scholarly journals Estrogen and sex-dependent loss of the vocal learning system in female zebra finches

2020 ◽  
Author(s):  
Ha Na Choe ◽  
Jeevan Tewari ◽  
Kevin W. Zhu ◽  
Matthew Davenport ◽  
Hiroaki Matsunami ◽  
...  
Keyword(s):  
Expression Profiles ◽  
Critical Role ◽  
Vocal Learning ◽  
Song Learning ◽  
Learning System ◽  
Normal Male ◽  
Zebra Finches ◽  
Song System ◽  
Estrogen Synthesis

AbstractSex hormones alter the organization of the brain during early development and coordinate various behaviors throughout life. In zebra finches, song learning is limited to males, and the associated song learning brain pathway only matures in males and atrophies in females. This atrophy can be reversed by giving females exogenous estrogen during early post-hatch development, but whether normal male song system development requires estrogen is uncertain. For the first time in songbirds, we administered exemestane, a potent third generation estrogen synthesis inhibitor, from the day of hatching until adulthood. We examined the behavior, brain, and transcriptome of individual song nuclei of these pharmacologically manipulated animals. We found that males with long-term exemestane treatment had diminished male-specific plumage, impaired song learning, but retained normal song nuclei sizes and most, but not all, of their specialized transcriptome. Consistent with prior findings, females with long-term estrogen treatment retained a functional song system, and we further observed their song nuclei had specialized gene expression profiles similar, but not identical to males. We also observed that different song nuclei responded to estrogen manipulation differently, with Area X in the striatum being the most altered by estrogen modulation. These findings support the hypothesis that song learning is an ancestral trait in both sexes, which was subsequently suppressed in females of some species, and that estrogen has come to play a critical role in modulating this suppression as well as refinement of song learning.

scholarly journals Adding colour-realistic video images to audio playbacks increases stimulus engagement but does not enhance vocal learning in zebra finches

2021 ◽  
Author(s):  
Judith M. Varkevisser ◽  
Ralph Simon ◽  
Ezequiel Mendoza ◽  
Martin How ◽  
Idse van Hijlkema ◽  
...  
Keyword(s):  
Visual Cues ◽  
Sound Production ◽  
Visual Stimuli ◽  
Vocal Learning ◽  
Song Learning ◽  
Frame Rate ◽  
Zebra Finches ◽  
Video Content ◽  
Biologically Relevant ◽  
Video Images

AbstractBird song and human speech are learned early in life and for both cases engagement with live social tutors generally leads to better learning outcomes than passive audio-only exposure. Real-world tutor–tutee relations are normally not uni- but multimodal and observations suggest that visual cues related to sound production might enhance vocal learning. We tested this hypothesis by pairing appropriate, colour-realistic, high frame-rate videos of a singing adult male zebra finch tutor with song playbacks and presenting these stimuli to juvenile zebra finches (Taeniopygia guttata). Juveniles exposed to song playbacks combined with video presentation of a singing bird approached the stimulus more often and spent more time close to it than juveniles exposed to audio playback only or audio playback combined with pixelated and time-reversed videos. However, higher engagement with the realistic audio–visual stimuli was not predictive of better song learning. Thus, although multimodality increased stimulus engagement and biologically relevant video content was more salient than colour and movement equivalent videos, the higher engagement with the realistic audio–visual stimuli did not lead to enhanced vocal learning. Whether the lack of three-dimensionality of a video tutor and/or the lack of meaningful social interaction make them less suitable for facilitating song learning than audio–visual exposure to a live tutor remains to be tested.

scholarly journals Song preferences predict the quality of vocal learning in zebra finches

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.

scholarly journals Blocking neuroestrogen synthesis modifies neural representations of learned song without altering vocal imitation accuracy in developing songbirds

2019 ◽  
Author(s):  
Daniel M. Vahaba ◽  
Amelia Hecsh ◽  
Luke Remage-Healey
Keyword(s):  
Memory Consolidation ◽  
Temporal Cortex ◽  
Vocal Learning ◽  
Song Learning ◽  
Auditory Memory ◽  
Vocal Imitation ◽  
Neural Representations ◽  
Estrogen Synthesis ◽  
Auditory Experience ◽  
Caudomedial Nidopallium

ABSTRACTBirdsong, like human speech, is learned early in life by first memorizing an auditory model. Once memorized, birds compare their own burgeoning vocalizations to their auditory memory, and adjust their song to match the model. While much is known about this latter part of vocal learning, less is known about how initial auditory experiences are formed and consolidated. In both adults and developing songbirds, there is strong evidence suggesting the caudomedial nidopallium (NCM), a higher order auditory forebrain area, is the site of auditory memory consolidation. However, the mechanisms that facilitate this consolidation are poorly understood. One likely mechanism is 17β-estradiol (E2), which is associated with speech-language development and disorders in humans, and is abundant in both mammalian temporal cortex and songbird NCM. Circulating E2 is also elevated during the auditory memory phase, and in NCM immediately after song learning sessions, suggesting it functions to encode recent auditory experience. Therefore, we tested a role for E2 production in auditory memory consolidation during development using a comprehensive set of investigations to ask this question at the level of neuroanatomy, neurophysiology, and behavior. Our results demonstrate that while systemic estrogen synthesis blockade regulates juvenile song production, inhibiting E2 synthesis locally within NCM does not adversely affect song learning outcomes. Surprisingly, early life E2 manipulations in NCM modify the neural representations of birds’ own song and the model tutor song in both NCM and a downstream sensorimotor nucleus (HVC). Further, we show that the capacity to synthesize neuroestrogens remains high throughout development alongside substantial changes in NCM cell density across age. Taken together, these findings suggest that E2 plays a multifaceted role during development, and demonstrate that contrary to prediction, unilateral post-training estrogen synthesis blockade in the auditory cortex does not negatively impact vocal learning. Acute downregulation of neuroestrogens are therefore likely permissive for juvenile auditory memorization, while neuroestrogen synthesis influences communication production and representation in adulthood.

scholarly journals Dynamic gene expression in the song system of zebra finches during the song learning period

2015 ◽  
Vol 75 (12) ◽  
pp. 1315-1338 ◽  
Author(s):  
Christopher R. Olson ◽  
Lisa K. Hodges ◽  
Claudio V. Mello
Keyword(s):  
Gene Expression ◽  
Song Learning ◽  
Zebra Finches ◽  
Song System

scholarly journals A subcortical circuit linking the cerebellum to the basal ganglia engaged in vocal learning

2017 ◽  
Author(s):  
Ludivine Pidoux ◽  
Pascale Leblanc ◽  
Arthur Leblois
Keyword(s):  
Basal Ganglia ◽  
Vocal Learning ◽  
Song Learning ◽  
Sensorimotor Learning ◽  
Zebra Finches ◽  
Subcortical Structures ◽  
Song Production ◽  
Cerebellar Lesions ◽  
Avian Song

AbstractSpeech is a complex sensorimotor skill, and vocal learning involves both the basal ganglia and the cerebellum. These subcortical structures interact indirectly through their respective loops with thalamo-cortical and brainstem networks, and directly via subcortical pathways, but the role of their interaction during sensorimotor learning remains undetermined. While songbirds and their song-dedicated basal ganglia-thalamo-cortical circuitry offer a unique opportunity to study subcortical circuits involved in vocal learning, the cerebellar contribution to avian song learning remains unknown. We demonstrate that the cerebellum provides a strong input to the song-related basal ganglia nucleus in zebra finches. Cerebellar signals are transmitted to the basal ganglia via a disynaptic connection through the thalamus and then conveyed to their cortical target and to the premotor nucleus controlling song production. Finally, cerebellar lesions impair juvenile song learning, opening new opportunities to investigate how subcortical interactions between the cerebellum and basal ganglia contribute to sensorimotor learning.

Sensorimotor Nucleus NIf Is Necessary for Auditory Processing But Not Vocal Motor Output in the Avian Song System

2005 ◽  
Vol 93 (4) ◽  
pp. 2157-2166 ◽  
Author(s):  
Jessica A. Cardin ◽  
Jonathan N. Raksin ◽  
Marc F. Schmidt
Keyword(s):  
Auditory Processing ◽  
Sensorimotor Integration ◽  
Motor Behavior ◽  
Motor Output ◽  
Zebra Finches ◽  
Auditory Input ◽  
Song System ◽  
Song Production ◽  
Avian Song

Sensorimotor integration in the avian song system is crucial for both learning and maintenance of song, a vocal motor behavior. Although a number of song system areas demonstrate both sensory and motor characteristics, their exact roles in auditory and premotor processing are unclear. In particular, it is unknown whether input from the forebrain nucleus interface of the nidopallium (NIf), which exhibits both sensory and premotor activity, is necessary for both auditory and premotor processing in its target, HVC. Here we show that bilateral NIf lesions result in long-term loss of HVC auditory activity but do not impair song production. NIf is thus a major source of auditory input to HVC, but an intact NIf is not necessary for motor output in adult zebra finches.

scholarly journals Estrogen and sex-dependent loss of the vocal learning system in female zebra finches

2021 ◽  
Vol 129 ◽  
pp. 104911
Author(s):  
Ha Na Choe ◽  
Jeevan Tewari ◽  
Kevin W. Zhu ◽  
Matthew Davenport ◽  
Hiroaki Matsunami ◽  
...  
Keyword(s):  
Vocal Learning ◽  
Learning System ◽  
Zebra Finches

scholarly journals A subcortical circuit linking the cerebellum to the basal ganglia engaged in vocal learning

eLife ◽  
2018 ◽  
Vol 7 ◽  
Author(s):  
Ludivine Pidoux ◽  
Pascale Le Blanc ◽  
Carole Levenes ◽  
Arthur Leblois
Keyword(s):  
Basal Ganglia ◽  
Vocal Learning ◽  
Song Learning ◽  
Sensorimotor Learning ◽  
Zebra Finches ◽  
Subcortical Structures ◽  
Song Production ◽  
Cerebellar Lesions ◽  
Avian Song

Speech is a complex sensorimotor skill, and vocal learning involves both the basal ganglia and the cerebellum. These subcortical structures interact indirectly through their respective loops with thalamo-cortical and brainstem networks, and directly via subcortical pathways, but the role of their interaction during sensorimotor learning remains undetermined. While songbirds and their song-dedicated basal ganglia-thalamo-cortical circuitry offer a unique opportunity to study subcortical circuits involved in vocal learning, the cerebellar contribution to avian song learning remains unknown. We demonstrate that the cerebellum provides a strong input to the song-related basal ganglia nucleus in zebra finches. Cerebellar signals are transmitted to the basal ganglia via a disynaptic connection through the thalamus and then conveyed to their cortical target and to the premotor nucleus controlling song production. Finally, cerebellar lesions impair juvenile song learning, opening new opportunities to investigate how subcortical interactions between the cerebellum and basal ganglia contribute to sensorimotor learning.

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