Johnson R R, Burkhalter A
Department of Anatomy and Neurobiology, Washington University School of Medicine, St. Louis, Missouri 63110, USA.
J Comp Neurol. 1996 May 6;368(3):383-98. doi: 10.1002/(SICI)1096-9861(19960506)368:3<383::AID-CNE5>3.0.CO;2-1.
Visual cortex in mammals is composed of many distinct areas that are linked by reciprocal connections to form a multilevel hierarchy. Ascending information is sent via forward connections from lower to higher areas and is thought to contribute to the emergence of increasingly complex receptive field properties at higher levels. Descending signals are transmitted via feedback connections from higher to lower areas and are believed to provide information about the context in which a stimulus appears, to contribute to modulation of visual responses by attention, and to play a role in memory processes. To determine whether forward and feedback pathways in rat visual cortex constitute distinct intracortical circuits, we have studied the distribution of reciprocal corticocortical inputs to pyramidal cells and gamma-aminobutyric acid (GABA)ergic interneurons. For this purpose, we chose forward and feedback connections between primary visual cortex and the secondary extrastriate lateromedial (LM) area as a model system. Pathways were traced with the axonal marker phaseolus vulgaris-leucoagglutinin. Labeled terminals were identified in the electron microscope, and GABA immunocytochemistry was used to identify the postsynaptic dendritic shafts of GABAergic interneurons. In both pathways, inputs to pyramidal cells were directed preferentially to dendritic spines and not to shafts. In the forward pathway, 90% of labeled inputs were distributed to pyramidal cells and 10% to interneurons. This proportion was similar to that of nearby unlabeled connections in the neuropil, indicating that forward connections are not selective for pyramidal cells or interneurons. In sharp contrast, feedback connections were significantly different from the unlabeled connections and supplied almost exclusively pyramidal cells (98%). Feedback inputs to GABAergic neurons were five times weaker (2%) relative to the forward direction. These structural differences suggest that disynaptic GABAergic inhibition is much stronger in forward than in feedback pathways. Recent physiological experiments have confirmed this prediction (Shao et al. [1995] Soc. Neurosci. Abstr., 21:1274) and we, therefore, conclude that relatively small anatomical differences in the microcircuitry can have important functional consequences. It remains an open question whether generally reciprocal interareal circuits at all levels of the cortical hierarchy are organized in similar fashion.
哺乳动物的视觉皮层由许多不同的区域组成，这些区域通过相互连接形成多级层次结构。上行信息通过从低级区域到高级区域的前馈连接进行传递，被认为有助于在更高层次上出现越来越复杂的感受野特性。下行信号通过从高级区域到低级区域的反馈连接进行传输，据信这些信号可提供有关刺激出现背景的信息，有助于通过注意力调节视觉反应，并在记忆过程中发挥作用。为了确定大鼠视觉皮层中的前馈和反馈通路是否构成不同的皮质内回路，我们研究了锥体细胞和γ-氨基丁酸（GABA）能中间神经元的相互皮质皮质输入的分布。为此，我们选择初级视觉皮层与次级纹外背内侧（LM）区域之间的前馈和反馈连接作为模型系统。用轴突标记物菜豆白细胞凝集素追踪通路。在电子显微镜下识别标记的终末，并使用GABA免疫细胞化学来识别GABA能中间神经元的突触后树突轴。在这两条通路中，锥体细胞的输入优先指向树突棘而非树突轴。在前馈通路中，90%的标记输入分布到锥体细胞，10%分布到中间神经元。这个比例与神经毡中附近未标记连接的比例相似，表明前馈连接对锥体细胞或中间神经元没有选择性。与之形成鲜明对比的是，反馈连接与未标记连接有显著差异，几乎只供应锥体细胞（98%）。相对于前馈方向，对GABA能神经元的反馈输入要弱五倍（2%）。这些结构差异表明，双突触GABA能抑制在前馈通路中比在反馈通路中要强得多。最近的生理学实验证实了这一预测（Shao等人，[1995]《神经科学学会摘要》，21:1274），因此我们得出结论，微回路中相对较小的解剖差异可能会产生重要的功能后果。皮质层次结构各级普遍存在的相互区域间回路是否以类似方式组织，仍是一个悬而未决的问题。
