Department of Epileptology, University Hospital Bonn, Bonn, Germany.
Department of Experimental Psychology, University of Oxford, Oxford, UK.
Nature. 2024 Oct;634(8034):626-634. doi: 10.1038/s41586-024-08016-5. Epub 2024 Oct 9.
Olfaction is a fundamental sensory modality that guides animal and human behaviour. However, the underlying neural processes of human olfaction are still poorly understood at the fundamental-that is, the single-neuron-level. Here we report recordings of single-neuron activity in the piriform cortex and medial temporal lobe in awake humans performing an odour rating and identification task. We identified odour-modulated neurons within the piriform cortex, amygdala, entorhinal cortex and hippocampus. In each of these regions, neuronal firing accurately encodes odour identity. Notably, repeated odour presentations reduce response firing rates, demonstrating central repetition suppression and habituation. Different medial temporal lobe regions have distinct roles in odour processing, with amygdala neurons encoding subjective odour valence, and hippocampal neurons predicting behavioural odour identification performance. Whereas piriform neurons preferably encode chemical odour identity, hippocampal activity reflects subjective odour perception. Critically, we identify that piriform cortex neurons reliably encode odour-related images, supporting a multimodal role of the human piriform cortex. We also observe marked cross-modal coding of both odours and images, especially in the amygdala and piriform cortex. Moreover, we identify neurons that respond to semantically coherent odour and image information, demonstrating conceptual coding schemes in olfaction. Our results bridge the long-standing gap between animal models and non-invasive human studies and advance our understanding of odour processing in the human brain by identifying neuronal odour-coding principles, regional functional differences and cross-modal integration.
嗅觉是一种基本的感觉模式，指导着动物和人类的行为。然而，人类嗅觉的基本神经过程，即在单个神经元水平上，仍知之甚少。在这里，我们报告了在清醒人类执行气味评分和识别任务时，嗅球皮层和内侧颞叶的单个神经元活动的记录。我们在嗅球皮层、杏仁核、内嗅皮层和海马体中识别出气味调制神经元。在这些区域中的每一个区域，神经元的发射都准确地编码了气味的身份。值得注意的是，重复呈现气味会降低反应发射率，表明中枢重复抑制和习惯化。不同的内侧颞叶区域在气味处理中具有不同的作用，杏仁核神经元编码主观气味效价，而海马体神经元预测行为气味识别性能。虽然嗅球神经元优选地编码化学气味身份，但海马体活动反映了主观气味感知。至关重要的是，我们确定嗅球皮层神经元可靠地编码与气味相关的图像，支持人类嗅球皮层的多模态作用。我们还观察到气味和图像的显著跨模态编码，尤其是在杏仁核和嗅球皮层中。此外，我们确定了对语义连贯的气味和图像信息有反应的神经元，证明了嗅觉中的概念编码方案。我们的研究结果弥合了动物模型和非侵入性人类研究之间的长期差距，通过确定神经元气味编码原则、区域功能差异和跨模态整合，推进了我们对人类大脑嗅觉处理的理解。
