Projection neurons within a vocal motor pathway are born during song learning in zebra finches

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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Parvalbumin-positive projection neurons characterise the vocal premotor pathway in male, but not female, zebra finches

Brain Research ◽

10.1016/s0006-8993(01)02938-9 ◽

2001 ◽

Vol 917 (2) ◽

pp. 235-252 ◽

Cited By ~ 33

Author(s):

J Martin Wild ◽

Matthew N Williams ◽

Roderick A Suthers

Keyword(s):

Projection Neurons ◽

Zebra Finches ◽

Positive Projection

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The influences of visual and vocal interaction on song learning in Zebra finches

Animal Behaviour ◽

10.1016/0003-3472(89)90097-3 ◽

1989 ◽

Vol 37 ◽

pp. 507-508 ◽

Cited By ~ 82

Author(s):

Lucy A. Eales

Keyword(s):

Song Learning ◽

Zebra Finches

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Sexually dimorphic SCAMP1 expression in the forebrain motor pathway for song production of juvenile zebra finches

Developmental Neurobiology ◽

10.1002/dneu.20354 ◽

2007 ◽

Vol 67 (4) ◽

pp. 474-482 ◽

Cited By ~ 14

Author(s):

Yu Ping Tang ◽

Camilla Peabody ◽

Michelle L. Tomaszycki ◽

Juli Wade

Keyword(s):

Sexually Dimorphic ◽

Zebra Finches ◽

Motor Pathway ◽

Song Production

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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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Dopamine Modulates Excitatory Synaptic Transmission by Activating Presynaptic D1-like Dopamine Receptors in the RA Projection Neurons of Zebra Finches

Frontiers in Cellular Neuroscience ◽

10.3389/fncel.2020.00126 ◽

2020 ◽

Vol 14 ◽

Author(s):

Songhua Wang ◽

Shaoyi Liu ◽

Qingqin Wang ◽

Yalun Sun ◽

Lihua Yao ◽

...

Keyword(s):

Synaptic Transmission ◽

Dopamine Receptors ◽

Excitatory Synaptic Transmission ◽

Projection Neurons ◽

Zebra Finches

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Noradrenergic and GABAB Receptor Activation Differentially Modulate Inputs to the Premotor Nucleus RA in Zebra Finches

Journal of Neurophysiology ◽

10.1152/jn.01212.2007 ◽

2008 ◽

Vol 100 (1) ◽

pp. 8-18 ◽

Cited By ~ 22

Author(s):

Max Sizemore ◽

David J. Perkel

Keyword(s):

Gabab Receptor ◽

Cell Voltage ◽

Receptor Activation ◽

Social Contexts ◽

Excitatory Input ◽

Song Learning ◽

Zebra Finches ◽

Proper Name ◽

Magnocellular Nucleus

Neuromodulators can rapidly modify neural circuits, altering behavior. Songbirds provide an excellent system for studying the role of neuromodulation in modifying circuits that underlie behavior because song learning and production are mediated by a discrete set of interconnected nuclei. We examined the neuromodulatory effects of noradrenergic and GABAB receptor activation on synaptic inputs to the premotor robust nucleus of the arcopallium (RA) in zebra finches using whole cell voltage-clamp recording in vitro. In adults, norepinephrine strongly reduced input from the lateral magnocellular nucleus of the anterior nidopallium (LMAN) but only slightly reduced the input from nucleus HVC (proper name), the excitatory input from axon collaterals of other RA neurons, and input from GABAergic interneurons. The effect of norepinephrine was mimicked by the α2 adrenoceptor agonist UK14,304 and blocked by the α2 antagonist yohimbine. Conversely, the GABAB receptor agonist baclofen strongly decreased HVC, collateral, and GABAergic inputs to RA neurons while causing little reduction in the LMAN input. In juveniles undergoing song learning, norepinephrine reduced the LMAN input, caused only a small reduction in the HVC input, and greatly reduced the collateral and GABAergic inputs. Baclofen caused similar results in juvenile and adult birds, reducing HVC, collateral, and GABAergic inputs significantly more than the LMAN input. Significant increases in paired-pulse ratio accompanied all reductions in synaptic transmission, suggesting a presynaptic locus. The reduction in the LMAN input by norepinephrine may be important for mediating changes in song elicited by different social contexts and is well-placed to play a role in song learning.

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