Miller Ryan L, Stein Barry E, Rowland Benjamin A
Department of Neurobiology and Anatomy, Wake Forest School of Medicine, Winston-Salem, North Carolina 27157.
Department of Neurobiology and Anatomy, Wake Forest School of Medicine, Winston-Salem, North Carolina 27157
J Neurosci. 2017 May 17;37(20):5183-5194. doi: 10.1523/JNEUROSCI.2767-16.2017. Epub 2017 Apr 27.
The manner in which the brain integrates different sensory inputs to facilitate perception and behavior has been the subject of numerous speculations. By examining multisensory neurons in cat superior colliculus, the present study demonstrated that two operational principles are sufficient to understand how this remarkable result is achieved: (1) unisensory signals are integrated continuously and in real time as soon as they arrive at their common target neuron and (2) the resultant multisensory computation is modified in shape and timing by a delayed, calibrating inhibition. These principles were tested for descriptive sufficiency by embedding them in a neurocomputational model and using it to predict a neuron's moment-by-moment multisensory response given only knowledge of its responses to the individual modality-specific component cues. The predictions proved to be highly accurate, reliable, and unbiased and were, in most cases, not statistically distinguishable from the neuron's actual instantaneous multisensory response at any phase throughout its entire duration. The model was also able to explain why different multisensory products are often observed in different neurons at different time points, as well as the higher-order properties of multisensory integration, such as the dependency of multisensory products on the temporal alignment of crossmodal cues. These observations not only reveal this fundamental integrative operation, but also identify quantitatively the multisensory transform used by each neuron. As a result, they provide a means of comparing the integrative profiles among neurons and evaluating how they are affected by changes in intrinsic or extrinsic factors. Multisensory integration is the process by which the brain combines information from multiple sensory sources (e.g., vision and audition) to maximize an organism's ability to identify and respond to environmental stimuli. The actual transformative process by which the neural products of multisensory integration are achieved is poorly understood. By focusing on the millisecond-by-millisecond differences between a neuron's unisensory component responses and its integrated multisensory response, it was found that this multisensory transform can be described by two basic principles: unisensory information is integrated in real time and the multisensory response is shaped by calibrating inhibition. It is now possible to use these principles to predict a neuron's multisensory response accurately armed only with knowledge of its unisensory responses.
大脑整合不同感觉输入以促进感知和行为的方式一直是众多猜测的主题。通过研究猫上丘中的多感觉神经元,本研究表明,有两个操作原则足以理解如何实现这一显著结果:(1)单感觉信号一旦到达它们的共同目标神经元,就会持续且实时地进行整合;(2)由此产生的多感觉计算在形状和时间上会被延迟的校准抑制所改变。通过将这些原则嵌入神经计算模型中,并利用该模型仅根据神经元对各个模态特定成分线索的反应来预测其逐时刻的多感觉反应,对这些原则的描述充分性进行了测试。结果证明这些预测高度准确、可靠且无偏差,并且在大多数情况下,与神经元在其整个持续时间内任何阶段的实际瞬时多感觉反应在统计学上没有显著差异。该模型还能够解释为什么在不同时间点的不同神经元中经常观察到不同的多感觉产物,以及多感觉整合的高阶特性,例如多感觉产物对跨模态线索时间对齐的依赖性。这些观察结果不仅揭示了这种基本的整合操作,还定量地确定了每个神经元所使用的多感觉转换。因此,它们提供了一种比较神经元之间整合概况并评估它们如何受到内在或外在因素变化影响的方法。多感觉整合是大脑将来自多个感觉源(如视觉和听觉)的信息结合起来以最大化生物体识别和响应环境刺激能力的过程。人们对实现多感觉整合神经产物的实际转换过程了解甚少。通过关注神经元单感觉成分反应与其整合多感觉反应之间毫秒级的差异,发现这种多感觉转换可以用两个基本原则来描述:单感觉信息实时整合,多感觉反应由校准抑制塑造。现在仅凭借对神经元单感觉反应的了解,就可以利用这些原则准确预测其多感觉反应。