Female Social Feedback Reveals Non-imitative Mechanisms of Vocal Learning in Zebra Finches

Carouso-Peck, Samantha; Goldstein, Michael H.

doi:10.1016/j.cub.2018.12.026

Cited by 77 publications

(67 citation statements)

References 36 publications

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“…Importantly, successful song learning also requires multiple factors beyond simply matching vocal output to an auditory goal -for instance, vocal learning in juvenile zebra finches that are tutored with only passive playback of the tutor song is severely impaired, whereas pairing auditory tutoring with a visual model of an adult zebra finch enhances learning (Derégnaucourt et al, 2013;Ljubičić et al, 2016). Moreover, visual cues provided during singing, such as wing strokes or fluff-ups from adult females, provide feedback that can influence juvenile vocal learning (West and King, 1988;King et al, 2005;Carouso-Peck and Goldstein, 2019). Multi-modal inputs from dNCL and singing-related inputs from LMAN may converge in AId, integrating important non-vocal and vocal elements of courtship song behavior that must be learned during a sensitive period of development.…”

Section: Aid Is Uniquely Situated To Mediate Learning and Performancementioning

confidence: 99%

“…Vocal learning in songbirds entails integration of social cues and visual, auditory, and somatosensory feedback information to guide refinement of variable juvenile babbling into stereotyped song and thus serves as a powerful model for investigating goal-directed sensorimotor learning (Price, 1979;West and King, 1988;Eales, 1989;Mann et al, 1991;Mann and Slater, 1995;King et al, 2005;Derégnaucourt et al, 2013;Chen et al, 2016;Ljubičić et al, 2016;Carouso-Peck and Goldstein, 2019). In songbirds, the cortical region AId lies within an area that has been considered to be analogous to motor cortex in mammals: akin to infragranular layers of mammalian motor cortex, AId receives inputs that process multi-modal sensory information via dNCL (dorsal caudolateral nidopallium) as well as information from corticobasal ganglia circuitry that is dedicated to vocal learning, and in turn makes a variety of projections that give rise to feedforward and feedback pathways through subcortical and brainstem regions ( Fig.…”

Section: Introductionmentioning

confidence: 99%

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Multi-dimensional tuning in motor cortical neurons during active behavior

Yuan

Bottjer

2020

Preprint

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A region within songbird cortex, AId (dorsal intermediate arcopallium), is functionally analogous to motor cortex in mammals and has been implicated in vocal learning during development. AId thus serves as a powerful model for investigating motor cortical contributions to developmental skill learning. We made extracellular recordings in AId of freely behaving juvenile zebra finches and evaluated neural activity during diverse motor behaviors throughout entire recording sessions, including song production as well as hopping, pecking, preening, fluffups, beak interactions with cage objects, scratching, and stretching. A large population of single neurons showed significant modulation of activity during singing relative to quiescence. In addition, AId neurons demonstrated heterogeneous response patterns that were evoked during multiple movements, with single neurons often demonstrating excitation during one movement type and suppression during another. Lesions of AId do not disrupt vocal motor output or impair generic movements, suggesting that the responses observed during active behavior do not reflect direct motor drive. Consistent with this idea, we found that some AId neurons showed differential activity during pecking movements depending on the context in which pecks occurred, suggesting that AId circuitry encodes diverse inputs beyond generic motor parameters.Moreover, we found evidence of neurons that did not respond during discrete movements but were nonetheless modulated during active behavioral states compared to quiescence. Taken together, our results support the idea that AId neurons are involved in sensorimotor integration of external sensory inputs and/or internal feedback cues to help modulate goal-directed behaviors. SIGNIFICANCE STATEMENTMotor cortex across taxa receives highly integrated, multi-modal information and has been implicated in both execution and acquisition of complex motor skills, yet studies of motor cortex typically employ restricted behavioral paradigms that target select movement parameters, preventing wider assessment of the diverse sensorimotor factors that can affect motor cortical activity. Recording in AId of freely behaving juvenile songbirds that are actively engaged in sensorimotor learning offers unique advantages for elucidating the functional role of motor cortical neurons. The results demonstrate that a diverse array of factors modulate motor cortical activity and lay important groundwork for future investigations of how multi-modal information is integrated in motor cortical regions to contribute to learning and execution of complex motor skills.3

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Section: Aid Is Uniquely Situated To Mediate Learning and Performancementioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Multi-dimensional tuning in motor cortical neurons during active behavior

Yuan

Bottjer

2020

Preprint

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“…At the end of ontogeny (or seasonally at the end of each plastic period) song features become highly stereotyped (crystallization). More recent behavioral and neurobiological evidence suggests that social interactions also shape how vocal production proceeds during the sensorimotor period (West and King, ; Fehér et al , ; Caruso‐Peck and Goldstein, ), thus expanding the template model for vocal ontogeny (Soha, ).…”

Section: Introductionmentioning

confidence: 99%

Song Feature Specific Analysis of Isolate Song Reveals Interspecific Variation in Learned Components

Love

Goller

2019

Developmental Neurobiology

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Studies of avian vocal development without exposure to conspecific song have been conducted in many passerine species, and the resultant isolate song is often interpreted to represent an expression of the genetic code for conspecific song. There is wide recognition that vocal learning exists in oscine songbirds, but vocal learning has only been thoroughly investigated in a few model species, resulting in a narrow view of birdsong learning. By extracting acoustic signals from published spectrograms, we have reexamined the findings of isolate studies with a universally applicable semi‐automated quantitative analysis regimen. When song features were analyzed in light of three different production aspects (respiratory, syringeal, and central programming of sequence), all three show marked interspecific variability in how close isolate song features are to normal. This implies that song learning mechanisms are more variable than is commonly recognized. Our results suggest that the interspecific variation shows no readily observable pattern reflecting phylogeny, which has implications for understanding the mechanisms behind the evolution of avian vocal communication. We emphasize that song learning in passerines provides an excellent opportunity to investigate the evolution of a complex, plastic trait from a phylogenetic perspective.

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“…These results add to a small but growing understanding of tutor and pupil behavior during song learning. To our knowledge, these results are novel given the limited studies that explicitly quantify pupil behavior during tutoring (lab-reared, or otherwise) (Chen et al, 2016;Carouso-Peck and Goldstein, 2019). Juveniles are thought to preferentially learn from, and as an extension, imitate, more aggressive males who are mated or feed them early in development (Zann, 1996).…”

Section: Brain Estrogen Synthesis and Song Production In Developing Smentioning

confidence: 96%

Blocking neuroestrogen synthesis modifies neural representations of learned song without altering vocal imitation accuracy in developing songbirds

Hecsh

Remage‐Healey

2019

Preprint

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Birdsong, like human speech, is learned early in life by first memorizing an auditory model. Once memorized, birds compare their own burgeoning vocalizations to their auditory memory, and adjust their song to match the model. While much is known about this latter part of vocal learning, less is known about how initial auditory experiences are formed and consolidated. In both adults and developing songbirds, there is strong evidence suggesting the caudomedial nidopallium (NCM), a higher order auditory forebrain area, is the site of auditory memory consolidation. However, the mechanisms that facilitate this consolidation are poorly understood. One likely mechanism is 17β-estradiol (E2), which is associated with speech-language development and disorders in humans, and is abundant in both mammalian temporal cortex and songbird NCM. Circulating E2 is also elevated during the auditory memory phase, and in NCM immediately after song learning sessions, suggesting it functions to encode recent auditory experience. Therefore, we tested a role for E2 production in auditory memory consolidation during development using a comprehensive set of investigations to ask this question at the level of neuroanatomy, neurophysiology, and behavior. Our results demonstrate that while systemic estrogen synthesis blockade regulates juvenile song production, inhibiting E2 synthesis locally within NCM does not adversely affect song learning outcomes. Surprisingly, early life E2 manipulations in NCM modify the neural representations of birds' own song and the model tutor song in both NCM and a downstream sensorimotor nucleus (HVC). Further, we show that the capacity to synthesize neuroestrogens remains high throughout development alongside substantial changes in NCM cell density across age. Taken together, these findings suggest that E2 plays a multifaceted role during development, and demonstrate that contrary to prediction, unilateral post-training estrogen synthesis blockade in the auditory cortex does not negatively impact vocal learning. Acute downregulation of neuroestrogens are therefore likely permissive for juvenile auditory memorization, while neuroestrogen synthesis influences communication production and representation in adulthood. AntibodiesAntibodies and dilutions for aromatase and parvalbumin were identical to those used in Ikeda et al. (2017). Briefly, we used a polyclonal anti-aromatase primary antibody raised in rabbit (1:2,000; a generous gift from Dr. Colin Saldanha), and a monoclonal anti-parvalbumin primary antibody raised in mouse (1:10,000; Millipore MAB1572; RRID: AB_2174013). Secondary antibodies included goat antirabbit Alexa 488 (1:500; Thermo Fisher Scientific Inc.), and goat anti-mouse Alexa 647 (1:100; Thermo Fisher Scientific Inc.). ProcedureBrain sections were first manually washed 3 x in 0.1 M PB, followed by 3 x 15-minute washes in 0.1 M PB on a plate shaker, followed by a 2-hour incubation at room temperature with 10% normal goat serum (Vector) in 0.3 % PBT. Tissue was then transferred to a 10% normal goat...

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Female Social Feedback Reveals Non-imitative Mechanisms of Vocal Learning in Zebra Finches

Cited by 77 publications

References 36 publications

Multi-dimensional tuning in motor cortical neurons during active behavior

Multi-dimensional tuning in motor cortical neurons during active behavior

Song Feature Specific Analysis of Isolate Song Reveals Interspecific Variation in Learned Components

Blocking neuroestrogen synthesis modifies neural representations of learned song without altering vocal imitation accuracy in developing songbirds

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