Gellért Levente, Luhmann Heiko J, Kilb Werner
Institute of Physiology, University Medical Center of the Johannes Gutenberg University Mainz, Mainz, Germany.
Front Neuroanat. 2023 Jan 25;17:1105998. doi: 10.3389/fnana.2023.1105998. eCollection 2023.
The development of functionally interconnected networks between primary (S1), secondary somatosensory (S2), and motor (M1) cortical areas requires coherent neuronal activity corticocortical projections. However, the anatomical substrate of functional connections between S1 and M1 or S2 during early development remains elusive. In the present study, we used carbocyanine dye (DiI) tracing in paraformaldehyde-fixed newborn mouse brain to investigate axonal projections of neurons in different layers of S1 barrel field (S1Bf), M1, and S2 toward the subplate (SP), a hub layer for sensory information transfer in the immature cortex. In addition, we performed extracellular recordings in neocortical slices to unravel the functional connectivity between these areas. Our experiments demonstrate that already at P0 neurons from the cortical plate (CP), layer 5/6 (L5/6), and the SP of both M1 and S2 send projections through the SP of S1Bf. Reciprocally, neurons from CP to SP of S1Bf send projections through the SP of M1 and S2. Electrophysiological recordings with multi-electrode arrays in cortical slices revealed weak, but functional synaptic connections between SP and L5/6 within and between S1 and M1. An even lower functional connectivity was observed between S1 and S2. In summary, our findings demonstrate that functional connections between SP and upper cortical layers are not confined to the same cortical area, but corticocortical connection between adjacent cortical areas exist already at the day of birth. Hereby, SP can integrate early cortical activity of M1, S1, and S2 and shape the development of sensorimotor integration at an early stage.
初级躯体感觉皮层(S1)、次级躯体感觉皮层(S2)和运动皮层(M1)区域之间功能互联网络的发育需要连贯的神经元活动和皮质-皮质投射。然而,在早期发育过程中,S1与M1或S2之间功能连接的解剖学基础仍不清楚。在本研究中,我们使用在多聚甲醛固定的新生小鼠大脑中进行的羰花青染料(DiI)示踪,来研究S1桶状区(S1Bf)、M1和S2不同层的神经元向亚板层(SP)的轴突投射,亚板层是未成熟皮层中感觉信息传递的枢纽层。此外,我们在新皮层切片中进行了细胞外记录,以揭示这些区域之间的功能连接。我们的实验表明,在出生后第0天(P0),来自M1和S2的皮质板(CP)、第5/6层(L5/6)以及亚板层的神经元就通过S1Bf的亚板层发出投射。反过来,从S1Bf的CP到亚板层的神经元通过M1和S2的亚板层发出投射。在皮质切片中使用多电极阵列进行的电生理记录显示,S1和M1内部及之间的亚板层与L5/6之间存在微弱但功能性的突触连接。在S1和S2之间观察到的功能连接性甚至更低。总之,我们的研究结果表明,亚板层与上层皮质之间的功能连接并不局限于同一皮质区域,相邻皮质区域之间的皮质-皮质连接在出生时就已存在。因此,亚板层可以整合M1、S1和S2的早期皮质活动,并在早期塑造感觉运动整合的发育。