Wallace H Coulter Department of Biomedical Engineering, Georgia Institute of Technology and Emory University, Atlanta, Georgia 30332.
Department of Biomedical Engineering, Georgia Institute of Technology, Emory University, Atlanta, Georgia 30332 and Beijing University, Beijing China 100871.
J Neurosci. 2021 Jun 23;41(25):5421-5439. doi: 10.1523/JNEUROSCI.3018-20.2021. Epub 2021 May 13.
Rapid sensory adaptation is observed across all sensory systems, and strongly shapes sensory percepts in complex sensory environments. Yet despite its ubiquity and likely necessity for survival, the mechanistic basis is poorly understood. A wide range of primarily and anesthetized studies have demonstrated the emergence of adaptation at the level of primary sensory cortex, with only modest signatures in earlier stages of processing. The nature of rapid adaptation and how it shapes sensory representations during wakefulness, and thus the potential role in perceptual adaptation, is underexplored, as are the mechanisms that underlie this phenomenon. To address these knowledge gaps, we recorded spiking activity in primary somatosensory cortex (S1) and the upstream ventral posteromedial (VPm) thalamic nucleus in the vibrissa pathway of awake male and female mice, and quantified responses to whisker stimuli delivered in isolation and embedded in an adapting sensory background. We found that cortical sensory responses were indeed adapted by persistent sensory stimulation; putative excitatory neurons were profoundly adapted, and inhibitory neurons only modestly so. Further optogenetic manipulation experiments and network modeling suggest this largely reflects adaptive changes in synchronous thalamic firing combined with robust engagement of feedforward inhibition, with little contribution from synaptic depression. Taken together, these results suggest that cortical adaptation in the regime explored here results from changes in the timing of thalamic input, and the way in which this differentially impacts cortical excitation and feedforward inhibition, pointing to a prominent role of thalamic gating in rapid adaptation of primary sensory cortex. Rapid adaptation of sensory activity strongly shapes representations of sensory inputs across all sensory pathways over the timescale of seconds, and has profound effects on sensory perception. Despite its ubiquity and theoretical role in the efficient encoding of complex sensory environments, the mechanistic basis is poorly understood, particularly during wakefulness. In this study in the vibrissa pathway of awake mice, we show that cortical representations of sensory inputs are strongly shaped by rapid adaptation, and that this is mediated primarily by adaptive gating of the thalamic inputs to primary sensory cortex and the differential way in which these inputs engage cortical subpopulations of neurons.
快速感觉适应存在于所有感觉系统中，并在复杂的感觉环境中强烈地塑造感觉知觉。尽管它无处不在，可能对生存是必要的，但它的机制基础却知之甚少。大量主要在麻醉状态下的研究已经证明了在初级感觉皮层水平上适应的出现，而在处理的早期阶段只有适度的特征。快速适应的性质以及它在清醒状态下如何塑造感觉表示，从而在感觉适应中潜在的作用，以及支持这种现象的机制，都没有得到充分的探索。为了填补这些知识空白，我们在雄性和雌性小鼠的触须通路中记录了初级体感皮层 (S1) 和上游腹后内侧 (VPm) 丘脑核的尖峰活动，并量化了在孤立和适应感觉背景中呈现的触须刺激的反应。我们发现皮质感觉反应确实受到持续感觉刺激的适应；假定兴奋性神经元被强烈适应，而抑制性神经元则适度适应。进一步的光遗传学操作实验和网络建模表明，这主要反映了同步丘脑放电的适应性变化，以及前馈抑制的强大作用，而突触抑制的贡献很小。总之，这些结果表明，在本文所探讨的范围内，皮质适应是由丘脑输入的时间变化引起的，并且这种变化以不同的方式影响皮质兴奋和前馈抑制，这表明丘脑门控在初级感觉皮层的快速适应中起着重要作用。在数秒的时间尺度上，感觉活动的快速适应强烈地塑造了所有感觉通路的感觉输入的表示，对感觉知觉有深远的影响。尽管它无处不在，在有效编码复杂感觉环境方面具有理论作用，但它的机制基础却知之甚少，尤其是在清醒状态下。在这项针对清醒小鼠触须通路的研究中，我们表明感觉输入的皮质表示强烈受到快速适应的影响，而这主要是由初级感觉皮层的丘脑输入的自适应门控以及这些输入以不同的方式与皮质神经元亚群相互作用介导的。
