Elsevier

Current Opinion in Neurobiology

Volume 64, October 2020, Pages 119-126
Current Opinion in Neurobiology

Network dynamics underlie learning and performance of birdsong

https://doi.org/10.1016/j.conb.2020.04.004Get rights and content

Highlights

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    Striking parallels between the developmental learning of human speech and birdsong suggest a deep conservation of brain function underlies the capacity for vocal imitation.

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    In juvenile zebra finches, an auditory memory of adult vocal sounds is encoded within the premotor architecture of the forebrain network that controls song.

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    Dual premotor pathways control the sensorimotor acquisition of song, one of which includes the basal ganglia, where auditory feedback and dopamine-driven ‘actor-critic’ functionality guides vocal output toward the auditory memory of adult vocal sounds.

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    Given the complexity of the overall network required for juveniles to learn song, a surprisingly small portion of the network is needed for adults to recite it.

Understanding the sensorimotor control of the endless variety of human speech patterns stands as one of the apex problems in neuroscience. The capacity to learn – through imitation – to rapidly sequence vocal sounds in meaningful patterns is clearly one of the most derived of human behavioral traits. Selection pressure produced an analogous capacity in numerous species of vocal-learning birds, and due to an increasing appreciation for the cognitive and computational flexibility of avian cortex and basal ganglia, a general understanding of the forebrain network that supports the learning and production of birdsong is beginning to emerge. Here, we review recent advances in experimental studies of the zebra finch (Taeniopygia guttata), which offer new insights into the network dynamics that support this surprising analogue of human speech learning and production.

Section snippets

Auditory learning in a ‘motor’ pathway

Although only male zebra finches learn to produce song, juveniles of both sexes experience auditory learning, forming an auditory memory of the song of the adult male ‘tutor’ that raises them. For juvenile males, the auditory memory of tutor song serves as an internal reference – accessed via auditory feedback – to guide the sensorimotor learning of song. To understand how auditory memory is encoded, a first step is to characterize the neural loci and pathways involved in memory formation.

While

Sensorimotor learning – distinct neural pathways for variation, acquisition, and evaluation of song

Three behavioral stages characterize sensorimotor learning in males – subsong, plastic song, and crystallized adult song. Figure 1b shows the configuration of the network at the onset of juvenile subsong, when the activity of vocal motor cortex (RA) is dominated by input from the Anterior Forebrain Pathway (AFP, green). AFP premotor activity, conveyed to RA from LMANcore, results in rambling vocal sequences that resemble infant babbling [17]. By driving the vocal organ throughout its dynamic

Adult song – a small portion of the forebrain network required to learn song is needed to recite it

The adult songs of male zebra finches contain 3–5 spectrally distinct syllables produced in a serial order. Songs are produced several hundred times per day in a variety of social settings, the most salient being female-directed singing for the purpose of courtship. One of the fascinating aspects of adult song is that only a small portion of the forebrain sensorimotor network needed to learn the song pattern is required to recite it (magenta in Figure 1c). Remarkably, recent work suggests that

Conflict of interest statement

Nothing declared.

CRediT authorship contribution statement

Richard Bertram: Conceptualization, Writing - original draft. Richard L Hyson: Conceptualization, Writing - original draft, Validation. Amanda J Brunick: Writing - review & editing. Diana Flores: Writing - review & editing, Investigation. Frank Johnson: Conceptualization, Writing - original draft.

Acknowledgements

The Bertram, Hyson, and Johnson laboratories acknowledge generous support from the National Science Foundation (IOS‐1456965, IOS-1656360).

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