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Higher intrinsic network excitability in ventral compared with the dorsal hippocampus is controlled less effectively by GABAB receptors.

Papatheodoropoulos C - BMC Neurosci (2015)

Bottom Line: Importantly, blockade of GABAB receptors produced a stronger effect in enhancing the probability of generation of spfps and spfps-nmda in the dorsal compared with the ventral hippocampal slices and increased spfps-nmda only in dorsal slices.These results demonstrate a higher intrinsic neuronal excitability of the ventral compared with the dorsal local circuitry with the considerable contribution of NMDA receptors.It is proposed that NMDA and GABAB receptors significantly contribute to differentiate local network dynamics between the dorsal and the ventral hippocampus with important implications in the information processing performed along the long hippocampal axis.

View Article: PubMed Central - PubMed

Affiliation: Laboratory of Physiology, Department of Medicine, School of Health Sciences, University of Patras, Rion, 26504, Patras, Greece. cepapath@upatras.gr.

ABSTRACT

Background: Elucidating specializations of the intrinsic neuronal network between the dorsal and the ventral hippocampus is a recently emerging area of research that is expected to help us understand the mechanisms underlying large scale functional diversification along the hippocampus. The aim of this study was to characterize spontaneous network activity between the dorsal and the ventral hippocampus induced under conditions of partial or complete blockade of GABAergic inhibition (i.e. disinhibition).

Results: Using field recordings from the CA3 and CA1 fields of hippocampal slices from adult rats I found that ventral compared with dorsal hippocampus slices displayed higher propensity for and higher frequency of occurrence of spontaneous field potentials (spfps) at every level of disinhibition. Also NMDA receptor-depended spfps (spfps-nmda) occurred with higher probability more frequently and were larger in the ventral compared with the dorsal hippocampus. Importantly, blockade of GABAB receptors produced a stronger effect in enhancing the probability of generation of spfps and spfps-nmda in the dorsal compared with the ventral hippocampal slices and increased spfps-nmda only in dorsal slices.

Conclusion: These results demonstrate a higher intrinsic neuronal excitability of the ventral compared with the dorsal local circuitry with the considerable contribution of NMDA receptors. Furthermore, the GABAB receptors control the total and the NMDA receptor-dependent excitation much less effectively in the ventral part of the hippocampus. It is proposed that NMDA and GABAB receptors significantly contribute to differentiate local network dynamics between the dorsal and the ventral hippocampus with important implications in the information processing performed along the long hippocampal axis.

No MeSH data available.


Related in: MedlinePlus

The rate of spfps correlates with the position of the slice along the ventral but not the dorsal hippocampus. a Example recordings illustrating that slices taken from more extreme locations in the VH but not the DH displayed higher rates of spfps. The number on the left of each trace indicates the position of the slice along the dorsoventral axis of the hippocampus. b Cumulative graph showing that the rate of spfps was linearly correlated with the distance of the slice from the ventral but not the dorsal end of the hippocampus. The numbers in abscissa correspond to the successive locations along the dorsoventral axis of the structure that slices were taken from. Thus, about twenty positions for 500–550 μm thick slices can be allocated along the entire rat hippocampus which is 10–11 mm long. The medial part of the hippocampus (i.e. locations 9–12) is not shown for clarity reasons. Data were obtained from all SR 95531 concentrations. Only slices that displayed spfps were included in the analysis. The ANOVA test showed that the rate of spfps differed along the VH (F = 6.29, p < 0.001) but not along the DH
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Fig2: The rate of spfps correlates with the position of the slice along the ventral but not the dorsal hippocampus. a Example recordings illustrating that slices taken from more extreme locations in the VH but not the DH displayed higher rates of spfps. The number on the left of each trace indicates the position of the slice along the dorsoventral axis of the hippocampus. b Cumulative graph showing that the rate of spfps was linearly correlated with the distance of the slice from the ventral but not the dorsal end of the hippocampus. The numbers in abscissa correspond to the successive locations along the dorsoventral axis of the structure that slices were taken from. Thus, about twenty positions for 500–550 μm thick slices can be allocated along the entire rat hippocampus which is 10–11 mm long. The medial part of the hippocampus (i.e. locations 9–12) is not shown for clarity reasons. Data were obtained from all SR 95531 concentrations. Only slices that displayed spfps were included in the analysis. The ANOVA test showed that the rate of spfps differed along the VH (F = 6.29, p < 0.001) but not along the DH

Mentions: Spontaneous field potentials (spfps) induced under conditions of blockade of GABAARs (Fig. 1b) were comparatively studied in DH and VH slices (Fig. 1c). GABAAR-mediated transmission was reduced by applying different concentrations of the antagonist of GABAAR SR 95531, from 0.1 to 10 μM. The incidence of spfps in the slice population (i.e. the percentage of slices displaying spfps) and the rate of spfps in each drug concentration were measured in DH and VH. Perfusing slices with increasing concentrations of SR 95531 induced the appearance of spfps in a, respectively, increasing number of slices, in both DH and VH. Furthermore, the incidence of spfps was very different between DH and VH at all concentrations of SR 95531 used (Fig. 1d). In particular, the incidence of spfps at the drug concentrations of 0.1, 0.2, 0.3, 0.5, 1 and 10 μM were 0 % (15), 6.3 ± 2.8 % (32), 11.8 ± 7.1 % (17), 47.5 ± 11.8 % (66), 57.6 ± 9.4 % (57) and 60.0 ± 13.6 % (35), respectively, in DH and 30.0 ± 7.1 % (20), 41.0 ± 13.7 % (31), 77.8 ± 1.8 % (18), 86.2 ± 6.2 % (56), 85.2 ± 7.5 (37) and 90.4 ± 8.0 % (32), respectively, in VH. The difference in incidence between DH and VH was significantly different at every drug concentration (Mann–Whitney U test and χ2 test, p < 0.05). The calculation of the total incidence’s values (i.e. taking into account all drug concentrations) gave 29.1 ± 11.0 % for DH and 68.4 ± 10.6 % for VH (Mann–Whitney U test and χ2 test, p < 0.05). The rate of spfps was several folds higher in VH compared with DH at all drug concentrations (Fig. 1e). In particular, the rate of spfps at the drug concentrations of 0.1, 0.2, 0.3, 0.5, 1 and 10 μM were 0, 4.7 ± 0.9 % (2), 3.4 ± 0.6 % (2), 4.3 ± 0.6 % (25), 2.0 ± 0.3 % (30) and 2.0 ± 0.9 % (20), respectively, in DH and 3.1 ± 1.3 % (6), 14.7 ± 1.8 % (12), 14.8 ± 4.1 % (13), 23.7 ± 1.9 % (48), 22.7 ± 2.1 (26) and 17.3 ± 2.7 % (29), respectively, in VH. The difference in the rate of spfps between DH and VH was significantly different at every drug concentration (Mann–Whitney U-test, p < 0.05 or p < 0.01, see Fig. 1e). The overall rate of spfps (i.e. taking into account all drug concentrations) was 2.3 ± 0.7 spfps/min for DH and 16.0 ± 3.0 spfps/min for VH (Mann–Whitney U test, p < 0.01). An interesting observation was that the rate of spfps was significantly correlated with the precise location of the VH but not DH slices in the long axis of the structure. As shown in Fig. 2, the rate of spfps was significantly higher in slices taken from more extreme compared with more medial positions in the VH but not the DH, regardless the concentration of SR 95531. Specifically, the rate of spfps increased from about 5 spfps/min in slices located 3.5–4.0 mm from the ventral end to about 35 spfps/min in the slices obtained from the extreme 1.0 mm of the VH (ANOVA, F = 6.29, p < 0.001). On the contrary, the rate of spfps was quite comparable among slices obtained from the DH (ANOVA, F = 1.85, p > 0.1).Fig. 2


Higher intrinsic network excitability in ventral compared with the dorsal hippocampus is controlled less effectively by GABAB receptors.

Papatheodoropoulos C - BMC Neurosci (2015)

The rate of spfps correlates with the position of the slice along the ventral but not the dorsal hippocampus. a Example recordings illustrating that slices taken from more extreme locations in the VH but not the DH displayed higher rates of spfps. The number on the left of each trace indicates the position of the slice along the dorsoventral axis of the hippocampus. b Cumulative graph showing that the rate of spfps was linearly correlated with the distance of the slice from the ventral but not the dorsal end of the hippocampus. The numbers in abscissa correspond to the successive locations along the dorsoventral axis of the structure that slices were taken from. Thus, about twenty positions for 500–550 μm thick slices can be allocated along the entire rat hippocampus which is 10–11 mm long. The medial part of the hippocampus (i.e. locations 9–12) is not shown for clarity reasons. Data were obtained from all SR 95531 concentrations. Only slices that displayed spfps were included in the analysis. The ANOVA test showed that the rate of spfps differed along the VH (F = 6.29, p < 0.001) but not along the DH
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Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4641374&req=5

Fig2: The rate of spfps correlates with the position of the slice along the ventral but not the dorsal hippocampus. a Example recordings illustrating that slices taken from more extreme locations in the VH but not the DH displayed higher rates of spfps. The number on the left of each trace indicates the position of the slice along the dorsoventral axis of the hippocampus. b Cumulative graph showing that the rate of spfps was linearly correlated with the distance of the slice from the ventral but not the dorsal end of the hippocampus. The numbers in abscissa correspond to the successive locations along the dorsoventral axis of the structure that slices were taken from. Thus, about twenty positions for 500–550 μm thick slices can be allocated along the entire rat hippocampus which is 10–11 mm long. The medial part of the hippocampus (i.e. locations 9–12) is not shown for clarity reasons. Data were obtained from all SR 95531 concentrations. Only slices that displayed spfps were included in the analysis. The ANOVA test showed that the rate of spfps differed along the VH (F = 6.29, p < 0.001) but not along the DH
Mentions: Spontaneous field potentials (spfps) induced under conditions of blockade of GABAARs (Fig. 1b) were comparatively studied in DH and VH slices (Fig. 1c). GABAAR-mediated transmission was reduced by applying different concentrations of the antagonist of GABAAR SR 95531, from 0.1 to 10 μM. The incidence of spfps in the slice population (i.e. the percentage of slices displaying spfps) and the rate of spfps in each drug concentration were measured in DH and VH. Perfusing slices with increasing concentrations of SR 95531 induced the appearance of spfps in a, respectively, increasing number of slices, in both DH and VH. Furthermore, the incidence of spfps was very different between DH and VH at all concentrations of SR 95531 used (Fig. 1d). In particular, the incidence of spfps at the drug concentrations of 0.1, 0.2, 0.3, 0.5, 1 and 10 μM were 0 % (15), 6.3 ± 2.8 % (32), 11.8 ± 7.1 % (17), 47.5 ± 11.8 % (66), 57.6 ± 9.4 % (57) and 60.0 ± 13.6 % (35), respectively, in DH and 30.0 ± 7.1 % (20), 41.0 ± 13.7 % (31), 77.8 ± 1.8 % (18), 86.2 ± 6.2 % (56), 85.2 ± 7.5 (37) and 90.4 ± 8.0 % (32), respectively, in VH. The difference in incidence between DH and VH was significantly different at every drug concentration (Mann–Whitney U test and χ2 test, p < 0.05). The calculation of the total incidence’s values (i.e. taking into account all drug concentrations) gave 29.1 ± 11.0 % for DH and 68.4 ± 10.6 % for VH (Mann–Whitney U test and χ2 test, p < 0.05). The rate of spfps was several folds higher in VH compared with DH at all drug concentrations (Fig. 1e). In particular, the rate of spfps at the drug concentrations of 0.1, 0.2, 0.3, 0.5, 1 and 10 μM were 0, 4.7 ± 0.9 % (2), 3.4 ± 0.6 % (2), 4.3 ± 0.6 % (25), 2.0 ± 0.3 % (30) and 2.0 ± 0.9 % (20), respectively, in DH and 3.1 ± 1.3 % (6), 14.7 ± 1.8 % (12), 14.8 ± 4.1 % (13), 23.7 ± 1.9 % (48), 22.7 ± 2.1 (26) and 17.3 ± 2.7 % (29), respectively, in VH. The difference in the rate of spfps between DH and VH was significantly different at every drug concentration (Mann–Whitney U-test, p < 0.05 or p < 0.01, see Fig. 1e). The overall rate of spfps (i.e. taking into account all drug concentrations) was 2.3 ± 0.7 spfps/min for DH and 16.0 ± 3.0 spfps/min for VH (Mann–Whitney U test, p < 0.01). An interesting observation was that the rate of spfps was significantly correlated with the precise location of the VH but not DH slices in the long axis of the structure. As shown in Fig. 2, the rate of spfps was significantly higher in slices taken from more extreme compared with more medial positions in the VH but not the DH, regardless the concentration of SR 95531. Specifically, the rate of spfps increased from about 5 spfps/min in slices located 3.5–4.0 mm from the ventral end to about 35 spfps/min in the slices obtained from the extreme 1.0 mm of the VH (ANOVA, F = 6.29, p < 0.001). On the contrary, the rate of spfps was quite comparable among slices obtained from the DH (ANOVA, F = 1.85, p > 0.1).Fig. 2

Bottom Line: Importantly, blockade of GABAB receptors produced a stronger effect in enhancing the probability of generation of spfps and spfps-nmda in the dorsal compared with the ventral hippocampal slices and increased spfps-nmda only in dorsal slices.These results demonstrate a higher intrinsic neuronal excitability of the ventral compared with the dorsal local circuitry with the considerable contribution of NMDA receptors.It is proposed that NMDA and GABAB receptors significantly contribute to differentiate local network dynamics between the dorsal and the ventral hippocampus with important implications in the information processing performed along the long hippocampal axis.

View Article: PubMed Central - PubMed

Affiliation: Laboratory of Physiology, Department of Medicine, School of Health Sciences, University of Patras, Rion, 26504, Patras, Greece. cepapath@upatras.gr.

ABSTRACT

Background: Elucidating specializations of the intrinsic neuronal network between the dorsal and the ventral hippocampus is a recently emerging area of research that is expected to help us understand the mechanisms underlying large scale functional diversification along the hippocampus. The aim of this study was to characterize spontaneous network activity between the dorsal and the ventral hippocampus induced under conditions of partial or complete blockade of GABAergic inhibition (i.e. disinhibition).

Results: Using field recordings from the CA3 and CA1 fields of hippocampal slices from adult rats I found that ventral compared with dorsal hippocampus slices displayed higher propensity for and higher frequency of occurrence of spontaneous field potentials (spfps) at every level of disinhibition. Also NMDA receptor-depended spfps (spfps-nmda) occurred with higher probability more frequently and were larger in the ventral compared with the dorsal hippocampus. Importantly, blockade of GABAB receptors produced a stronger effect in enhancing the probability of generation of spfps and spfps-nmda in the dorsal compared with the ventral hippocampal slices and increased spfps-nmda only in dorsal slices.

Conclusion: These results demonstrate a higher intrinsic neuronal excitability of the ventral compared with the dorsal local circuitry with the considerable contribution of NMDA receptors. Furthermore, the GABAB receptors control the total and the NMDA receptor-dependent excitation much less effectively in the ventral part of the hippocampus. It is proposed that NMDA and GABAB receptors significantly contribute to differentiate local network dynamics between the dorsal and the ventral hippocampus with important implications in the information processing performed along the long hippocampal axis.

No MeSH data available.


Related in: MedlinePlus