Decision letter: A neural circuit mechanism for regulating vocal variability 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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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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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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Inhibition within a premotor circuit controls the timing of vocal turn-taking in zebra finches

Nature Communications ◽

10.1038/s41467-019-13938-0 ◽

2020 ◽

Vol 11 (1) ◽

Author(s):

Jonathan I. Benichov ◽

Daniela Vallentin

Keyword(s):

Neural Circuit ◽

Zebra Finches ◽

Vocal Responses ◽

Local Inhibition ◽

Impaired Ability ◽

Neuron Activation ◽

Electrophysiological Recordings ◽

Vocal Signals ◽

Turn Taking ◽

Pharmacological Manipulations

AbstractVocal turn-taking is a fundamental organizing principle of human conversation but the neural circuit mechanisms that structure coordinated vocal interactions are unknown. The ability to exchange vocalizations in an alternating fashion is also exhibited by other species, including zebra finches. With a combination of behavioral testing, electrophysiological recordings, and pharmacological manipulations we demonstrate that activity within a cortical premotor nucleus orchestrates the timing of calls in socially interacting zebra finches. Within this circuit, local inhibition precedes premotor neuron activation associated with calling. Blocking inhibition results in faster vocal responses as well as an impaired ability to flexibly avoid overlapping with a partner. These results support a working model in which premotor inhibition regulates context-dependent timing of vocalizations and enables the precise interleaving of vocal signals during turn-taking.

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

Nature ◽

10.1038/334149a0 ◽

1988 ◽

Vol 334 (6178) ◽

pp. 149-151 ◽

Cited By ~ 133

Author(s):

Kathy W. Nordeen ◽

Ernest J. Nordeen

Keyword(s):

Song Learning ◽

Projection Neurons ◽

Zebra Finches ◽

Motor Pathway

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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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