Hippocampal CA1 place cell spatial maps are known to alter their firing properties in response to contextual fear conditioning, a process called "remapping." In the present study, we use chronic calcium imaging to examine remapping during fear retrieval and extinction of an inhibitory avoidance task in mice of both sexes over an extended period of time and with thousands of neurons. We demonstrate that hippocampal ensembles encode space at a finer scale following fear memory acquisition. This effect is strongest near the shock grid. We also characterize the long-term effects of shock on place cell ensemble stability, demonstrating that shock delivery induces several days of high fear and low between-session place field stability, followed by a new, stable spatial representation that appears after fear extinction. Finally, we identify a novel group of CA1 neurons that robustly encode freeze behavior independently from spatial location. Thus, following fear acquisition, hippocampal CA1 place cells sharpen their spatial tuning and dynamically change spatial encoding stability throughout fear learning and extinction.

SIGNIFICANCE STATEMENT The hippocampus contains place cells that encode an animal's location. This spatial code updates, or remaps, in response to environmental change. It is known that contextual fear can induce such remapping; in the present study, we use chronic calcium imaging to examine inhibitory avoidance-induced remapping over an extended period of time and with thousands of neurons and demonstrate that hippocampal ensembles encode space at a finer scale following electric shock, an effect which is enhanced by threat proximity. We also identify a novel group of freeze behavior-activated neurons. These results suggest that, more than merely shuffling their spatial code following threat exposure, place cells enhance their spatial coding with the possible benefit of improved threat localization.

已知海马CA1位置细胞空间图会根据情境恐惧条件改变其放电特性，这一过程称为“重新映射”。在本研究中，我们使用慢性钙成像来检查恐惧症恢复过程中的重映射以及抑制性避免任务的消失，这两种性别的小鼠在较长的时间内都具有成千上万的神经元。我们证明恐惧记忆获得后海马合奏以较小的规模编码空间。在冲击网格附近，此效果最强。我们还表征了电击对位置细胞集合稳定性的长期影响，证明电击传递会引起几天的高恐惧和低会话间位置场稳定性，然后在恐惧消失后出现新的，稳定的空间表示。最后，我们确定了一组新的CA1神经元，它们独立于空间位置来稳定地编码冻结行为。因此，恐惧获得后，海马CA1放置细胞会增强其空间调节能力，并在恐惧学习和灭绝过程中动态改变空间编码的稳定性。

重要声明海马包含编码动物位置的位置细胞。该空间代码会根据环境变化进行更新或重新映射。众所周知，情境恐惧会引起这种重新映射。在本研究中，我们使用慢性钙成像检查了长时间内和成千上万个神经元的抑制性避免诱发的重映射，并证明了电击后海马集成体以较小的尺度编码空间，这种效应会因受到威胁而增强接近。我们还确定了一组新的冻结行为激活神经元。这些结果表明，不仅仅是威胁暴露后改组其空间代码，放置单元还可以增强其空间编码，并具有改善威胁定位的可能好处。