A neural circuit mechanism for regulating vocal variability during song learning in zebra finches.
A neural circuit mechanism for regulating vocal variability during song learning in zebra finches.
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DOI：
10.7554/elife.03697
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发表时间：
2014-12-15
期刊：
影响因子：
7.7
通讯作者：
Ölveczky BP
中科院分区：
文献类型：
--
作者：
Garst-Orozco J;Babadi B;Ölveczky BP
运动技能学习的特点是提高表现和减少运动变异性。然而，结合技能水平和可变性的神经机制尚不清楚。斑马雀，一种鸣禽，提供了一个独特的机会来解决这个问题，因为学习歌曲的产生和声音变化的诱导是在不同的电路中实例化的，这些电路汇聚在控制声音输出的运动皮层模拟物上。为了探索学习和变异性之间的相互作用，我们对这一区域的神经元进行了细胞内记录，描述了它们从功能不同的途径输入的信息在歌曲发育过程中是如何变化的。我们发现驱动刻板歌曲模式的输入得到加强和修剪，而诱导变异的输入保持不变。一个简单的网络模型表明，加强和修剪特定动作的连接降低了运动控制回路对可变输入和神经“噪声”的敏感性。这确定了一种简单而通用的运动可变性学习相关调节机制。DOI: http://dx.doi.org/10.7554/eLife.03697.001“熟能生巧”抓住了我们学习新技能的本质。例如，当我们学习演奏一种乐器时，通常需要几个小时的练习才能第一次正确地演奏一首曲子。随着我们变得越来越好，我们表现的可变性——这在学习的早期阶段是一个优势——变得越来越少。同样，鸣禽也需要大量的练习来掌握它们用来吸引配偶的复杂歌曲。对鸣禽的研究表明，大脑中负责鸣叫和产生声音变异性的神经回路都集中在一个被称为翅翼强健核（简称RA）的运动控制区域。然而，人们对学习一首歌如何减少声乐表演的可变性的细节知之甚少。现在，Garst-Orozco等人通过研究斑胸草雀的大脑切片，研究了学习和变异性之间的关系。他们的实验表明，RA神经元从控制鸣叫的高阶大脑区域接收的输入会随着练习而改变，随着鸟类鸣叫能力的提高，一些输入会变得更强，而另一些则会被消除。然而，尽管歌曲变得越来越精确，但RA神经元从产生声音变异性的电路中接收到的输入并没有改变。Garst-Orozco等人通过计算机模拟表明，当来自控制歌曲的大脑区域的输入被自适应地加强和消除时，RA神经元对可变或“嘈杂”输入的敏感性会降低。这确保了当组成鸟叫声的音符和音节最终被学会时，它们将以高保真和精确的方式发出。有趣的是，哺乳动物的运动技能学习与Garst-Orozco等人描述的神经连接变化非常相似，这表明从鸣禽身上获得的见解可能会让我们更好地理解“熟能生巧”在人类身上的作用。DOI: http://dx.doi.org/10.7554/eLife.03697.002
Motor skill learning is characterized by improved performance and reduced motor variability. The neural mechanisms that couple skill level and variability, however, are not known. The zebra finch, a songbird, presents a unique opportunity to address this question because production of learned song and induction of vocal variability are instantiated in distinct circuits that converge on a motor cortex analogue controlling vocal output. To probe the interplay between learning and variability, we made intracellular recordings from neurons in this area, characterizing how their inputs from the functionally distinct pathways change throughout song development. We found that inputs that drive stereotyped song-patterns are strengthened and pruned, while inputs that induce variability remain unchanged. A simple network model showed that strengthening and pruning of action-specific connections reduces the sensitivity of motor control circuits to variable input and neural ‘noise’. This identifies a simple and general mechanism for learning-related regulation of motor variability. DOI: http://dx.doi.org/10.7554/eLife.03697.001 ‘Practice makes perfect’ captures the essence of how we learn new skills. When learning to play a musical instrument, for example, it often takes hours of practice before we can play a single piece of music properly for the first time. And as we get better, the variability in our performance—which is an advantage during the early stages of learning—becomes less. Likewise, songbirds need lots of practice in order to master the intricate songs they need to sing to attract mates. Studies in songbirds show that the neural circuits in the brain that are responsible for producing song and for generating vocal variability both converge on a motor control region called the robust nucleus of the arcopallium (or RA for short). However, the details of how learning a song leads to reduced variability in vocal performance are poorly understood. Now Garst-Orozco et al. have investigated the relationship between learning and variability by studying brain slices of zebra finches. Their experiments reveal that the inputs received by RA neurons from a higher-order brain region that controls song change with practice, with some inputs becoming stronger and others being eliminated as the birds' singing ability improves. However, inputs received by RA neurons from the circuit that generates vocal variability do not change despite the song becoming increasingly precise. Using a computer simulation, Garst-Orozco et al. show that the sensitivity of RA neurons to variable or ‘noisy’ input is reduced when inputs from the brain region that controls song are adaptively strengthened and eliminated. This ensures that when the notes and syllables that make up the bird's song have finally been learned, they will be uttered with high fidelity and precision. Intriguingly, motor skill learning in mammals have been associated with neural connectivity changes very similar to those described by Garst-Orozco et al., suggesting that insights from songbirds may lead to a better understanding of how ‘practice makes perfect’ also works in humans. DOI: http://dx.doi.org/10.7554/eLife.03697.002