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

Carasatorre M, Ochoa-Alvarez A, Velázquez-Campos G, Lozano-Flores C, Ramírez-Amaya V, Díaz-Cintra SY - PLoS ONE (2015)

Bottom Line: 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.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.

View Article: PubMed Central - PubMed

Affiliation: Department of "Neurobiología del Desarrollo y Neurofisiología, Instituto de Neurobiología", Universidad Nacional Autónoma de México, Querétaro, México.

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.

No MeSH data available.


Related in: MedlinePlus

Raw catFISH results.The bar graphs (in A and C) show the percentage of Arc-expressing cells in the CA1 (A) and CA3 (C) networks in each epoch. The solid bars represent the proportion of active cells for epoch 1, and the lighter, textured bars represent the proportion of active cells for epoch 2 (*p<0.01 Bonferroni posthoc analysis for all exploration groups vs. the cage control). The percentage of Arc-expressing cells for each classification is shown in B and D. Each bar represents the proportion of nuclear (Diagonal line pattern), cytoplasmic (Dots), or double (Solid) Arc mRNA staining. Note that the proportion of double activated cells in both CA1 and CA3 after the AA exploration condition is larger than other classifications (i.e., nuclear and cytoplasmic), which is particularly clear in the WM-treated animals (*p<0.01 Bonferroni posthoc analysis vs. the cage control).
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pone.0132676.g004: Raw catFISH results.The bar graphs (in A and C) show the percentage of Arc-expressing cells in the CA1 (A) and CA3 (C) networks in each epoch. The solid bars represent the proportion of active cells for epoch 1, and the lighter, textured bars represent the proportion of active cells for epoch 2 (*p<0.01 Bonferroni posthoc analysis for all exploration groups vs. the cage control). The percentage of Arc-expressing cells for each classification is shown in B and D. Each bar represents the proportion of nuclear (Diagonal line pattern), cytoplasmic (Dots), or double (Solid) Arc mRNA staining. Note that the proportion of double activated cells in both CA1 and CA3 after the AA exploration condition is larger than other classifications (i.e., nuclear and cytoplasmic), which is particularly clear in the WM-treated animals (*p<0.01 Bonferroni posthoc analysis vs. the cage control).

Mentions: Once neurons were identified, they were classified according to their cytoplasmic and nuclear Arc mRNA staining, detected with the CY3 signal (Fig 2B and 2C; Fig 3). Neurons whose nuclei were > 60% surrounded by CY3 signal in 4 or more Z-section planes were classified as cytoplasmic Arc-positive cells (Fig 2B and 2C; Fig 3). Neurons with two intense CY3 nuclear foci visible across 3 or more Z-section planes were classified as nuclear Arc-positive cells, and those that fulfilled both criteria were classified as double-activated cells. Cells that did not fulfil any of the previous criteria were considered Arc negative. The analysis yields the proportion of Arc-mRNA positive neurons (from each classification) out of the total population of neurons included in the analysis (Fig 4).


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

Carasatorre M, Ochoa-Alvarez A, Velázquez-Campos G, Lozano-Flores C, Ramírez-Amaya V, Díaz-Cintra SY - PLoS ONE (2015)

Raw catFISH results.The bar graphs (in A and C) show the percentage of Arc-expressing cells in the CA1 (A) and CA3 (C) networks in each epoch. The solid bars represent the proportion of active cells for epoch 1, and the lighter, textured bars represent the proportion of active cells for epoch 2 (*p<0.01 Bonferroni posthoc analysis for all exploration groups vs. the cage control). The percentage of Arc-expressing cells for each classification is shown in B and D. Each bar represents the proportion of nuclear (Diagonal line pattern), cytoplasmic (Dots), or double (Solid) Arc mRNA staining. Note that the proportion of double activated cells in both CA1 and CA3 after the AA exploration condition is larger than other classifications (i.e., nuclear and cytoplasmic), which is particularly clear in the WM-treated animals (*p<0.01 Bonferroni posthoc analysis vs. the cage control).
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4526663&req=5

pone.0132676.g004: Raw catFISH results.The bar graphs (in A and C) show the percentage of Arc-expressing cells in the CA1 (A) and CA3 (C) networks in each epoch. The solid bars represent the proportion of active cells for epoch 1, and the lighter, textured bars represent the proportion of active cells for epoch 2 (*p<0.01 Bonferroni posthoc analysis for all exploration groups vs. the cage control). The percentage of Arc-expressing cells for each classification is shown in B and D. Each bar represents the proportion of nuclear (Diagonal line pattern), cytoplasmic (Dots), or double (Solid) Arc mRNA staining. Note that the proportion of double activated cells in both CA1 and CA3 after the AA exploration condition is larger than other classifications (i.e., nuclear and cytoplasmic), which is particularly clear in the WM-treated animals (*p<0.01 Bonferroni posthoc analysis vs. the cage control).
Mentions: Once neurons were identified, they were classified according to their cytoplasmic and nuclear Arc mRNA staining, detected with the CY3 signal (Fig 2B and 2C; Fig 3). Neurons whose nuclei were > 60% surrounded by CY3 signal in 4 or more Z-section planes were classified as cytoplasmic Arc-positive cells (Fig 2B and 2C; Fig 3). Neurons with two intense CY3 nuclear foci visible across 3 or more Z-section planes were classified as nuclear Arc-positive cells, and those that fulfilled both criteria were classified as double-activated cells. Cells that did not fulfil any of the previous criteria were considered Arc negative. The analysis yields the proportion of Arc-mRNA positive neurons (from each classification) out of the total population of neurons included in the analysis (Fig 4).

Bottom Line: 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.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.

View Article: PubMed Central - PubMed

Affiliation: Department of "Neurobiología del Desarrollo y Neurofisiología, Instituto de Neurobiología", Universidad Nacional Autónoma de México, Querétaro, México.

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.

No MeSH data available.


Related in: MedlinePlus