The Role of Auditory Experience in the Formation of Neural Circuits Underlying Vocal Learning in Zebra Finches

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

10.1101/198317 ◽

2017 ◽

Cited By ~ 1

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.

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

eLife ◽

10.7554/elife.32167 ◽

2018 ◽

Vol 7 ◽

Cited By ~ 13

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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Vocal learning in songbirds: the role of syllable order in song recognition

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2020.0248 ◽

2021 ◽

Vol 376 (1836) ◽

Cited By ~ 2

Author(s):

Carien Mol ◽

Johan J. Bolhuis ◽

Sanne Moorman

Keyword(s):

Vocal Learning ◽

Serial Order ◽

Song Learning ◽

Zebra Finches ◽

Speech Acquisition ◽

Human Infants ◽

Song Recognition ◽

First Results ◽

Sequential Information

Songbird vocal learning has interesting behavioural and neural parallels with speech acquisition in human infants. Zebra finch males sing one unique song that they imitate from conspecific males, and both sexes learn to recognize their father's song. Although males copy the stereotyped syllable sequence of their father's song, the role of sequential information in recognition remains unclear. Here, we investigated father's song recognition after changing the serial order of syllables (switching the middle syllables, first and last syllables, or playing all syllables in inverse order). Behavioural approach and call responses of adult male and female zebra finches to their father's versus unfamiliar songs in playback tests demonstrated significant recognition of father's song with all syllable-order manipulations. We then measured behavioural responses to normal versus inversed-order father's song. In line with our first results, the subjects did not differentiate between the two. Interestingly, when males' strength of song learning was taken into account, we found a significant correlation between song imitation scores and the approach responses to the father's song. These findings suggest that syllable sequence is not essential for recognition of father's song in zebra finches, but that it does affect responsiveness of males in proportion to the strength of vocal learning. This article is part of the theme issue ‘Vocal learning in animals and humans’.

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Corticostriatal control of defense behavior in mice induced by auditory looming cues

Nature Communications ◽

10.1038/s41467-021-21248-7 ◽

2021 ◽

Vol 12 (1) ◽

Author(s):

Zhong Li ◽

Jin-Xing Wei ◽

Guang-Wei Zhang ◽

Junxiang J. Huang ◽

Brian Zingg ◽

...

Keyword(s):

Essential Role ◽

Neural Circuits ◽

Temporal Dynamics ◽

Defense Behavior ◽

Innate Defense ◽

Sensory Inputs ◽

Corticostriatal Projections ◽

Behavioral Transition ◽

Auditory Looming

AbstractAnimals exhibit innate defense behaviors in response to approaching threats cued by the dynamics of sensory inputs of various modalities. The underlying neural circuits have been mostly studied in the visual system, but remain unclear for other modalities. Here, by utilizing sounds with increasing (vs. decreasing) loudness to mimic looming (vs. receding) objects, we find that looming sounds elicit stereotypical sequential defensive reactions: freezing followed by flight. Both behaviors require the activity of auditory cortex, in particular the sustained type of responses, but are differentially mediated by corticostriatal projections primarily innervating D2 neurons in the tail of the striatum and corticocollicular projections to the superior colliculus, respectively. The behavioral transition from freezing to flight can be attributed to the differential temporal dynamics of the striatal and collicular neurons in their responses to looming sound stimuli. Our results reveal an essential role of the striatum in the innate defense control.

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

Animal Cognition ◽

10.1007/s10071-021-01547-8 ◽

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.

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Inhibition protects acquired song segments during vocal learning in zebra finches

Science ◽

10.1126/science.aad3023 ◽

2016 ◽

Vol 351 (6270) ◽

pp. 267-271 ◽

Cited By ~ 72

Author(s):

D. Vallentin ◽

G. Kosche ◽

D. Lipkind ◽

M. A. Long

Keyword(s):

Vocal Learning ◽

Zebra Finches

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Differential developmental changes in cortical representations of auditory-vocal stimuli in songbirds

Journal of Neurophysiology ◽

10.1152/jn.00714.2018 ◽

2019 ◽

Vol 121 (2) ◽

pp. 530-548 ◽

Cited By ~ 1

Author(s):

Rachel C. Yuan ◽

Sarah W. Bottjer

Keyword(s):

Motor Skill ◽

Motor Pattern ◽

Vocal Learning ◽

Skill Learning ◽

Neural Representation ◽

Cortical Region ◽

Motor Skill Learning ◽

Zebra Finches ◽

Cortical Regions ◽

Song Playback

Procedural skill learning requires iterative comparisons between feedback of self-generated motor output and a goal sensorimotor pattern. In juvenile songbirds, neural representations of both self-generated behaviors (each bird’s own immature song) and the goal motor pattern (each bird’s adult tutor song) are essential for vocal learning, yet little is known about how these behaviorally relevant stimuli are encoded. We made extracellular recordings during song playback in anesthetized juvenile and adult zebra finches ( Taeniopygia guttata) in adjacent cortical regions RA (robust nucleus of the arcopallium), AId (dorsal intermediate arcopallium), and RA cup, each of which is well situated to integrate auditory-vocal information: RA is a motor cortical region that drives vocal output, AId is an adjoining cortical region whose projections converge with basal ganglia loops for song learning in the dorsal thalamus, and RA cup surrounds RA and receives inputs from primary and secondary auditory cortex. We found strong developmental differences in neural selectivity within RA, but not in AId or RA cup. Juvenile RA neurons were broadly responsive to multiple songs but preferred juvenile over adult vocal sounds; in addition, spiking responses lacked consistent temporal patterning. By adulthood, RA neurons responded most strongly to each bird’s own song with precisely timed spiking activity. In contrast, we observed a complete lack of song responsivity in both juvenile and adult AId, even though this region receives song-responsive inputs. A surprisingly large proportion of sites in RA cup of both juveniles and adults did not respond to song playback, and responsive sites showed little evidence of song selectivity. NEW & NOTEWORTHY Motor skill learning entails changes in selectivity for behaviorally relevant stimuli across cortical regions, yet the neural representation of these stimuli remains understudied. We investigated how information important for vocal learning in zebra finches is represented in regions analogous to infragranular layers of motor and auditory cortices during vs. after the developmentally regulated learning period. The results provide insight into how neurons in higher level stages of cortical processing represent stimuli important for motor skill learning.

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Role of the medulla oblongata in normal and high arterial blood pressure regulation: the contribution of Escola Paulista de Medicina - UNIFESP

Anais da Academia Brasileira de Ciências ◽

10.1590/s0001-37652009000300021 ◽

2009 ◽

Vol 81 (3) ◽

pp. 589-603 ◽

Cited By ~ 3

Author(s):

Sergio L. Cravo ◽

Ruy R. Campos ◽

Eduardo Colombari ◽

Mônica A. Sato ◽

Cássia M. Bergamaschi ◽

...

Keyword(s):

Blood Pressure ◽

Arterial Blood Pressure ◽

Medulla Oblongata ◽

Neural Circuits ◽

Ventrolateral Medulla ◽

Vasomotor Tone ◽

Arterial Blood ◽

Pathological Conditions ◽

De Medicina

Several forms of experimental evidence gathered in the last 37 years have unequivocally established that the medulla oblongata harbors the main neural circuits responsible for generating the vasomotor tone and regulating arterial blood pressure. Our current understanding of this circuitry derives mainly from the studies of Pedro Guertzenstein, a former student who became Professor of Physiology at UNIFESP later, and his colleagues. In this review, we have summarized the main findings as well as our collaboration to a further understanding of the ventrolateral medulla and the control of arterial blood pressure under normal and pathological conditions.

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FoxP2 isoforms delineate spatiotemporal transcriptional networks for vocal learning in the zebra finch

eLife ◽

10.7554/elife.30649 ◽

2018 ◽

Vol 7 ◽

Cited By ~ 8

Author(s):

Zachary Daniel Burkett ◽

Nancy F Day ◽

Todd Haswell Kimball ◽

Caitlin M Aamodt ◽

Jonathan B Heston ◽

...

Keyword(s):

Vocal Learning ◽

Transcriptional Networks ◽

Zebra Finches ◽

Rna Seq ◽

Song Development ◽

Gene Modules ◽

Area X ◽

First Time ◽

Vocal Variability ◽

Coexpression Network Analysis

Human speech is one of the few examples of vocal learning among mammals yet ~half of avian species exhibit this ability. Its neurogenetic basis is largely unknown beyond a shared requirement for FoxP2 in both humans and zebra finches. We manipulated FoxP2 isoforms in Area X, a song-specific region of the avian striatopallidum analogous to human anterior striatum, during a critical period for song development. We delineate, for the first time, unique contributions of each isoform to vocal learning. Weighted gene coexpression network analysis of RNA-seq data revealed gene modules correlated to singing, learning, or vocal variability. Coexpression related to singing was found in juvenile and adult Area X whereas coexpression correlated to learning was unique to juveniles. The confluence of learning and singing coexpression in juvenile Area X may underscore molecular processes that drive vocal learning in young zebra finches and, by analogy, humans.

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