Epigenetic regulation of transcriptional plasticity associated with developmental song learning

Kelly, Theresa K.; Ahmadiantehrani, Somayeh; Blattler, Adam; London, Sarah E.

doi:10.1098/rspb.2018.0160

Cited by 22 publications

(23 citation statements)

References 51 publications

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“…The observation that left NCM ICC depends upon tutor experience during the CP is consistent with a large and growing body of evidence indicating that NCM undergoes tutor experience-dependent plasticity in support of tutor song memorization (Ahmadiantehrani & London, 2017;Kelly, Ahmadiantehrani, Blattler, & London, 2018;London & Clayton, 2008;Yanagihara & Yazaki-Sugiyama, 2016). The current results extend these findings to the systems level using rs-fMRI.…”

Section: Discussionsupporting

confidence: 89%

Functional connectivity strength within the auditory forebrain is altered by song learning and predicts song stereotypy in developing male zebra finches

Berman

et al. 2019

Preprint

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Much as humans acquire speech in early childhood, the zebra finch (Taeniopygia guttata) songbird learns to sing from an adult "tutor" during the first three months of life. Within a welldefined critical period (CP), juvenile zebra finches memorize a tutor song that will guide subsequent motor patterning. This sensory learning process is mediated by tutor experiencedependent neuroplasticity within the auditory forebrain. Here, we used longitudinal resting-state fMRI analyses to investigate whether tutor experience also modifies patterns of functional connectivity (FC) within the juvenile zebra finch brain. Eighteen male zebra finches (only males sing) were scanned before, during, and at the end of the CP, as well as at the young adult stage.Prior to the onset of the CP, birds were separated into rearing conditions: Normal (aviaryhoused; N=5), Tutored (one adult male tutor and one adult female; N=7), and Isolate (two adult females, isolated from male song; N=6). Brain-wide voxel-wise analyses identified a single cluster overlapping the left caudomedial nidopallium (NCM) of the auditory forebrain that showed developmentally decreasing FC strength in Isolates but stable or increasing FC in Normal and Tutored birds. Additionally, FC between left NCM and left dorsal cerebellum showed a parallel developmental difference. Developmental changes in left NCM FC strength statistically mediated condition-related differences in song stereotypy. These results extend previous reports of tutor experience-dependent plasticity in NCM at epigenetic, genomic, molecular, and cellular levels to the whole-brain functional network level by demonstrating that tutor experience also influences the development of NCM FC. Moreover, these results link NCM FC to the emergence of song stereotypy.

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Section: Discussionsupporting

confidence: 89%

Functional connectivity strength within the auditory forebrain is altered by song learning and predicts song stereotypy in developing male zebra finches

Berman

et al. 2019

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“…This comparison thus controls for aviary removal and standardizes social complexity while still varying tutor experience. There is precedence for these conditions causing distinctions in epigenetic-and systemslevels of analysis in juveniles males (Kelly et al, 2018;Layden et al, 2019).…”

Section: Discussionmentioning

confidence: 99%

“…In fact, tutor song memorization is not rote, it is optimal when song is presented in social interactions and multimodal sensory experiences (Adret, 2004;Deregnaucourt et al, 2013). Third, a feature of the CP in primary visual cortex is that extended experience-dependent plasticity is a delay of maturation, but epigenetic evidence from juvenile male auditory forebrain is not consistent with this idea (Takesian and Hensch, 2013;Kelly et al, 2018). Fourth, the cellular organization of avian brains is not the same as in mammals.…”

Section: Discussionmentioning

confidence: 99%

“…Normalization via adjacent regions was done in order to control for potential variations in tissue background or staining efficiency. These normalized section measures were averaged by song area within each subject to give one normalized average cell density measure per subject per song network node (Mello et al, 1992;Kelly et al, 2018). The normalized average cell density is the measure used in the following statistical analysis and in Statistics.…”

Section: Methodsmentioning

confidence: 99%

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Inhibitory cell populations depend on age, sex, and prior experience across a neural network for Critical Period learning

Gogola

Gores

London

2019

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In many ways, the complement of cell subtypes determines the information processing that a local brain circuit can perform. For example, the balance of excitatory and inhibitory (E/I) signaling within a brain region contributes to response magnitude and specificity in ways that influence the effectiveness of information processing. An extreme example of response changes to sensory information occur across Critical Periods (CPs). In primary mammalian visual cortex, GAD65 and parvalbumin inhibitory cell types in particular control experience-dependent responses during a CP. Here, we test how the density of GAD65-and parvalbumin-expressing cells may inform on a CP for complex behavioral learning. Juvenile male zebra finch songbirds (females cannot sing) learn to sing through coordinated sensory, sensorimotor, and motor learning processes distributed throughout a well-defined neural network.There is a CP is for sensory learning, the stage during which a young male forms a memory of his "tutor's" song, which is then used to guide the young bird's emerging song structure. We quantified the effect of sex and experience with a tutor on the cell densities of GAD65-and parvalbumin-expressing cells across major nodes of the song network, using ages that span the CP for tutor song memorization.As a resource, we also include whole-brain mapping data for both genes. Results indicate that inhibitory cell populations differ across sex, age, and experiential conditions, but not always in the ways we predicted.

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“…Although we sampled at only a few older ages, the timing of the decrease is suggestive, 199 as P65 is around the time when the sensory acquisition phase ends, and birds are no longer able 200 to learn new song elements (Gobes et al, 2017). If, as we posit, phasic excitability facilitates both 201 auditory processing development and song learning, then the shift back to more tonic dynamics at 202 this age could contribute more directly to the process of song acquisition; specifically, a diminished 203 ability to learn new material during sensorimotor learning may be regulated by the processes that 204 cause the song memorization period to close (London, 2017;Kelly et al, 2018). This hypothesis 205 could be tested by determining if phasic excitability remains high in VI animals, who retain the 206 ability to learn new song material into adulthood (Morrison and Nottebohm, 1993).…”

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confidence: 94%

Experience- and sex-dependent intrinsic plasticity in the zebra finch auditory cortex during song memorization

Chen

Meliza

2019

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1Early auditory experience is critical to the development of vocal communication. Zebra finches and 2 other songbirds have a sensitive period when young birds memorize a song to use as a model for 3 vocal production. We found that intrinsic spiking dynamics change dramatically during this period 4 in the caudal mesopallium, a cortical-level auditory area. Specifically, the proportion of neurons 5 that only fire transiently at the onset of intracellular current injections increases, along with Kv1.1, 6 a channel that facilitates transient spiking. Plasticity is greater in males and requires exposure to a 7 complex, noisy environment. These observations indicate that intrinsic dynamics are modulated in 8 response to the acoustic environment to support robust auditory processing during a critical phase 9 of vocal learning. 10 Main Text 11Vocal communicators require auditory systems that can reliably encode information over the broad 12 range of spectral and temporal scales found in vocalizations (Singh and Theunissen, 2003; Wang et 13 al., 2008). In humans, songbirds, and other species that learn how to vocalize through sensorimotor 14 learning, the auditory system must also provide reliable feedback so that motor production can 15 be adjusted to match desired targets. Early experience hearing conspecific vocalizations not only 16Chen and Meliza -Intrinsic plasticity during song memorization (preprint) p. 2 determines the targets to be imitated, but also influences auditory perception (Doupe and Kuhl, 17 1999). A classic example is the perceptual narrowing that occurs in humans during the first year of 18 life, in which exposure to speech establishes the phonetic distinctions an infant is able to perceive 19 (Werker and Lalonde, 1988;Kuhl et al., 1992;Kuhl, 2004). The neural plasticity underlying this 20 critical stage in development is poorly understood. 21As in humans, early auditory experience is critical to vocal communication in zebra finches (Tae-22 niopygia guttata). Around 25 days of age, juvenile males begin to memorize the song of an adult 23 male tutor whom they will learn to imitate (Gobes et al., 2017). Birds who do not hear song during 24 this sensory acquisition period are unable to produce species-typical songs as adults, even if they 25 are exposed to a tutor later in life (Marler and Tamura, 1964;Eales, 1985). To understand this process 26 and relate it to human speech development, it is important to consider not only how specific song 27 memories guide sensorimotor learning, but also how the early acoustic environment (including 28 but not limited to the song of a primary tutor) might shape auditory processing more generally 29 (Woolley, 2012). In support of this idea, raising birds in acoustically impoverished environments 30 produces a range of behavioral and physiological deficits consistent with abnormal auditory pro-31 cessing (Sturdy et al., 2001;Chen et al., 2017;Amin et al., 2013). Conversely, birds raised without 32 exposure to a tutor but in an acoustically rich environment retain some...

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Epigenetic regulation of transcriptional plasticity associated with developmental song learning

Cited by 22 publications

References 51 publications

Functional connectivity strength within the auditory forebrain is altered by song learning and predicts song stereotypy in developing male zebra finches

Functional connectivity strength within the auditory forebrain is altered by song learning and predicts song stereotypy in developing male zebra finches

Inhibitory cell populations depend on age, sex, and prior experience across a neural network for Critical Period learning

Experience- and sex-dependent intrinsic plasticity in the zebra finch auditory cortex during song memorization

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