Emergent tuning for learned vocalizations in auditory cortex

Moore, Jordan M.; Woolley, Sarah M. N.

doi:10.1038/s41593-019-0458-4

Cited by 58 publications

(57 citation statements)

References 55 publications

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“…A number of previous studies in songbirds have examined the effects of acoustic experience on auditory responses (Adret et al, 2012;Amin et al, 2013;Moore and Woolley, 2019), perception (Sturdy et al, 2001;Chen et al, 2017), and intrinsic excitability (Ross et al, 2019). However, the assumption has been that the acoustic structure of the tutor song is the most important factor shaping development, and the effects of the acoustic background have not been considered.…”

Section: Discussionmentioning

confidence: 99%

“…Birds who do not hear song during this sensory acquisition period are unable to produce species-typical songs as adults, even if they are exposed to a tutor later in life (Marler and Tamura, 1964;Eales, 1985). Although the failure to develop normal song undoubtedly reflects the lack of a specific model to guide sensorimotor learning, it is also important to consider how the early acoustic environment impacts auditory processing more generally (Woolley, 2012;Moore and Woolley, 2019). In rodents, the statistics of sensory experience during an early critical period have lasting effects on cortical tuning (Zhang et al, 2001;de Villers-Sidani et al, 2007;Levelt and Hübener, 2012).…”

Section: Introductionmentioning

confidence: 99%

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Experience- and Sex-Dependent Intrinsic Plasticity in the Zebra Finch Auditory Cortex during Song Memorization

Chen

Meliza

2020

J. Neurosci.

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For vocal communicators like humans and songbirds, survival and reproduction depend on highly developed auditory processing systems that can detect and differentiate nuanced differences in vocalizations, even amid noisy environments. Early auditory experience is critical to the development of these systems. In zebra finches and other songbirds, there is a sensitive period when young birds memorize a song that will serve as a model for their own vocal production. In addition to learning a specific tutor's song, the auditory system may also undergo critical developmental processes that support auditory perception of vocalizations more generally. Here, we investigate changes in intrinsic spiking dynamics among neurons in the caudal mesopallium, a cortical-level auditory area implicated in discriminating and learning species-specific vocalizations. A subset of neurons in this area only fire transiently at the onset of current injections (i.e., phasic firing), a dynamical property that can enhance the reliability and selectivity of neural responses to complex acoustic stimuli. At the beginning of the sensitive period, just after zebra finches have fledged from the nest, there is an increase in the proportion of caudal mesopallium neurons with phasic excitability, and in the proportion of neurons expressing Kv1.1, a low-threshold channel that facilitates phasic firing. This plasticity requires exposure to a complex, noisy environment and is greater in males, the only sex that sings in this species. This shift to more phasic dynamics is therefore an experience-dependent adaptation that could facilitate auditory processing in noisy, acoustically complex conditions during a key stage of vocal development.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Experience- and Sex-Dependent Intrinsic Plasticity in the Zebra Finch Auditory Cortex during Song Memorization

Chen

Meliza

2020

J. Neurosci.

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“…Surprisingly little is known about how sensory representations of natural stimuli differ across species (Theunissen and Elie, 2014). This question is central to understanding how evolution and development shape sensory representations (Moore and Woolley, 2019) as well as developing animal models of human brain functions. Audition provides a natural test case because speech and music play a unique role in human hearing (Zatorre et al, 2002;Hickok and Poeppel, 2007;Patel, 2012).…”

Section: Introductionmentioning

confidence: 99%

Distinct higher-order representations of natural sounds in human and ferret auditory cortex

Landemard

Bimbard

Demené

et al. 2020

Preprint

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Little is known about how neural representations of natural stimuli differ across species. Speech and music for example play a unique role in human hearing, but it is unclear how auditory representations of speech and music differ between humans and other animals. Using functional Ultrasound imaging, we measured responses in ferret auditory cortex to a set of natural and spectrotemporally-matched synthetic sounds previously tested in humans, as well as natural and synthetic ferret vocalizations. Ferrets showed similar frequency and modulation tuning to that observed in humans. But while humans showed selective responses to natural speech and music in non-primary auditory cortex, ferret responses to natural and synthetic sounds were closely matched throughout primary and non-primary regions, even when tested with ferret vocalizations. This finding suggests the unique demands of speech and music have substantially altered higher-order acoustic representations in human auditory cortex, while largely preserving lower-level tuning for frequency and modulation.

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“…It is inversely proportional to the fundamental frequency, which in zebra finch females ranges from 400 to 700 Hz (Elie and Theunissen, 2016) and in males from 600 to 1000 Hz (Vignal et al, 2008). We generated ripples with spectral modulation densities of 1.2, 1.6, and 2.0 cyc/kHz, which match the spectral modulation densities of zebra finch calls (1.2 cyc/kHz for males, 1.6 and 2.0 cyc/kHz for females) and song syllables (Vignal et al, 2008;Elie and Theunissen, 2016;Moore and Woolley, 2019). Eight ripple phases were spaced evenly across a cycle for each modulation density.…”

Section: Stimulimentioning

confidence: 99%

“…Sections were mounted and imaged (Olympus America) under CY3 and FITC filters to localize fluorescent DiI and DiO tracks. A bright-field image was taken for each brain section to delineate the borders of the thalamorecipient regions L2a, where dark fibers are visualized (Calabrese and Woolley, 2015;Moore and Woolley, 2019). Sections were then dried, stained for Nissl bodies and imaged to delineate borders between cortical regions based on their cytoarchitectural features (Fortune and Margoliash, 1992).…”

Section: Electrophysiologymentioning

confidence: 99%

Auditory Selectivity for Spectral Contrast in Cortical Neurons and Behavior

Edwards

Woolley

2019

J. Neurosci.

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Vocal communication relies on the ability of listeners to identify, process, and respond to vocal sounds produced by others in complex environments. To accurately recognize these signals, animals' auditory systems must robustly represent acoustic features that distinguish vocal sounds from other environmental sounds. Vocalizations typically have spectral structure; power regularly fluctuates along the frequency axis, creating spectral contrast. Spectral contrast is closely related to harmonicity, which refers to spectral power peaks occurring at integer multiples of a fundamental frequency. Although both spectral contrast and harmonicity typify natural sounds, they may differ in salience for communication behavior and engage distinct neural mechanisms. Therefore, it is important to understand which of these properties of vocal sounds underlie the neural processing and perception of vocalizations. Here, we test the importance of vocalization-typical spectral features in behavioral recognition and neural processing of vocal sounds, using male zebra finches. We show that behavioral responses to natural and synthesized vocalizations rely on the presence of discrete frequency components, but not on harmonic ratios between frequencies. We identify a specific population of neurons in primary auditory cortex that are sensitive to the spectral resolution of vocal sounds. We find that behavioral and neural response selectivity is explained by sensitivity to spectral contrast rather than harmonicity. This selectivity emerges within the cortex; it is absent in the thalamorecipient region and present in the deep output region. Further, deep-region neurons that are contrast-sensitive show distinct temporal responses and selectivity for modulation density compared with unselective neurons.

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Emergent tuning for learned vocalizations in auditory cortex

Cited by 58 publications

References 55 publications

Experience- and Sex-Dependent Intrinsic Plasticity in the Zebra Finch Auditory Cortex during Song Memorization

Experience- and Sex-Dependent Intrinsic Plasticity in the Zebra Finch Auditory Cortex during Song Memorization

Distinct higher-order representations of natural sounds in human and ferret auditory cortex

Auditory Selectivity for Spectral Contrast in Cortical Neurons and Behavior

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