Hippocampal Synaptic Expansion Induced by Spatial Experience in Rats Correlates with Improved Information Processing in the Hippocampus.

Mariana Carasatorre,Víctor Ramírez-Amaya,Sofía Y Díaz-Cintra,Giovanna Velázquez-Campos,Adrian Ochoa-Alvarez,Carlos Lozano-Flores,Thierry Amédée

doi:10.1371/journal.pone.0132676

Mariana Carasatorre, Víctor Ramírez-Amaya + Show 5 more

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https://doi.org/10.1371/journal.pone.0132676

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Abstract

Spatial water maze (WM) overtraining induces hippocampal mossy fiber (MF) expansion, and it has been suggested that spatial pattern separation depends on the MF pathway. We hypothesized that WM experience inducing MF expansion in rats would improve spatial pattern separation in the hippocampal network. We first tested this by using the the delayed non-matching to place task (DNMP), in animals that had been previously trained on the water maze (WM) and found that these animals, as well as animals treated as swim controls (SC), performed better than home cage control animals the DNMP task. The “catFISH” imaging method provided neurophysiological evidence that hippocampal pattern separation improved in animals treated as SC, and this improvement was even clearer in animals that experienced the WM training. Moreover, these behavioral treatments also enhance network reliability and improve partial pattern separation in CA1 and pattern completion in CA3. By measuring the area occupied by synaptophysin staining in both the stratum oriens and the stratun lucidum of the distal CA3, we found evidence of structural synaptic plasticity that likely includes MF expansion. Finally, the measures of hippocampal network coding obtained with catFISH correlate significantly with the increased density of synaptophysin staining, strongly suggesting that structural synaptic plasticity in the hippocampus induced by the WM and SC experience is related to the improvement of spatial information processing in the hippocampus.

Highlights

Behavioral experience promotes structural synaptic plasticity [1]
Morris water maze overtraining improves the performance in a delay non-matching to place (DNMP) task Since the DNMP task was previously used to measure spatial pattern separation and WM training induces mossy fiber expansion, we test the hypothesis that WM training inducing MF expansion could improve the performance of animals in the DNMP task
Training in the WM consisted of 5 daily sessions of 10 trials each, and the latency to reach the target in each pair of trials (5 pairs) was used for statistical analysis

Summary

Introduction

One remarkable example is the observation that overtraining rats in the Morris water maze (WM) spatial task induces mossy fiber (MF) expansion in the hippocampal CA3 region [2, 3, 4]. This is observed across different rat strains with slightly different remodeling dynamics [4] and in mice [5] in response to environmental enrichment and fear conditioning [6, 7]. The MFs promote pattern separation in the CA3 network [13, 16]; this process transforms similar inputs into less-overlapping outputs, allowing us to discriminate between similar experiences and store them separately [17, 18]. Later, during retrieval, even when a partial or distorted input is presented to the animal, the CA3 network is able to perform pattern completion [17, 18], but this process is thought to be directed by the perforant pathway [13]

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