Corticobasal ganglia projecting neurons are required for juvenile vocal learning but not for adult vocal plasticity in songbirds-猫眼课题宝

DOI：

10.1073/pnas.1913575116

发表时间：

2019-10

期刊：

Proceedings of the National Academy of Sciences

影响因子：

通讯作者：

中科院分区：

其他

文献类型：

作者：

Miguel Sánchez-Valpuesta;Yumeno Suzuki;Yukino Shibata;Noriyuki Toji;Yu Ji;Nasiba Afrin;C. N. Asogwa;Ippei Kojima;Daisuke Mizuguchi;S. Kojima;K. Okanoya;H. Okado;Kenta Kobayashi;Kazuhiro Wada

意义我们回答了这个问题，“皮质-基底节投射神经元如何对发声学习做出贡献？”我们对一只鸣禽中投射到基底节的发声皮质神经元HVC(X)神经元进行了特定的消融，这些神经元在歌唱时会产生时间上的精确放电。对青少年HVC(X)神经元的特定消融导致学习辅导曲的声学缺陷和歌曲序列的不一致。相反，成年HVC(X)神经元消融不影响发声波动的程度，也不会通过听觉反馈抑制引起歌曲结构的改变。这些结果支持这样的假设，即HVC(X)神经元是传递时间信号的神经底物，而不是调节发声波动或传递听觉反馈的神经底物，用于发声学习和维持。鸟鸣，就像人类的语言一样，由通过发声学习获得的一系列在时间上精确的动作组成。这种顺序发声的学习依赖于运动皮质和基底节的神经功能。然而，目前尚不清楚皮质和基底节成分之间的联系如何有助于发声运动技能学习，因为哺乳动物的运动皮质服务于多种类型的运动动作，而大多数实验上容易驯服的动物没有表现出发声学习。在这里，我们利用鸣鸟斑马雀作为动物模型，探索皮质样(HVC)和基底节(X区)之间的连接功能，该连接由HVC(X)投射神经元连接，在歌唱时具有时间上的精确放电。通过专门消融HVC(X)神经元，幼年斑雀无法复制经过训练的音节声学，并发展出序列一致性较低的时间不稳定的歌曲。相比之下，HVC(X)消融的成年人没有改变他们学习的歌曲结构，但产生了声学波动，并通过引入歌曲恶化来对听觉反馈中断做出反应，正常成年人也是如此。这些结果表明，皮质基底节的输入对于学习歌曲结构的声学和时间方面是重要的，但对于产生有助于维持已经学习的发声模式的声音波动来说并不重要。

Significance We addressed the question, “How do corticobasal ganglia projecting neurons contribute to vocal learning?” We performed specific ablation of the vocal cortical neurons projecting to the basal ganglia, HVC(X) neurons in a songbird, which generate temporally precise firing during singing. Specific ablation of HVC(X) neurons in juveniles caused deficits in learning the tutor song’s acoustics and less consistency of song sequence. In contrast, adult HVC(X) neuron ablation did not affect the degree of vocal fluctuations or cause alteration in song structure by auditory feedback inhibition. These results support the hypothesis that HVC(X) neurons are a neural substrate for transferring temporal signals, but not for regulating vocal fluctuations or conveying auditory feedback, to the basal ganglia for vocal learning and maintenance. 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.

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

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