Shallow Molly C, Tian Lucy, Lin Hudson, Lefton Katheryn B, Chen Siyu, Dougherty Joseph D, Culver Joe P, Lambo Mary E, Hengen Keith B
Department of Biology, Washington University in Saint Louis.
Department of Neuroscience, Washington University in Saint Louis.
bioRxiv. 2024 Jun 5:2024.06.04.597353. doi: 10.1101/2024.06.04.597353.
The development of motor control over sensory organs is a critical milestone in sensory processing, enabling active exploration and shaping of the sensory environment. However, whether the onset of sensory organ motor control directly influences the development of corresponding sensory cortices remains unknown. Here, we exploit the late onset of whisking behavior in mice to address this question in the somatosensory system. Using ex vivo electrophysiology, we discovered a transient increase in the intrinsic excitability of excitatory neurons in layer IV of the barrel cortex, which processes whisker input, precisely coinciding with the onset of active whisking at postnatal day 14 (P14). This increase in neuronal gain was specific to layer IV, independent of changes in synaptic strength, and required prior sensory experience. Strikingly, the effect was not observed in layer II/III of the barrel cortex or in the visual cortex upon eye opening, suggesting a unique interaction between the development of active sensing and the thalamocortical input layer in the somatosensory system. Predictive modeling indicated that changes in active membrane conductances alone could reliably distinguish P14 neurons in control but not whisker-deprived hemispheres. Our findings demonstrate an experience-dependent, lamina-specific refinement of neuronal excitability tightly linked to the emergence of active whisking. This transient increase in the gain of the thalamic input layer coincides with a critical period for synaptic plasticity in downstream layers, suggesting a role in facilitating cortical maturation and sensory processing. Together, our results provide evidence for a direct interaction between the development of motor control and sensory cortex, offering new insights into the experience-dependent development and refinement of sensory systems. These findings have broad implications for understanding the interplay between motor and sensory development, and how the mechanisms of perception cooperate with behavior.
对感觉器官的运动控制的发展是感觉处理中的一个关键里程碑，它能够对感觉环境进行主动探索和塑造。然而，感觉器官运动控制的开始是否直接影响相应感觉皮层的发育仍然未知。在这里，我们利用小鼠中触须行为出现较晚的特点，在体感系统中解决这个问题。通过离体电生理学，我们发现处理触须输入的桶状皮层第IV层兴奋性神经元的内在兴奋性出现短暂增加，这与出生后第14天（P14）主动触须行为的开始恰好吻合。这种神经元增益的增加是第IV层特有的，与突触强度的变化无关，并且需要先前的感觉经验。引人注目的是，在桶状皮层的第II/III层或视觉皮层睁眼时并未观察到这种效应，这表明主动感觉的发展与体感系统中的丘脑皮质输入层之间存在独特的相互作用。预测模型表明，仅主动膜电导的变化就能可靠地区分对照半球而非触须剥夺半球中的P14神经元。我们的研究结果表明，神经元兴奋性的经验依赖性、层特异性细化与主动触须行为的出现紧密相关。丘脑输入层增益的这种短暂增加与下游层突触可塑性的关键期相吻合，表明其在促进皮层成熟和感觉处理中发挥作用。总之，我们的结果为运动控制和感觉皮层的发展之间的直接相互作用提供了证据，为感觉系统的经验依赖性发展和细化提供了新的见解。这些发现对于理解运动和感觉发展之间的相互作用以及感知机制如何与行为协作具有广泛的意义。
