Cell and Developmental Biology, University College London, Gower Street, London WC1E 6BT, UK.
Neuroscience, Physiology and Pharmacology, University College London, Gower Street, London WC1E 6BT, UK.
Curr Biol. 2019 Mar 4;29(5):834-840.e4. doi: 10.1016/j.cub.2019.01.005. Epub 2019 Feb 14.
Hippocampal place cells encode an animal's current position in space during exploration [1]. During sleep, hippocampal network activity recapitulates patterns observed during recent experience: place cells with overlapping spatial fields show a greater tendency to co-fire ("reactivation") [2], and temporally ordered and compressed sequences of place cell firing observed during wakefulness are reinstated ("replay") [3-5]. Reactivation and replay may underlie memory consolidation [6-10]. Compressed sequences of place cell firing also occur during exploration: during each cycle of the theta oscillation, the set of active place cells shifts from those signaling positions behind to those signaling positions ahead of an animal's current location [11, 12]. These "theta sequences" have been linked to spatial planning [13]. Here, we demonstrate that, before weaning (post-natal day [P]21), offline place cell activity associated with sharp-wave ripples (SWRs) reflects predominantly stationary locations in recently visited environments. By contrast, sequential place cell firing, describing extended trajectories through space during exploration (theta sequences) and subsequent rest (replay), emerge gradually after weaning in a coordinated fashion, possibly due to a progressive decrease in the threshold for experience-driven plasticity. Hippocampus-dependent learning and memory emerge late in altricial mammals [14-17], appearing around weaning in rats and slowly maturing thereafter [14,15]. In contrast, spatially localized firing is observed 1 week earlier (with reduced spatial tuning and stability) [18-21]. By examining the development of hippocampal reactivation, replay, and theta sequences, we show that the coordinated maturation of offline consolidation and online sequence generation parallels the late emergence of hippocampal memory in the rat.
海马体位置细胞在动物探索过程中编码其在空间中的当前位置[1]。在睡眠期间,海马体网络活动再现了最近经验中观察到的模式:具有重叠空间场的位置细胞显示出更大的共同发射(“再激活”)[2],并且在清醒时观察到的时间顺序和压缩的位置细胞发射序列被重新建立(“回放”)[3-5]。再激活和重放可能是记忆巩固的基础[6-10]。在探索过程中也会发生压缩的位置细胞发射序列:在 theta 振荡的每个周期中,活跃的位置细胞集从信号传递动物当前位置后面的位置转移到信号传递动物当前位置前面的位置[11,12]。这些“theta 序列”与空间规划有关[13]。在这里,我们证明了,在断奶(出生后第 21 天)之前,与尖峰波涟漪(SWRs)相关的离线位置细胞活动主要反映了最近访问环境中的静止位置。相比之下,在断奶后协调地逐渐出现描述在探索期间(theta 序列)和随后的休息(重放)中通过空间的扩展轨迹的顺序位置细胞发射,可能是由于经验驱动可塑性的阈值逐渐降低。晚成性哺乳动物的海马体依赖性学习和记忆出现较晚[14-17],在大鼠中大约在断奶时出现,并在此后缓慢成熟[14,15]。相比之下,1 周前就观察到了空间定位发射(具有降低的空间调谐和稳定性)[18-21]。通过检查海马体再激活、重放和 theta 序列的发展,我们表明离线巩固和在线序列生成的协调成熟与大鼠海马体记忆的晚出现平行。