Lum Cecilia S, Zhurov Yuriy, Cropper Elizabeth C, Weiss Klaudiusz R, Brezina Vladimir
Department of Physiology and Biophysics, New York, NY 10029, USA.
J Neurophysiol. 2005 Oct;94(4):2427-46. doi: 10.1152/jn.00280.2005. Epub 2005 Jun 8.
Variability in nervous systems is often taken to be merely "noise." Yet in some cases it may play a positive, active role in the production of behavior. The central pattern generator (CPG) that drives the consummatory feeding behaviors of Aplysia generates large, quasi-random variability in the parameters of the feeding motor programs from one cycle to the next; the variability then propagates through the firing patterns of the motor neurons to the contractions of the feeding muscles. We have proposed that, when the animal is faced with a new, imperfectly known feeding task in each cycle, the variability implements a trial-and-error search through the space of possible feeding movements. Although this strategy will not be successful in every cycle, over many cycles it may be the optimal strategy for feeding in an uncertain and changing environment. To play this role, however, the variability must actually appear in the feeding movements and, presumably, in the functional performance of the feeding behavior. Here we have tested this critical prediction. We have developed a technique to measure, in intact, freely feeding animals, the performance of Aplysia swallowing behavior, by continuously recording with a length transducer the movement of the seaweed strip being swallowed. Simultaneously, we have recorded with implanted electrodes activity at each of the internal levels, the CPG, motor neurons, and muscles, of the feeding neuromusculature. Statistical analysis of a large data set of these recordings suggests that functional performance is not determined strongly by one or a few parameters of the internal activity, but weakly by many. Most important, the internal variability does emerge in the behavior and its functional performance. Even when the animal is swallowing a long, perfectly regular seaweed strip, remarkably, the length swallowed from cycle to cycle is extremely variable, as variable as the parameters of the activity of the CPG, motor neurons, and muscles.
神经系统的变异性通常仅仅被视为“噪音”。然而在某些情况下，它可能在行为产生过程中发挥积极、主动的作用。驱动海兔进食行为的中枢模式发生器（CPG）在进食运动程序的参数上，从一个周期到下一个周期会产生巨大的、类似随机的变异性；这种变异性随后通过运动神经元的放电模式传播到进食肌肉的收缩。我们提出，当动物在每个周期面临新的、不完全了解的进食任务时，这种变异性会在可能的进食运动空间中进行试错搜索。尽管这种策略并非在每个周期都能成功，但在许多周期中，它可能是在不确定且不断变化的环境中进食的最优策略。然而，要发挥这一作用，变异性必须实际出现在进食运动中，大概也出现在进食行为的功能表现中。在此我们对这一关键预测进行了测试。我们开发了一种技术，通过用长度传感器连续记录被吞咽海藻条的运动，来测量完整的、自由进食的海兔吞咽行为的表现。同时，我们用植入电极记录了进食神经肌肉系统内部各级（CPG、运动神经元和肌肉）的活动。对这些记录的大量数据集进行统计分析表明，功能表现并非由内部活动的一个或几个参数强烈决定，而是由许多参数微弱决定。最重要的是，内部变异性确实出现在行为及其功能表现中。即使动物在吞咽一条长的、非常规则的海藻条时，值得注意的是，从一个周期到下一个周期吞咽的长度变化极大，与CPG、运动神经元和肌肉活动的参数变化一样大。
