Troyer T W, Doupe A J
Department of Psychiatry, University of California, San Francisco, California 94143-0444, USA. ttroyer@ psyc.umd.edu
J Neurophysiol. 2000 Sep;84(3):1224-39. doi: 10.1152/jn.2000.84.3.1224.
Understanding the neural mechanisms underlying serially ordered behavior is a fundamental problem in motor learning. We present a computational model of sensorimotor learning in songbirds that is constrained by the known functional anatomy of the song circuit. The model subsumes our companion model for learning individual song "syllables" and relies on the same underlying assumptions. The extended model addresses the problem of learning to produce syllables in the correct sequence. Central to our approach is the hypothesis that the Anterior Forebrain Pathway (AFP) produces signals related to the comparison of the bird's own vocalizations and a previously memorized "template." This "AFP comparison hypothesis" is challenged by the lack of a direct projection from the AFP to the song nucleus HVc, a candidate site for the generator of song sequence. We propose that sequence generation in HVc results from an associative chain of motor and sensory representations (motor --> sensory --> next motor. ) encoded within the two known populations of HVc projection neurons. The sensory link in the chain is provided, not by auditory feedback, but by a centrally generated efference copy that serves as an internal prediction of this feedback. The use of efference copy as a substitute for the sensory signal explains the ability of adult birds to produce normal song immediately after deafening. We also predict that the AFP guides sequence learning by biasing motor activity in nucleus RA, the premotor nucleus downstream of HVc. Associative learning then remaps the output of the HVc sequence generator. By altering the motor pathway in RA, the AFP alters the correspondence between HVc motor commands and the resulting sensory feedback and triggers renewed efference copy learning in HVc. Thus, auditory feedback-mediated efference copy learning provides an indirect pathway by which the AFP can influence sequence generation in HVc. The model makes predictions concerning the role played by specific neural populations during the sensorimotor phase of song learning and demonstrates how simple rules of associational plasticity can contribute to the learning of a complex behavior on multiple time scales.
理解序列行为背后的神经机制是运动学习中的一个基本问题。我们提出了一种鸣禽感觉运动学习的计算模型，该模型受到鸣唱回路已知功能解剖结构的限制。该模型包含了我们用于学习单个鸣唱“音节”的配套模型，并依赖于相同的基本假设。扩展模型解决了学习以正确顺序发出音节的问题。我们方法的核心假设是，前脑通路（AFP）产生与鸟类自身发声和先前记忆的“模板”比较相关的信号。由于缺乏从AFP到鸣唱核HVc（鸣唱序列发生器的候选部位）的直接投射，这一“AFP比较假设”受到了挑战。我们提出，HVc中的序列生成源于在HVc投射神经元的两个已知群体中编码的运动和感觉表征的关联链（运动→感觉→下一个运动）。链中的感觉联系不是由听觉反馈提供的，而是由中央产生的传出副本提供的，该传出副本作为这种反馈的内部预测。使用传出副本替代感觉信号解释了成年鸟类在致聋后立即能够发出正常鸣唱的能力。我们还预测，AFP通过偏向HVc下游的运动前核RA中的运动活动来指导序列学习。关联学习随后重新映射HVc序列发生器的输出。通过改变RA中的运动通路，AFP改变了HVc运动指令与由此产生的感觉反馈之间的对应关系，并触发了HVc中传出副本学习的更新。因此，听觉反馈介导的传出副本学习提供了一条间接途径，通过该途径AFP可以影响HVc中的序列生成。该模型对特定神经群体在鸣唱学习的感觉运动阶段所起的作用做出了预测，并展示了关联可塑性的简单规则如何在多个时间尺度上有助于复杂行为的学习。
