A mechanistic account of visual discomfort

Much of the neural machinery of the early visual cortex, from the extraction of local orientations to contextual modulations through lateral interactions, is thought to have developed to provide a sparse encoding of contour in natural scenes, allowing the brain to process efficiently most of the visual scenes we are exposed to. Certain visual stimuli, however, cause visual stress, a set of adverse effects ranging from simple discomfort to migraine attacks, and epileptic seizures in the extreme, all phenomena linked with an excessive metabolic demand. The theory of efficient coding suggests a link between excessive metabolic demand and images that deviate from natural statistics. Yet, the mechanisms linking energy demand and image spatial content in discomfort remain elusive. Here, we used theories of visual coding that link image spatial structure and brain activation to characterize the response to images observers reported as uncomfortable. Our biologically based neurodynamic model of the early visual cortex included excitatory and inhibitory layers to implement contextual influences. We found three clear markers of aversive images: a larger overall activation in the model, a less sparse response, and a more unbalanced distribution of activity across spatial orientations. When the ratio of excitation over inhibition was increased in the model, a phenomenon hypothesised to underlie interindividual differences in susceptibility to visual discomfort, the three markers of discomfort progressively shifted towards values typical of the response to uncomfortable stimuli. Overall, these findings propose a unifying mechanistic explanation for why there are differences between images and between observers, suggesting how visual input and idiosyncratic hyperexcitability give rise to abnormal brain responses that result in visual stress.

早期视觉皮层（early visual cortex）的多数神经机制，从局部方位提取到通过侧向交互实现的上下文调制，一般被认为是为了对自然场景中的轮廓进行稀疏编码而演化而来，使大脑能够高效处理我们日常接触的绝大多数视觉场景。然而，某些视觉刺激会引发视觉不适（visual stress）——这类不良反应范围从轻微不适到偏头痛发作，极端情况下还会诱发癫痫发作，所有这些现象都与过度代谢需求相关。高效编码（efficient coding）理论指出，过度代谢需求与偏离自然统计特性的图像之间存在关联，但目前将能量需求与图像空间内容关联起来的不适诱发机制仍不明确。本研究借助将图像空间结构与大脑激活相联系的视觉编码理论，对观察者报告为不适的图像所引发的反应进行了表征。我们基于生物学原理构建的早期视觉皮层神经动力学模型（neurodynamic model）包含兴奋层与抑制层，用以实现上下文影响的模拟。研究发现不适图像存在三个明确的特征：模型整体激活水平更高、响应稀疏性更低，以及空间方位间的活动分布更不均衡。当模型中兴奋-抑制比（excitation over inhibition）升高时——这一现象被假设为视觉不适易感性存在个体间差异的潜在基础——上述三个不适特征会逐渐向不适刺激响应的典型数值偏移。综上，这些发现为不同图像间以及不同观察者间的差异提供了统一的机制性解释，揭示了视觉输入与个体特有的过度兴奋性如何引发异常脑反应，进而导致视觉不适。