Preconfigured patterns are the primary driver of offline multi-neuronal sequence replay

Area of Science:

• Neuroscience
• Systems Neuroscience
• Cognitive Neuroscience

Background:

• Hippocampal spontaneous neuronal activity arises from internal dynamics and recent experiences.
• Preconfigured neuronal patterns (preplay) influence future place cell sequences and post-experience replay.
• The contribution of internal versus experience-driven factors to replay is assumed to favor recent experience.

Purpose of the Study:

• To directly compare the contributions of internally generated and experience-driven factors to hippocampal sequential activity during post-run sleep.
• To investigate the influence of de novo spatial experience on preconfigured network dynamics.

Main Methods:

• Utilized multi-neuronal sequence analysis, unbiased by firing rate, in naïve adult rats.
• Directly computed and compared contributions of pre-run (internal) and post-run (experience-driven) factors.
• Analyzed sequential neuronal activity during post-run sleep following a de novo run session.

Main Results:

• Multi-neuronal sequences during post-run sleep were predominantly driven by pre-run, internally generated patterns.
• Sequences associated with recent awake experience contributed to a much smaller extent.
• Awake and sleep sequences showed weak, similar correlations, indicating limited impact of de novo experience.

Conclusions:

• The hippocampal network exhibits a robust default internal organization into sequential ensembles.
• This internal organization withstands de novo spatial experiences.
• Integration of novel information during de novo experience leads to more subtle lasting changes than previously assumed.