Department of Neuroscience, Columbia University, New York, NY 10032, USA; Doctoral Program in Neurobiology and Behavior, Columbia University, New York, NY 10027, USA.
Department of Psychiatry, Columbia University, New York, NY 10032, USA; Division of Molecular Therapeutics, New York State Psychiatric Institute, New York, NY 10032, USA.
Neuron. 2022 Mar 2;110(5):783-794.e6. doi: 10.1016/j.neuron.2021.12.003. Epub 2022 Jan 5.
Hippocampal place cells underlie spatial navigation and memory. Remarkably, CA1 pyramidal neurons can form new place fields within a single trial by undergoing rapid plasticity. However, local feedback circuits likely restrict the rapid recruitment of individual neurons into ensemble representations. This interaction between circuit dynamics and rapid feature coding remains unexplored. Here, we developed "all-optical" approaches combining novel optogenetic induction of rapidly forming place fields with 2-photon activity imaging during spatial navigation in mice. We find that induction efficacy depends strongly on the density of co-activated neurons. Place fields can be reliably induced in single cells, but induction fails during co-activation of larger subpopulations due to local circuit constraints imposed by recurrent inhibition. Temporary relief of local inhibition permits the simultaneous induction of place fields in larger ensembles. We demonstrate the behavioral implications of these dynamics, showing that our ensemble place field induction protocol can enhance subsequent spatial association learning.
海马体位置细胞是空间导航和记忆的基础。值得注意的是，CA1 锥体神经元可以通过快速的可塑性在单个试验中形成新的位置场。然而，局部反馈回路可能限制了单个神经元快速被招募到集合表示中。这种电路动力学和快速特征编码之间的相互作用仍然没有得到探索。在这里，我们开发了“全光学”方法，将新型光遗传学诱导的快速形成的位置场与小鼠在空间导航期间的双光子活性成像相结合。我们发现，诱导效率强烈依赖于共同激活神经元的密度。可以在单个细胞中可靠地诱导位置场，但由于递归抑制施加的局部回路限制，在更大的亚群共同激活时诱导失败。局部抑制的暂时缓解允许在更大的集合中同时诱导位置场。我们展示了这些动力学的行为意义，表明我们的集合位置场诱导方案可以增强随后的空间关联学习。
