Ermeng Huang1  · Da Xu1  · Huangao Zhu1  · Zhaoqin Chen2,3 · Yulei Chen1,3 · Shujun Lei2,3 · Jiawei Liu1  · Chengyu T. Li1,2,3 · Xiaoxing Zhang2,3

1 Institute of Neuroscience, State Key Laboratory of Neuroscience, CAS Center for Excellence in Brain Science and Intelligence Technology, Chinese Academy of Sciences, Shanghai 200031, China 

2 Shanghai Center for Brain Science and Brain-Inspired Technology, Shanghai 200031, China 

3 Lingang Laboratory, Shanghai 201602, China

Abstract

How do millisecond-scale neural activities mediate second-scale behaviors? We recorded brain-wide activity in mice performing an olfactory working-memory task to decipher the cross-region organization of activity. Spike-correlograms analysis revealed millisecond within- and cross-region spike couplings, which were enriched among memory-encoding neurons with similar odor preferences. Spike coupling linked neurons into motifs of chains, single loops, and nested loops, especially among hippocampal and prefrontal-cortex neurons. Spike-coupling direction and activity-chain propagation aligned with that of memory-associated activity waves. Intriguingly, activity motifs were replayed before and after task performance, and during inter-trial intervals. Motifs exhibited hierarchical organization, with progressively longer time constants and the number of participating neurons. Thus, hierarchically organized and replayed cross-region spiking motifs are modulated on demand during the delay period, providing a potential mechanism for perceptual working-memory maintenance.

Keywords

Global dynamic hierarchy; Replay; Working memory; Functional coupling; Activity loop; Synfire chain; Activity wave; Neuropixels

[SpringerLink]