Hippocampal spatial memory representations in mice are heterogeneously stable.

Area of Science:

• Neuroscience
• Cognitive Neuroscience
• Systems Neuroscience

Background:

• The stability of neural representations supporting memory and behavior is debated.
• Hippocampal place cells exhibit dynamic population changes over time.
• The role of active cell replacement in memory representation evolution is unclear.

Purpose of the Study:

• To investigate how active cell replacement in the hippocampus affects the evolution of neural representations during a spatial memory task.
• To determine if dynamic neural population changes support stable behavioral performance.

Main Methods:

• Calcium imaging in area CA1 of the dorsal hippocampus in mice performing a delayed nonmatching to place task.
• Analysis of neural activity patterns, specifically "splitter" neurons, in relation to task variables like turn direction and task phase.
• Tracking of neuronal population dynamics and cell replacement over multiple weeks of training.

Main Results:

• Hippocampal neurons split their activity based on upcoming turn direction, task phase, or both, even with stable spatial cues.
• Unequal replacement rates of different splitter neuron populations were observed.
• An increase in cells modulated by turn direction and a decrease in cells modulated by both turn direction and task phase were noted.
• Despite population turnover, the ensemble code consistently segregated task dimensions.

Conclusions:

• Hippocampal memory representations can reorganize dynamically and heterogeneously, even when behavior remains stable.
• Active cell replacement contributes to disambiguating unique episodes and reorganizing memory representations.
• The hippocampus maintains stable encoding of task dimensions through dynamic population coding.