New Insights into the Avian Song System and Neuronal Control of Learned Vocalizations

Murphy, Karagh; Lawley, Koedi S.; Smith, Perry; Prather, Jonathan F.

doi:10.1007/978-3-030-34683-6_3

Cited by 9 publications

(12 citation statements)

References 137 publications

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“…Consequently, it will be important to reveal the degree to which the observed changes in syllable structure, timing, and sequencing are due to specific changes in these populations. In addition, because Area X is part of the circuit that forms an independent input into RA and that includes the lateral magnocellular nucleus of the anterior nidopallium (LMAN) and because manipulations of activity in LMAN can lead to changes to the mean and variability of syllable structure (reviewed in Brainard and Doupe 2013;Murphy et al 2020), it will be important to assess the effects of manipulations of inhibition in HVC in Bengalese finches with lesions of LMAN (e.g., .…”

Section: Discussionmentioning

confidence: 99%

“…Such vocalizations are regulated by activity in a cortical nucleus, HVC (used as a proper name) (Aronov et al 2008;Nottebohm et al 1976). HVC is analogous to the supplementary motor cortex in mammals (Brainard and Doupe 2013;Pfenning et al 2014;Reiner et al 2004;Sakata and Yazaki-Sugiyama 2020), and neurons in HVC encode the motor signals for song production and regulate the moment-by-moment control of spectral and temporal features of song (Ashmore et al 2005;Daliparthi et al 2019;Hahnloser et al 2002;Kosche et al 2015;Lynch et al 2016;Markowitz et al 2015;Murphy et al 2017Murphy et al , 2020Okubo et al 2015;Picardo et al 2016;Prather et al 2008;Wang et al 2008;Woolley et al 2014;Zhang et al 2017). For example, manipulations of temperature in HVC alter song tempo by stretching and compressing the durations of vocal elements ("syllables") and gaps (Andalman et al 2011;Goldin et al 2013;Long and Fee 2008;Zhang et al 2017), and lesions within HVC significantly alter the acoustic structure and sequencing of syllables (Alalawi et al 2019;Aronov et al 2008;Basista et al 2014;Nottebohm et al 1976;Poole et al 2012;.…”

Section: Introductionmentioning

confidence: 99%

“…HVC consists of multiple populations of excitatory projection neurons as well as local inhibitory neurons that impinge on these excitatory neurons (Kornfeld et al 2017;Mooney and Prather 2005;Murphy et al 2020). Theoretical and computational models propose a wide range of functions of inhibition within HVC, ranging from models suggesting that inhibition plays a minor role in song control to models highlighting a central role of inhibition for syllable sequencing and timing (Cannon et al 2015;Gibb et al 2009;Jin et al 2007; Li and Greenside 2006;Long et al 2010;Yildiz and Kiebel 2011).…”

Section: Introductionmentioning

confidence: 99%

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Manipulations of inhibition in cortical circuitry differentially affect spectral and temporal features of Bengalese finch song

Isola

Vochin

Sakata

2020

Journal of Neurophysiology

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The interplay between inhibition and excitation can regulate behavioral expression and control, including the expression of communicative behaviors like birdsong. Computational models postulate varying degrees to which inhibition within vocal motor circuitry influences birdsong, but few studies have tested these models by manipulating inhibition. Here we enhanced and attenuated inhibition in the cortical nucleus HVC (used as proper name) of Bengalese finches ( Lonchura striata var. domestica). Enhancement of inhibition (with muscimol) in HVC dose-dependently reduced the amount of song produced. Infusions of higher concentrations of muscimol caused some birds to produce spectrally degraded songs, whereas infusions of lower doses of muscimol led to the production of relatively normal (nondegraded) songs. However, the spectral and temporal structures of these nondegraded songs were significantly different from songs produced under control conditions. In particular, muscimol infusions decreased the frequency and amplitude of syllables, increased various measures of acoustic entropy, and increased the variability of syllable structure. Muscimol also increased sequence durations and the variability of syllable timing and syllable sequencing. Attenuation of inhibition (with bicuculline) in HVC led to changes to song distinct from and often opposite to enhancing inhibition. For example, in contrast to muscimol, bicuculline infusions increased syllable amplitude, frequency, and duration and decreased the variability of acoustic features. However, like muscimol, bicuculline increased the variability of syllable sequencing. These data highlight the importance of inhibition to the production of stereotyped vocalizations and demonstrate that changes to neural dynamics within cortical circuitry can differentially affect spectral and temporal features of song. NEW & NOTEWORTHY We reveal that manipulations of inhibition in the cortical nucleus HVC affect the structure, timing, and sequencing of syllables in Bengalese finch song. Enhancing and blocking inhibition led to opposite changes to the acoustic structure and timing of vocalizations, but both caused similar changes to vocal sequencing. These data provide support for computational models of song control but also motivate refinement of existing models to account for differential effects on syllable structure, timing, and sequencing.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Manipulations of inhibition in cortical circuitry differentially affect spectral and temporal features of Bengalese finch song

Isola

Vochin

Sakata

2020

Journal of Neurophysiology

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“…Sensory learning serves as the foundation for the sensorimotor learning of many acquired behaviors. For example, the sensorimotor learning of birdsong during development involves comparing one's current vocal performance to a sensory representation of a "target" song; as such, the development of an accurate imitation of a tutor's song requires learning an accurate sensory representation of the tutor's song (14,16,20,22). Because studies in mammals highlight the importance of NE acting within sensory processing areas to sensory learning and plasticity (37,(42)(43)(44)65), we investigated how infusions of NE into the NCM, an auditory processing area implicated in song learning (16,23,66), affects the fidelity of song learning and imitation.…”

Section: Discussionmentioning

confidence: 99%

“…10 and 15-17). Because sensorimotor song learning involves comparing current vocal performance to a sensory representation of the target song, sensory learning serves as the foundation for the sensorimotor learning of song (18)(19)(20)(21)(22). Furthermore, sensorimotor learning occurs over weeks to months, progresses even without the continued presence of a tutor, and can start well after the sensory period closes; consequently, accurate sensory memories formed during sensory learning must persist in order for songbirds to develop accurate imitations of the tutor song (reviewed in Ref.…”

Section: Introductionmentioning

confidence: 99%

Norepinephrine in the avian auditory cortex enhances developmental song learning

Sakata

2021

Journal of Neurophysiology

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Sensory learning during critical periods in development has lasting effects on behavior. Neuromodulators like dopamine and norepinephrine (NE) have been implicated in various forms of sensory learning, but little is known about their contribution to sensory learning during critical periods. Songbirds like the zebra finch communicate with each other using vocal signals (e.g., songs) that are learned during a critical period in development, and the first crucial step in song learning is memorizing the sound of an adult conspecific's (tutor's) song. Here we analyzed the extent to which NE modulates the auditory learning of a tutor's song and the fidelity of song imitation. Specifically, we paired infusions of NE or vehicle into the caudomedial nidopallium (NCM) with brief epochs of song tutoring. We analyzed the effect of NE in juvenile zebra finches that had or had not previously been exposed to song. Regardless of previous exposure to song, juveniles that received NE infusions into NCM during song tutoring produced songs that were more acoustically similar to the tutor song and that incorporated more elements of the tutor song than juveniles with control infusions. These data support the notion that NE can regulate the formation of sensory memories that shape the development of vocal behaviors that are used throughout an organism's life.

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Manipulations of sensory experiences during development reveal mechanisms underlying vocal learning biases in zebra finches

James

Davies

Mori

et al. 2020

Developmental Neurobiology

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Biological predispositions in learning can bias and constrain the cultural evolution of social and 33 communicative behaviors (e.g., speech and birdsong), and lead to the emergence of behavioral and 34 cultural "universals". For example, surveys of laboratory and wild populations of zebra finches 35 (Taeniopygia guttata) document consistent patterning of vocal elements ("syllables") with respect to 36 their acoustic properties (e.g., duration, mean frequency). Furthermore, such universal patterns are 37 also produced by birds that are experimentally tutored with songs containing randomly sequenced 38 syllables ("tutored birds"). Despite extensive demonstrations of learning biases, much remains to be 39 uncovered about the nature of biological predispositions that bias song learning and production in 40 songbirds. Here we examined the degree to which "innate" auditory templates and/or biases in vocal 41 motor production contribute to vocal learning biases and production in zebra finches. Such 42 contributions can be revealed by examining acoustic patterns in the songs of birds raised without 43 sensory exposure to song ("untutored birds") or of birds that are unable to hear from early in 44 development ("early-deafened birds"). We observed that untutored zebra finches and early-deafened 45 zebra finches produce songs with positional variation in some acoustic features (e.g., mean frequency) 46 that resemble universal patterns observed in tutored birds. Similar to tutored birds, early-deafened 47 birds also produced song motifs with alternation in acoustic features across adjacent syllables. That 48 universal acoustic patterns are observed in the songs of both untutored and early-deafened birds 49 highlights the contribution motor production biases to the emergence of universals in culturally 50 transmitted behaviors.

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New Insights into the Avian Song System and Neuronal Control of Learned Vocalizations

Cited by 9 publications

References 137 publications

Manipulations of inhibition in cortical circuitry differentially affect spectral and temporal features of Bengalese finch song

Manipulations of inhibition in cortical circuitry differentially affect spectral and temporal features of Bengalese finch song

Norepinephrine in the avian auditory cortex enhances developmental song learning

Manipulations of sensory experiences during development reveal mechanisms underlying vocal learning biases in zebra finches

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