ◽

Oxytocin Receptor ◽

Developmental Trajectory ◽

The Other ◽

Sensitive Period ◽

Saline Control ◽

Zebra Finches ◽

Social Orienting ◽

Oxytocin Receptors

In species with vocal learning, acquiring species-typical vocalizations relies on early social orienting. In zebra finches (Taeniopygia guttata), for example, learning song requires dynamic social interactions with a "tutor" during an early sensitive period. The oxytocin system plays a central role in social orienting across species, yet it is unknown whether this system participates in the attentional and motivational processes that support vocal learning. Here, we tested whether blocking oxytocin receptors during exposure to tutors would impact learning from those tutors. Juvenile, song-naïve males were each tutored by two unfamiliar adults. During exposure to one tutor, juveniles were treated with oxytocin receptor antagonist (OTA) and during exposure to the other, saline (control). We found that OTA significantly reduced behaviors associated with approach and attention during tutoring sessions. Next, using an operant assay in which exposure to the two songs was balanced, we found that the juveniles preferred the control song over the OTA song. The developmental trajectory of preference for the control song resembled the pattern shown by father-reared birds choosing to hear their father's song. Finally, the adult songs of the tutored birds more closely resembled control song than OTA song. The magnitude of this difference was significantly predicted by the early preference for the control song. Overall, oxytocin antagonism during exposure to a tutor seemed to bias juveniles against that tutor and his song. Our results suggest that oxytocin receptors play a role in socially-guided vocal learning in zebra finches, perhaps by affecting attention and motivation during tutoring.

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Afferent influences on cell death and birth during development of a cortical nucleus necessary for learned vocal behavior in zebra finches

Development ◽

10.1242/dev.120.1.13 ◽

1994 ◽

Vol 120 (1) ◽

pp. 13-24

Author(s):

F. Johnson ◽

S. W. Bottjer

Keyword(s):

Vocal Learning ◽

Afferent Input ◽

Vocal Behavior ◽

Projection Neurons ◽

Zebra Finches ◽

Vocal Development ◽

Neuron Death ◽

Cortical Nucleus ◽

Alternate Source ◽

Cortical Regions

Forebrain nuclei that control learned vocal behavior in zebra finches are anatomically distinct and interconnected by a simple pattern of axonal pathways. In the present study, we examined afferent regulation of neuronal survival during development of the robust nucleus of the archistriatum (RA). RA projection neurons form the descending motor pathway of cortical vocal-control regions and are believed to be directly involved in vocal production. RA receives afferent inputs from two other cortical regions, the lateral magnocellular nucleus of the anterior neostriatum (lMAN) and the higher vocal center (HVC). However, because the ingrowth of HVC afferent input is delayed, lMAN projection neurons provide the majority of afferent input to RA during early vocal learning. lMAN afferent input to RA is of particular interest because lMAN is necessary for vocal learning only during a restricted period of development. By making lesions of lMAN in male zebra finches at various stages of vocal development (20-60 days of age) and in adults (>90-days old), we asked whether the survival of RA neurons depends on lMAN afferent input, and if so whether such dependence changes over the course of vocal learning. The results showed that removal of lMAN afferent input induced the loss of over 40% of RA neurons among birds in early stages of vocal development (20 days of age). However, lMAN lesions lost the ability to induce RA neuron death among birds in later stages of vocal development (40 days of age and older). These findings indicate that many RA neurons require lMAN afferent input for their survival during early vocal learning, whereas the inability of lMAN lesions to induce RA neuron death in older birds may indicate a reduced requirement for afferent input or perhaps the delayed ingrowth of HVC afferent input (at approx. 35 days of age) provides an alternate source of afferent support. Removal of lMAN afferent input also dramatically increased the incidence of mitotic figures in RA, but only among 20-day-old birds at 2 days post-lesion. The early, acute nature of the mitotic events raises the possibility that cell division in RA may be regulated by lMAN afferent input.

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Timing of perineuronal net development in the zebra finch song control system correlates with developmental song learning

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2018.0849 ◽

2018 ◽

Vol 285 (1883) ◽

pp. 20180849 ◽

Cited By ~ 9

Author(s):

Gilles Cornez ◽

Elisabeth Jonckers ◽

Sita M. ter Haar ◽

Annemie Van der Linden ◽

Charlotte A. Cornil ◽

...

Keyword(s):

Control System ◽

Neural Plasticity ◽

Ocular Dominance ◽

Song Learning ◽

Dominance Model ◽

Perineuronal Net ◽

Acoustic Environment ◽

Auditory Forebrain ◽

Song Control System ◽

Song Control

The appearance of perineuronal nets (PNNs) represents one of the mechanisms that contribute to the closing of sensitive periods for neural plasticity. This relationship has mostly been studied in the ocular dominance model in rodents. Previous studies also indicated that PNN might control neural plasticity in the song control system of songbirds. To further elucidate this relationship, we quantified PNN expression and their localization around parvalbumin interneurons at key time-points during ontogeny in both male and female zebra finches, and correlated these data with the well-described development of song in this species. We also extended these analyses to the auditory system. The development of PNN during ontogeny correlated with song crystallization although the timing of PNN appearance in the four main telencephalic song control nuclei slightly varied between nuclei in agreement with the established role these nuclei play during song learning. Our data also indicate that very few PNN develop in the secondary auditory forebrain areas even in adult birds, which may allow constant adaptation to a changing acoustic environment by allowing synaptic reorganization during adulthood.

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Nerve growth factor effects on the song control system of zebra finches

Neuroscience Letters ◽

10.1016/s0304-3940(97)13425-5 ◽

1997 ◽

Vol 223 (3) ◽

pp. 161-164 ◽

Cited By ~ 7

Author(s):

M Fiore ◽

S.N Patel ◽

E Alleva ◽

L Aloe ◽

N.S Clayton

Keyword(s):

Control System ◽

Nerve Growth Factor ◽

Growth Factor ◽

Zebra Finches ◽

Nerve Growth ◽

Song Control System ◽

Song Control

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Early life manipulations of vasopressin-family peptides alter vocal learning

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2017.1114 ◽

2017 ◽

Vol 284 (1859) ◽

pp. 20171114 ◽

Cited By ~ 8

Author(s):

Nicole M. Baran ◽

Samantha C. Peck ◽

Tabitha H. Kim ◽

Michael H. Goldstein ◽

Elizabeth Adkins-Regan

Keyword(s):

Vocal Learning ◽

Young Male ◽

Social Motivation ◽

Arginine Vasotocin ◽

Zebra Finches ◽

Human Infants ◽

Wide Range ◽

Typical Behaviour ◽

Interactive Feedback

Vocal learning from social partners is crucial for the successful development of communication in a wide range of species. Social interactions organize attention and enhance motivation to learn species-typical behaviour. However, the neurobiological mechanisms connecting social motivation and vocal learning are unknown. Using zebra finches ( Taeniopygia guttata ), a ubiquitous model for vocal learning, we show that manipulations of nonapeptide hormones in the vasopressin family (arginine vasotocin, AVT) early in development can promote or disrupt both song and social motivation. Young male zebra finches, like human infants, are socially gregarious and require interactive feedback from adult tutors to learn mature vocal forms. To investigate the role of social motivational mechanisms in song learning, in two studies, we injected hatchling males with AVT or Manning compound (MC, a nonapeptide receptor antagonist) on days 2–8 post-hatching and recorded song at maturity. In both studies, MC males produced a worse match to tutor song than controls. In study 2, which experimentally controlled for tutor and genetic factors, AVT males also learned song significantly better compared with controls. Furthermore, song similarity correlated with several measures of social motivation throughout development. These findings provide the first evidence that nonapeptides are critical to the development of vocal learning.

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Song preferences predict the quality of vocal learning in zebra finches

10.1101/2021.06.01.446570 ◽

2021 ◽

Author(s):

Carlos A. Rodriguez-Saltos ◽

Aditya Bhise ◽

Prasanna Karur ◽

Ramsha Nabihah Khan ◽

Sumin Lee ◽

...

Keyword(s):

Reinforcement Schedule ◽

Social Process ◽

Vocal Learning ◽

Song Learning ◽

Sensitive Period ◽

Social Reward ◽

Zebra Finches ◽

Vocal Development ◽

Song Preferences

In songbirds, learning to sing is a highly social process that likely involves social reward. Here, we hypothesized that the degree to which a juvenile songbird learns a song depends on the degree to which it finds that song rewarding to hear during vocal development. We tested this hypothesis by measuring song preferences in young birds during song learning and then analyzing their adult songs. Song preferences were measured in an operant key-pressing assay. Juvenile male zebra finches (Taeniopygia guttata) had access to two keys, each of which was associated with a higher likelihood of playing the song of their father or that of another familiar adult ("neighbor"). To minimize the effects of exposure on learning, we implemented a reinforcement schedule that allowed us to detect preferences while balancing exposure to each song. On average, the juveniles significantly preferred the father's song early during song learning, before they were themselves singing. At around post-hatch day 60, their preference shifted to the neighbor's song. At the end of the song learning period, we recorded the juveniles' songs and compared them to the father's and the neighbor's song. All of the birds copied father's song. The accuracy with which the father's song was imitated was positively correlated with the peak strength of the preference for the father's song during the sensitive period. Our results show that preference for a social stimulus, in this case a vocalization, predicted social learning during development.

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A sex chromosome drives the emergence of vocal learning following hormonal manipulation in female zebra finches

10.1101/2021.07.12.452102 ◽

2021 ◽

Author(s):

Matthew Davenport ◽

Ha Na Choe ◽

Hiroaki Matsunami ◽

Erich D Jarvis

Keyword(s):

Sex Chromosome ◽

System Development ◽

Regulatory Element ◽

Vocal Learning ◽

Brain Regions ◽

Z Chromosome ◽

Dependent Manner ◽

Zebra Finches ◽

Hormonal Manipulation ◽

Song Control

Zebra finches are sexually dimorphic vocal learners. Males learn to sing by imitating mature conspecifics, but females do not. The lack of vocal learning in females is associated with anatomical differences in the neural circuits responsible for vocal learning, including the atrophy of several brain regions during development. However, this atrophy can be prevented and song learning retained in females after pharmacological estrogen treatment. Little is known about the genetic machinery controlling this sex and estrogen responsive song system development. To screen for drivers, we performed an unbiased analysis of transcriptomes from song control nuclei and surrounding motor regions in zebra finches of either sex treated with 17-B-estradiol or vehicle until sacrifice on day 30, when divergence between the sexes is anatomically apparent. Utilizing the newly assembled autosomes and sex chromosomes from the zebra finch Vertebrate Genomes Project assemblies, we identified correlated gene modules that were associated to song nuclei in a sex and estradiol dependent manner. Female estradiol treated HVC, in the vocal learning circuit, acquired the smallest of the modular specializations observed in male HVC. This module was enriched for genes governing anatomical development, and its specilization was dispraportionately influenced by the expression of Z sex chromosome transcripts in HVC. We propose that vocal learning may be prevented in female zebra finches via the suppression of an estrogen inducible Z chromosome cis-acting regulatory element.

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