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

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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Conjunction of Vocal Production and Perception Regulates Expression of the Immediate Early Gene ZENK in a Novel Cortical Region of Songbirds

Journal of Neurophysiology ◽

10.1152/jn.00869.2009 ◽

2010 ◽

Vol 103 (4) ◽

pp. 1833-1842 ◽

Cited By ~ 6

Author(s):

Sarah W. Bottjer ◽

Tanya L. Alderete ◽

Daniel Chang

Keyword(s):

Vocal Learning ◽

Early Gene ◽

Vocal Behavior ◽

Projection Neurons ◽

Cortical Region ◽

Developmentally Regulated ◽

Vocal Production ◽

Cortical Nucleus ◽

Magnocellular Nucleus ◽

Low Levels

The cortical nucleus LMAN (lateral magnocellular nucleus of the anterior nidopallium) provides the output of a basal ganglia pathway that is necessary for acquisition of learned vocal behavior during development in songbirds. LMAN is composed of two subregions, a core and a surrounding shell, that give rise to independent pathways that traverse the forebrain in parallel. The LMANshell pathway forms a recurrent loop that includes a cortical region, the dorsal region of the caudolateral nidopallium (dNCL), hitherto unknown to be involved with learned vocal behavior. Here we show that vocal production strongly induces the IEG product ZENK in dNCL of zebra finches. Hearing tutor song while singing is more effective at inducing expression in dNCL of juvenile birds during the auditory–motor integration stage of vocal learning than is hearing conspecific song. In contrast, hearing conspecific song is relatively more effective at inducing expression in adult birds, regardless of whether they are producing song. Furthermore, ZENK+ neurons in dNCL include projection neurons that are part of the LMANshell recurrent loop and a high proportion of dNCL projection neurons express ZENK in singing juvenile birds that hear tutor song. Thus juvenile birds that are actively refining their vocal pattern to imitate a tutor song show high levels of ZENK induction in dNCL neurons when they are singing while hearing the song of their tutor and low levels when they hear a novel conspecific. This pattern indicates that dNCL is a novel brain region involved with vocal learning and that its function is developmentally regulated.

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

10.1101/739623 ◽

2019 ◽

Author(s):

Matthew T. Davis ◽

Kathleen E. Grogan ◽

Donna L. Maney

Keyword(s):

Vocal Learning ◽

Social Motivation ◽

Oxytocin Receptor ◽

Lateral Septum ◽

Zebra Finches ◽

Vocal Development ◽

Auditory Forebrain ◽

Oxytocin Receptors ◽

Song Control System ◽

Song Control

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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Regulation of learned vocal behavior by an auditory motor cortical nucleus in juvenile zebra finches

Journal of Neurophysiology ◽

10.1152/jn.01035.2010 ◽

2011 ◽

Vol 106 (1) ◽

pp. 291-300 ◽

Cited By ~ 23

Author(s):

Katja Naie ◽

Richard H. R. Hahnloser

Keyword(s):

Zebra Finch ◽

Brain Area ◽

Primary Afferents ◽

Song Learning ◽

Significant Source ◽

Vocal Behavior ◽

Zebra Finches ◽

Auditory Input ◽

Cortical Nucleus ◽

Song Production

In the process of song learning, songbirds such as the zebra finch shape their initial soft and poorly formed vocalizations (subsong) first into variable plastic songs with a discernable recurring motif and then into highly stereotyped adult songs. A premotor brain area critically involved in plastic and adult song production is the cortical nucleus HVC. One of HVC's primary afferents, the nucleus interface of the nidopallium (NIf), provides a significant source of auditory input to HVC. However, the premotor involvement of NIf has not been extensively studied yet. Here we report that brief and reversible pharmacological inactivation of NIf in juvenile birds leads to transient degradation of plastic song toward subsong, as revealed by spectral and temporal song features. No such song degradation is seen following NIf inactivation in adults. However, in both juveniles and adults NIf inactivation leads to a transient decrease in song stereotypy. Our findings reveal a contribution of NIf to song production in juveniles that agrees with its known role in adults in mediating thalamic drive to downstream vocal motor areas during sleep.

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High plasticity in marmoset monkey vocal development from infancy to adulthood

Science Advances ◽

10.1126/sciadv.abf2938 ◽

2021 ◽

Vol 7 (27) ◽

pp. eabf2938

Author(s):

Yasemin B. Gultekin ◽

David G. C. Hildebrand ◽

Kurt Hammerschmidt ◽

Steffen R. Hage

Keyword(s):

Nonhuman Primates ◽

Vocal Learning ◽

Vocal Behavior ◽

First Year ◽

High Plasticity ◽

Vocal Development ◽

Human Infants ◽

Development Stages ◽

Marmoset Monkey ◽

Physical Maturation

The vocal behavior of human infants undergoes marked changes across their first year while becoming increasingly speech-like. Conversely, vocal development in nonhuman primates has been assumed to be largely predetermined and completed within the first postnatal months. Contradicting this assumption, we found a dichotomy between the development of call features and vocal sequences in marmoset monkeys, suggestive of a role for experience. While changes in call features were related to physical maturation, sequences of and transitions between calls remained flexible until adulthood. As in humans, marmoset vocal behavior developed in stages correlated with motor and social development stages. These findings are evidence for a prolonged phase of plasticity during marmoset vocal development, a crucial primate evolutionary preadaptation for the emergence of vocal learning and speech.

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Traffic noise disrupts vocal development and suppresses immune function

Science Advances ◽

10.1126/sciadv.abe2405 ◽

2021 ◽

Vol 7 (20) ◽

pp. eabe2405

Author(s):

Henrik Brumm ◽

Wolfgang Goymann ◽

Sébastien Derégnaucourt ◽

Nicole Geberzahn ◽

Sue Anne Zollinger

Keyword(s):

Immune Function ◽

Noise Exposure ◽

Traffic Noise ◽

Vocal Learning ◽

Noise Pollution ◽

Experimental Models ◽

Speech Development ◽

Vocal Development ◽

Learning Impairments ◽

Cognitive Deficiencies

Noise pollution has been linked to learning and language deficits in children, but the causal mechanisms connecting noise to cognitive deficiencies remain unclear because experimental models are lacking. Here, we investigated the effects of noise on birdsong learning, the primary animal model for vocal learning and speech development in humans. We found that traffic noise exposure retarded vocal development and led to learning inaccuracies. In addition, noise suppressed immune function during the sensitive learning period, indicating that it is a potent stressor for birds, which is likely to compromise their cognitive functions. Our results provide important insights into the consequences of noise pollution and pave the way for future studies using birdsong as an experimental model for the investigation of noise-induced learning impairments.

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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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