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Dendritic morphology, synaptic transmission, and activity of mature granule cells born following pilocarpine-induced status epilepticus in the rat.

Gao F, Song X, Zhu D, Wang X, Hao A, Nadler JV, Zhan RZ - Front Cell Neurosci (2015)

Bottom Line: The complexity, spine density, miniature post-synaptic currents, and activity-regulated cytoskeleton-associated protein (Arc) expression of granule cells born 5 days after SE were studied between 10 and 17 weeks after CAG-GFP retroviral vector-mediated labeling.After maturation, granule cells born after SE did not show denser Arc expression in the resting condition or 2 h after being activated by pentylenetetrazol-induced transient seizure activity than vicinal GFP-unlabeled granule cells.Thus our results suggest that normotopic granule cells born after pilocarpine-induced SE are no more active when mature than age-matched, naturally born granule cells.

View Article: PubMed Central - PubMed

Affiliation: Department of Physiology, Shandong University School of Medicine Jinan, China.

ABSTRACT
To understand the potential role of enhanced hippocampal neurogenesis after pilocarpine-induced status epilepticus (SE) in the development of epilepsy, we quantitatively analyzed the geometry of apical dendrites, synaptic transmission, and activation levels of normotopically distributed mature newborn granule cells in the rat. SE in male Sprague-Dawley rats (between 6 and 7 weeks old) lasting for more than 2 h was induced by an intraperitoneal injection of pilocarpine. The complexity, spine density, miniature post-synaptic currents, and activity-regulated cytoskeleton-associated protein (Arc) expression of granule cells born 5 days after SE were studied between 10 and 17 weeks after CAG-GFP retroviral vector-mediated labeling. Mature granule cells born after SE had dendritic complexity similar to that of granule cells born naturally, but with denser mushroom-like spines in dendritic segments located in the outer molecular layer. Miniature inhibitory post-synaptic currents (mIPSCs) were similar between the controls and rats subjected to SE; however, smaller miniature excitatory post-synaptic current (mEPSC) amplitude with a trend toward less frequent was found in mature granule cells born after SE. After maturation, granule cells born after SE did not show denser Arc expression in the resting condition or 2 h after being activated by pentylenetetrazol-induced transient seizure activity than vicinal GFP-unlabeled granule cells. Thus our results suggest that normotopic granule cells born after pilocarpine-induced SE are no more active when mature than age-matched, naturally born granule cells.

No MeSH data available.


Related in: MedlinePlus

Arc immunoreactivity in newborn granule cells of control and SE rats with or without pentylenetetrazol (PTZ) treatment. Each GFP-labeled cell is indicated by two arrowheads in the middle panel. The scale bar (50 μm) applies to all panels. Note that Arc immunoreactivity in GFP-labeled cells is indistinguishable from surrounding granule cells in the same section. (A) In a PTZ-untreated control rat, Arc immunoreactivity is faint in the soma and dendrites of granule cells. (B) In a PTZ-untreated SE rat, Arc immunoreactivity became denser in the soma and apical dendrites of granule cells than that in PTZ-untreated controls, but the intensity of Arc immunoreactivity in the GFP-labeled cell is clearly indifferent from cells surrounding it. (C) Treatment with PTZ in a control rat increased Arc immunoreactivity in both the soma and apical dendrites of granule cells, including the GFP-labeled one. (D) Treatment with PTZ in an SE rat also increased Arc immunoreactivity in granule cells. However, Arc immunoreactivity in the GFP-labeled cell is similar to the vicinal granule cells unlabeled by GFP.
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Figure 7: Arc immunoreactivity in newborn granule cells of control and SE rats with or without pentylenetetrazol (PTZ) treatment. Each GFP-labeled cell is indicated by two arrowheads in the middle panel. The scale bar (50 μm) applies to all panels. Note that Arc immunoreactivity in GFP-labeled cells is indistinguishable from surrounding granule cells in the same section. (A) In a PTZ-untreated control rat, Arc immunoreactivity is faint in the soma and dendrites of granule cells. (B) In a PTZ-untreated SE rat, Arc immunoreactivity became denser in the soma and apical dendrites of granule cells than that in PTZ-untreated controls, but the intensity of Arc immunoreactivity in the GFP-labeled cell is clearly indifferent from cells surrounding it. (C) Treatment with PTZ in a control rat increased Arc immunoreactivity in both the soma and apical dendrites of granule cells, including the GFP-labeled one. (D) Treatment with PTZ in an SE rat also increased Arc immunoreactivity in granule cells. However, Arc immunoreactivity in the GFP-labeled cell is similar to the vicinal granule cells unlabeled by GFP.

Mentions: After PTZ treatments, tonic-clonic seizures were observed within 2 min in most rats and the intervals between two adjacent clonic seizures got longer over time. We terminated motor seizures by intraperitoneal injection of diazepam 15 min after the appearance of the first motor seizure. In PTZ-untreated controls, dentate granule cells constitutively expressed Arc at low level (Figure 7A). Arc immunoreactivity in granule cells of PTZ-untreated SE animals appeared more intense than that of granule cells in PTZ-untreated controls; however, the intensity of Arc immunoreactivity in the GFP-labeled newborn cells did not exceed that of nearby GFP-negative granule cells (Figure 7B). Treatment of controls with PTZ dramatically enhanced Arc immunoreactivity in the soma and apical dendrites of almost every granule cell (Figure 7C), but again, a difference between GFP-labeled granule cells and granule cells surrounding them could not be noticed. Treatment of SE rats with PTZ also increased Arc immunoreactivity in both the soma and apical dendrites of almost all granule cells and it appeared that the intensity of Arc immunoreactivity in GFP-labeled newborn granule cells was similar to that in adjacent GFP-negative granule cells (Figure 7D). Quantitative analyses that compared Arc immunoreactivity in GFP-labeled cells to the averaged Arc immunoreactivity of surrounding granule cells clearly shows that the intensities of Arc immunoreactivity in GFP-positive somata and dendrites were not different from surrounding granule cells in the resting condition (Figures 7A,B, 8) or during a transient seizure episode (Figures 7C,D, 8). Similar results were observed when c-fos was used as a cellular activity marker (Supplemental Figures 4, 5).


Dendritic morphology, synaptic transmission, and activity of mature granule cells born following pilocarpine-induced status epilepticus in the rat.

Gao F, Song X, Zhu D, Wang X, Hao A, Nadler JV, Zhan RZ - Front Cell Neurosci (2015)

Arc immunoreactivity in newborn granule cells of control and SE rats with or without pentylenetetrazol (PTZ) treatment. Each GFP-labeled cell is indicated by two arrowheads in the middle panel. The scale bar (50 μm) applies to all panels. Note that Arc immunoreactivity in GFP-labeled cells is indistinguishable from surrounding granule cells in the same section. (A) In a PTZ-untreated control rat, Arc immunoreactivity is faint in the soma and dendrites of granule cells. (B) In a PTZ-untreated SE rat, Arc immunoreactivity became denser in the soma and apical dendrites of granule cells than that in PTZ-untreated controls, but the intensity of Arc immunoreactivity in the GFP-labeled cell is clearly indifferent from cells surrounding it. (C) Treatment with PTZ in a control rat increased Arc immunoreactivity in both the soma and apical dendrites of granule cells, including the GFP-labeled one. (D) Treatment with PTZ in an SE rat also increased Arc immunoreactivity in granule cells. However, Arc immunoreactivity in the GFP-labeled cell is similar to the vicinal granule cells unlabeled by GFP.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC4596052&req=5

Figure 7: Arc immunoreactivity in newborn granule cells of control and SE rats with or without pentylenetetrazol (PTZ) treatment. Each GFP-labeled cell is indicated by two arrowheads in the middle panel. The scale bar (50 μm) applies to all panels. Note that Arc immunoreactivity in GFP-labeled cells is indistinguishable from surrounding granule cells in the same section. (A) In a PTZ-untreated control rat, Arc immunoreactivity is faint in the soma and dendrites of granule cells. (B) In a PTZ-untreated SE rat, Arc immunoreactivity became denser in the soma and apical dendrites of granule cells than that in PTZ-untreated controls, but the intensity of Arc immunoreactivity in the GFP-labeled cell is clearly indifferent from cells surrounding it. (C) Treatment with PTZ in a control rat increased Arc immunoreactivity in both the soma and apical dendrites of granule cells, including the GFP-labeled one. (D) Treatment with PTZ in an SE rat also increased Arc immunoreactivity in granule cells. However, Arc immunoreactivity in the GFP-labeled cell is similar to the vicinal granule cells unlabeled by GFP.
Mentions: After PTZ treatments, tonic-clonic seizures were observed within 2 min in most rats and the intervals between two adjacent clonic seizures got longer over time. We terminated motor seizures by intraperitoneal injection of diazepam 15 min after the appearance of the first motor seizure. In PTZ-untreated controls, dentate granule cells constitutively expressed Arc at low level (Figure 7A). Arc immunoreactivity in granule cells of PTZ-untreated SE animals appeared more intense than that of granule cells in PTZ-untreated controls; however, the intensity of Arc immunoreactivity in the GFP-labeled newborn cells did not exceed that of nearby GFP-negative granule cells (Figure 7B). Treatment of controls with PTZ dramatically enhanced Arc immunoreactivity in the soma and apical dendrites of almost every granule cell (Figure 7C), but again, a difference between GFP-labeled granule cells and granule cells surrounding them could not be noticed. Treatment of SE rats with PTZ also increased Arc immunoreactivity in both the soma and apical dendrites of almost all granule cells and it appeared that the intensity of Arc immunoreactivity in GFP-labeled newborn granule cells was similar to that in adjacent GFP-negative granule cells (Figure 7D). Quantitative analyses that compared Arc immunoreactivity in GFP-labeled cells to the averaged Arc immunoreactivity of surrounding granule cells clearly shows that the intensities of Arc immunoreactivity in GFP-positive somata and dendrites were not different from surrounding granule cells in the resting condition (Figures 7A,B, 8) or during a transient seizure episode (Figures 7C,D, 8). Similar results were observed when c-fos was used as a cellular activity marker (Supplemental Figures 4, 5).

Bottom Line: The complexity, spine density, miniature post-synaptic currents, and activity-regulated cytoskeleton-associated protein (Arc) expression of granule cells born 5 days after SE were studied between 10 and 17 weeks after CAG-GFP retroviral vector-mediated labeling.After maturation, granule cells born after SE did not show denser Arc expression in the resting condition or 2 h after being activated by pentylenetetrazol-induced transient seizure activity than vicinal GFP-unlabeled granule cells.Thus our results suggest that normotopic granule cells born after pilocarpine-induced SE are no more active when mature than age-matched, naturally born granule cells.

View Article: PubMed Central - PubMed

Affiliation: Department of Physiology, Shandong University School of Medicine Jinan, China.

ABSTRACT
To understand the potential role of enhanced hippocampal neurogenesis after pilocarpine-induced status epilepticus (SE) in the development of epilepsy, we quantitatively analyzed the geometry of apical dendrites, synaptic transmission, and activation levels of normotopically distributed mature newborn granule cells in the rat. SE in male Sprague-Dawley rats (between 6 and 7 weeks old) lasting for more than 2 h was induced by an intraperitoneal injection of pilocarpine. The complexity, spine density, miniature post-synaptic currents, and activity-regulated cytoskeleton-associated protein (Arc) expression of granule cells born 5 days after SE were studied between 10 and 17 weeks after CAG-GFP retroviral vector-mediated labeling. Mature granule cells born after SE had dendritic complexity similar to that of granule cells born naturally, but with denser mushroom-like spines in dendritic segments located in the outer molecular layer. Miniature inhibitory post-synaptic currents (mIPSCs) were similar between the controls and rats subjected to SE; however, smaller miniature excitatory post-synaptic current (mEPSC) amplitude with a trend toward less frequent was found in mature granule cells born after SE. After maturation, granule cells born after SE did not show denser Arc expression in the resting condition or 2 h after being activated by pentylenetetrazol-induced transient seizure activity than vicinal GFP-unlabeled granule cells. Thus our results suggest that normotopic granule cells born after pilocarpine-induced SE are no more active when mature than age-matched, naturally born granule cells.

No MeSH data available.


Related in: MedlinePlus