Hippocampal conditioning code dominates and disrupts the place code

Area of Science:

• Neuroscience
• Cognitive Neuroscience
• Systems Neuroscience

Background:

• The hippocampus is traditionally considered a spatial mapping system, evidenced by location-specific CA1 neuron activity.
• However, its role in non-spatial learning, like trace eye-blink conditioning, is also established.
• Prior studies suggested spatial encoding during locomotion and non-spatial encoding during immobility.

Purpose of the Study:

• To investigate hippocampal CA1 neural activity during active trace eye-blink conditioning in freely moving rats.
• To determine whether trace coding or place coding predominates during active, non-spatial learning.
• To challenge the prevailing hypothesis of the hippocampus as a stable spatial map.

Main Methods:

• Calcium imaging was used to record activity from thousands of CA1 neurons in rats performing trace eye-blink conditioning.
• Neural activity was analyzed in relation to locomotor speed and task periods.
• Spatial selectivity and task-related modulation of neuronal firing rates were quantified.

Main Results:

• Mean firing rates of CA1 neurons were significantly higher during trace-conditioning periods compared to non-trial periods, even after controlling for locomotion.
• Task-related neuronal modulation was widespread and biased towards increased firing, with task-enhanced neurons outnumbering spatially selective neurons over threefold.
• Spatial coding was reduced during trace periods, characterized by lower spatial information and decreased similarity between task and non-task rate maps.

Conclusions:

• During active behavior, trace coding in the hippocampus predominates over place coding.
• Hippocampal trace coding can disrupt spatial representations, challenging its exclusive role as a stable spatial map.
• These findings highlight the hippocampus's dynamic encoding capabilities during complex, non-spatial learning tasks.