Department of Clinical Neuroscience, Karolinska Institutet, Stockholm, Sweden.
Department of Neurology, Stanford School of Medicine, Stanford, California, United States of America.
PLoS Biol. 2024 Oct 14;22(10):e3002849. doi: 10.1371/journal.pbio.3002849. eCollection 2024 Oct.
A core function of the olfactory system is to determine the valence of odors. In humans, central processing of odor valence perception has been shown to take form already within the olfactory bulb (OB), but the neural mechanisms by which this important information is communicated to, and from, the olfactory cortex (piriform cortex, PC) are not known. To assess communication between the 2 nodes, we simultaneously measured odor-dependent neural activity in the OB and PC from human participants while obtaining trial-by-trial valence ratings. By doing so, we could determine when subjective valence information was communicated, what kind of information was transferred, and how the information was transferred (i.e., in which frequency band). Support vector machine (SVM) learning was used on the coherence spectrum and frequency-resolved Granger causality to identify valence-dependent differences in functional and effective connectivity between the OB and PC. We found that the OB communicates subjective odor valence to the PC in the gamma band shortly after odor onset, while the PC subsequently feeds broader valence-related information back to the OB in the beta band. Decoding accuracy was better for negative than positive valence, suggesting a focus on negative valence. Critically, we replicated these findings in an independent data set using additional odors across a larger perceived valence range. Combined, these results demonstrate that the OB and PC communicate levels of subjective odor pleasantness across multiple frequencies, at specific time points, in a direction-dependent pattern in accordance with a two-stage model of odor processing.
嗅觉系统的一个核心功能是确定气味的效价。在人类中,已经表明气味效价感知的中枢处理在嗅球(OB)中形成,但是将此重要信息传递到和来自嗅皮层(梨状皮层,PC)的神经机制尚不清楚。为了评估这两个节点之间的通讯,我们同时从人类参与者中测量了 OB 和 PC 中与气味相关的神经活动,同时获得了逐试的效价评分。通过这样做,我们可以确定何时传达主观效价信息,传递了什么样的信息以及信息是如何传递的(即,在哪个频带中)。支持向量机(SVM)学习用于相干谱和频率分辨格兰杰因果关系,以识别 OB 和 PC 之间功能和有效连接的效价依赖性差异。我们发现,OB 在气味开始后不久就在伽马频带中将主观气味效价传递到 PC,而 PC 随后在β频带中将更广泛的与效价相关的信息反馈到 OB。解码准确性对于负效价比正效价更好,这表明对负效价的关注。至关重要的是,我们在使用更大的感知效价范围的其他气味的独立数据集上复制了这些发现。这些结果表明,OB 和 PC 以与气味处理的两阶段模型一致的方向依赖性模式,在多个频率和特定时间点上传递主观气味宜人度的水平。