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

Abstract

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...