Zavitz Elizabeth, Yu Hsin-Hao, Rowe Elise G, Rosa Marcello G P, Price Nicholas S C
Department of Physiology, Neuroscience Program, Biomedicine Discovery Institute, and ARC Centre of Excellence for Integrative Brain Function, Monash University Node, Monash University, Clayton, VIC 3800, Australia
Department of Physiology, Neuroscience Program, Biomedicine Discovery Institute, and ARC Centre of Excellence for Integrative Brain Function, Monash University Node, Monash University, Clayton, VIC 3800, Australia.
J Neurosci. 2016 Apr 20;36(16):4579-90. doi: 10.1523/JNEUROSCI.4563-15.2016.
Each visual experience changes the neural response to subsequent stimuli. If the brain is unable to incorporate these encoding changes, the decoding, or perception, of subsequent stimuli is biased. Although the phenomenon of adaptation pervades the nervous system, its effects have been studied mainly in isolation, based on neuronal encoding changes induced by an isolated, prolonged stimulus. To understand how adaptation-induced biases arise and persist under continuous, naturalistic stimulation, we simultaneously recorded the responses of up to 61 neurons in the marmoset (Callithrix jacchus) middle temporal area to a sequence of directions that changed every 500 ms. We found that direction-specific adaptation following only 0.5 s of stimulation strongly affected encoding for up to 2 s by reducing both the gain and the spike count correlations between pairs of neurons with preferred directions close to the adapting direction. In addition, smaller changes in bandwidth and preferred direction were observed in some animals. Decoding individual trials of adaptation-affected activity in simultaneously recorded neurons predicted repulsive biases that are consistent with the direction aftereffect. Surprisingly, removing spike count correlations by trial shuffling did not impact decoding performance or bias. When adaptation had the largest effect on encoding, the decoder made the most errors. This suggests that neural and perceptual repulsion is not a mechanism to enhance perceptual performance but is instead a necessary consequence of optimizing neural encoding for the identification of a wide range of stimulus properties in diverse temporal contexts.
Although perception depends upon decoding the pattern of activity across a neuronal population, the encoding properties of individual neurons are unreliable: a single neuron's response to repetitions of the same stimulus is variable, and depends on both its spatial and temporal context. In this manuscript, we describe the complete cascade of adaptation-induced effects in sensory encoding and show how they predict population decoding errors consistent with perceptual biases. We measure the time course of adaptation-induced changes to the response properties of neurons in isolation, and to the correlation structure across pairs of simultaneously recorded neurons. These results provide novel insight into how and for how long adaptation affects the neural code, particularly during continuous, naturalistic vision.
每一次视觉体验都会改变大脑对后续刺激的神经反应。如果大脑无法整合这些编码变化，那么对后续刺激的解码或感知就会产生偏差。尽管适应现象遍及整个神经系统，但其影响主要是基于由孤立的、长时间的刺激所诱发的神经元编码变化进行单独研究的。为了了解在连续的、自然主义的刺激下适应诱导的偏差是如何产生并持续存在的，我们同时记录了狨猴（Callithrix jacchus）颞中区多达61个神经元对每500毫秒变化一次的一系列方向的反应。我们发现，仅0.5秒的刺激后，方向特异性适应通过降低增益以及具有接近适应方向的偏好方向的神经元对之间的尖峰计数相关性，强烈影响编码长达2秒。此外，在一些动物中还观察到带宽和偏好方向的较小变化。对同时记录的神经元中受适应影响的活动进行逐个试验解码，预测出与方向后效一致的排斥偏差。令人惊讶的是，通过试验重排消除尖峰计数相关性并不会影响解码性能或偏差。当适应对编码的影响最大时，解码器出现的错误最多。这表明神经和感知排斥不是提高感知性能的机制，而是在不同时间背景下优化神经编码以识别广泛刺激特性的必然结果。
尽管感知依赖于对神经元群体活动模式的解码，但单个神经元的编码特性是不可靠的：单个神经元对相同刺激重复的反应是可变的，并且取决于其空间和时间背景。在本论文中，我们描述了适应诱导的感觉编码效应的完整级联，并展示了它们如何预测与感知偏差一致的群体解码错误。我们测量了适应诱导的对单个神经元反应特性以及对同时记录的神经元对之间相关结构变化的时间进程。这些结果为适应如何以及在多长时间内影响神经编码提供了新的见解，特别是在连续的、自然主义的视觉过程中。
