Abstract
The hippocampus is the main locus of episodic memory formation and the neurons there encode the spatial map of the environment. Hippocampal place cells represent location, but their role in the learning of preferential location remains unclear. The hippocampus may encode locations independently from the stimuli and events that are associated with these locations. We have discovered a unique population code for the experience-dependent value of the context. The degree of reward-driven navigation preference highly correlates with the spatial distribution of the place fields recorded in the CA1 region of the hippocampus. We show place field clustering towards rewarded locations. Optogenetic manipulation of the ventral tegmental area demonstrates that the experience-dependent place field assembly distribution is directed by tegmental dopaminergic activity. The ability of the place cells to remap parallels the acquisition of reward context. Our findings present key evidence that the hippocampal neurons are not merely mapping the static environment but also store the concurrent context reward value, enabling episodic memory for past experience to support future adaptive behavior.
Highlights
The hippocampus mediates the formation of adaptive memory for positive or negative experiences [1], but the neurophysiological mechanisms of this learning process remain unknown [2]
The rats showed 2 types of navigation strategy (Fig 1C): (1) preference for the northeast (NE) corner passes, which was above chance level (S1A Fig, preference group, n = 10), with binomial probability values of p < 0.05 (Fig 1E, S1 Table); i.e., navigation predominantly based on proximal cues, and (2) no preference between corners in which the number of passes to each of the corners was below chance level (S1B Fig, nonpreference group, n = 10), with binomial probability values of p > 0.05 (Fig 1F, S1 Table); i.e., navigation based on opposing proximal and distal cues
Our maze setup allows for a combination of place fields global remapping with concurrent preferential navigation
Summary
The hippocampus mediates the formation of adaptive memory for positive or negative experiences [1], but the neurophysiological mechanisms of this learning process remain unknown [2]. Recent findings deduced artificial association between place cells and place preference through the use of optogenetic [4,5,6] or electrical stimulation [7] These results provide key evidence linking place cell activity and context-dependent encoding of space [8]. It remains unclear if the place cells are coincidence detectors or they actively mediate the learning between reward and location To address this question, we address here 2 possibilities: if place cells don’t integrate information about location and reward, after global remapping, the distribution of place fields should not be biased towards the location previously associated with reward. If place cells do integrate information about both location and reward, after global remapping, the distribution of place fields should be precisely biased towards the location previously associated with reward
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