Corticobasal ganglia projecting neurons are required for juvenile vocal learning but not for adult vocal plasticity in songbirds

皮质基底神经节投射神经元是幼年鸣禽发声学习所必需的,但不是成年鸣禽发声可塑性所必需的

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作者:Miguel Sánchez-Valpuesta, Yumeno Suzuki, Yukino Shibata, Noriyuki Toji, Yu Ji, Nasiba Afrin, Chinweike Norman Asogwa, Ippei Kojima, Daisuke Mizuguchi, Satoshi Kojima, Kazuo Okanoya, Haruo Okado, Kenta Kobayashi, Kazuhiro Wada

Abstract

Birdsong, like human speech, consists of a sequence of temporally precise movements acquired through vocal learning. The learning of such sequential vocalizations depends on the neural function of the motor cortex and basal ganglia. However, it is unknown how the connections between cortical and basal ganglia components contribute to vocal motor skill learning, as mammalian motor cortices serve multiple types of motor action and most experimentally tractable animals do not exhibit vocal learning. Here, we leveraged the zebra finch, a songbird, as an animal model to explore the function of the connectivity between cortex-like (HVC) and basal ganglia (area X), connected by HVC(X) projection neurons with temporally precise firing during singing. By specifically ablating HVC(X) neurons, juvenile zebra finches failed to copy tutored syllable acoustics and developed temporally unstable songs with less sequence consistency. In contrast, HVC(X)-ablated adults did not alter their learned song structure, but generated acoustic fluctuations and responded to auditory feedback disruption by the introduction of song deterioration, as did normal adults. These results indicate that the corticobasal ganglia input is important for learning the acoustic and temporal aspects of song structure, but not for generating vocal fluctuations that contribute to the maintenance of an already learned vocal pattern.

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