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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

Higher incidence and rate of disinhibition-induced spfps in VH compared with DH. a Schematic drawing of the hippocampus where the cutting plane directions and the extent of sliced structure are indicated by the solid lines. Dotted line indicates the longitudinal axis of the structure. b Fast sweep speed record of a single spontaneous field potential (spfp) induced under blockade of GABAARs by their antagonist SR 95531. Recording was made in the CA3 stratum pyramidale of a VH slice. c Continuous recordings from the CA3 stratum pyramidale illustrating that at the low concentration of 0.1 μM the antagonist of GABAARs SR 95531 induced spfps in VH but not DH. Even at the highest concentration of SR 95531 used (10 μM) the rate of spfps was higher in VH than in DH. d Histogram of percentages of DH and VH slices displaying spfps under different concentrations of SR 95531 (plot on the left) and the cumulative results for all concentrations (plot on the right) are shown. The number of slices examined under the six different drug concentrations are given in the main text. e Histogram of the rate of spfps in DH and VH under the various SR 95531 concentrations and the cumulative mean values for all concentrations are shown in the left and right graph, respectively. Asterisks in all graphs denote statistically significant differences between DH and VH at *p < 0.05 or **p < 0.01 (Mann–Whitney U test). Statistical comparison at 0.1 μM was not possible because of the absence of spfps in DH slices
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Fig1: Higher incidence and rate of disinhibition-induced spfps in VH compared with DH. a Schematic drawing of the hippocampus where the cutting plane directions and the extent of sliced structure are indicated by the solid lines. Dotted line indicates the longitudinal axis of the structure. b Fast sweep speed record of a single spontaneous field potential (spfp) induced under blockade of GABAARs by their antagonist SR 95531. Recording was made in the CA3 stratum pyramidale of a VH slice. c Continuous recordings from the CA3 stratum pyramidale illustrating that at the low concentration of 0.1 μM the antagonist of GABAARs SR 95531 induced spfps in VH but not DH. Even at the highest concentration of SR 95531 used (10 μM) the rate of spfps was higher in VH than in DH. d Histogram of percentages of DH and VH slices displaying spfps under different concentrations of SR 95531 (plot on the left) and the cumulative results for all concentrations (plot on the right) are shown. The number of slices examined under the six different drug concentrations are given in the main text. e Histogram of the rate of spfps in DH and VH under the various SR 95531 concentrations and the cumulative mean values for all concentrations are shown in the left and right graph, respectively. Asterisks in all graphs denote statistically significant differences between DH and VH at *p < 0.05 or **p < 0.01 (Mann–Whitney U test). Statistical comparison at 0.1 μM was not possible because of the absence of spfps in DH slices

Mentions: Forty-five adult (2–4 months old) male Wistar rats (Athens Pasteur Institute) were used in this study. Animals were obtained from the Animal Facility of the Medical School of the University of Patras. All experimental treatment and procedures were conducted in accordance with the European Communities Council Directive Guidelines (86/609/EEC, JL 358, 1, December, 12, 1987) for the care and use of Laboratory animals and they have been approved by the Prefectural Animal Care and Use Committee (No: EL 13BIO04). In addition, all efforts have been made to minimize the number and the suffering of animals used. Animals were housed in a room with a controlled light–dark cycle (12 h light–12 h dark) and free access to food and water. Slices from the two hippocampal poles were prepared as follows. The animals after deep anesthesia with diethyl ether were decapitated with a guillotine and their brain was removed and submerged in chilled (2–4 °C) standard medium containing (in mM): 124 NaCl; 4 KCl; 2 MgSO4; 2 CaCl2; 1.25 NaH2PO4; 26 NaHCO3; 10 glucose; at pH 7.4, and the two hippocampi were excised free. Using a McIlwain tissue chopper, 500–550 µm thick slices, transverse to the long axis of hippocampus, were prepared from the ventral (temporal) and the dorsal (septal) parts of the structure. In particular, slices were prepared from the regions extending between about 0.1 and 4.5 mm from the dorsal and the ventral ends of the hippocampus (Fig. 1a). These slices will be referred to as dorsal (DH) and ventral (VH) hippocampal slices. In each experiment, slices from both DH and VH from the same hippocampus or from the hippocampi of the same animal were used. In particular, 227 DH and 233 VH slices were studied. Immediately after sectioning, the slices were transferred to an interface type recording chamber where they were maintained at a constant temperature of 31 ± 0.5 °C, continuously humidified with a mixed gas containing 95 % O2 and 5 % CO2 and perfused with standard artificial cerebrospinal fluid.Fig. 1


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

Papatheodoropoulos C - BMC Neurosci (2015)

Higher incidence and rate of disinhibition-induced spfps in VH compared with DH. a Schematic drawing of the hippocampus where the cutting plane directions and the extent of sliced structure are indicated by the solid lines. Dotted line indicates the longitudinal axis of the structure. b Fast sweep speed record of a single spontaneous field potential (spfp) induced under blockade of GABAARs by their antagonist SR 95531. Recording was made in the CA3 stratum pyramidale of a VH slice. c Continuous recordings from the CA3 stratum pyramidale illustrating that at the low concentration of 0.1 μM the antagonist of GABAARs SR 95531 induced spfps in VH but not DH. Even at the highest concentration of SR 95531 used (10 μM) the rate of spfps was higher in VH than in DH. d Histogram of percentages of DH and VH slices displaying spfps under different concentrations of SR 95531 (plot on the left) and the cumulative results for all concentrations (plot on the right) are shown. The number of slices examined under the six different drug concentrations are given in the main text. e Histogram of the rate of spfps in DH and VH under the various SR 95531 concentrations and the cumulative mean values for all concentrations are shown in the left and right graph, respectively. Asterisks in all graphs denote statistically significant differences between DH and VH at *p < 0.05 or **p < 0.01 (Mann–Whitney U test). Statistical comparison at 0.1 μM was not possible because of the absence of spfps in DH slices
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

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

Fig1: Higher incidence and rate of disinhibition-induced spfps in VH compared with DH. a Schematic drawing of the hippocampus where the cutting plane directions and the extent of sliced structure are indicated by the solid lines. Dotted line indicates the longitudinal axis of the structure. b Fast sweep speed record of a single spontaneous field potential (spfp) induced under blockade of GABAARs by their antagonist SR 95531. Recording was made in the CA3 stratum pyramidale of a VH slice. c Continuous recordings from the CA3 stratum pyramidale illustrating that at the low concentration of 0.1 μM the antagonist of GABAARs SR 95531 induced spfps in VH but not DH. Even at the highest concentration of SR 95531 used (10 μM) the rate of spfps was higher in VH than in DH. d Histogram of percentages of DH and VH slices displaying spfps under different concentrations of SR 95531 (plot on the left) and the cumulative results for all concentrations (plot on the right) are shown. The number of slices examined under the six different drug concentrations are given in the main text. e Histogram of the rate of spfps in DH and VH under the various SR 95531 concentrations and the cumulative mean values for all concentrations are shown in the left and right graph, respectively. Asterisks in all graphs denote statistically significant differences between DH and VH at *p < 0.05 or **p < 0.01 (Mann–Whitney U test). Statistical comparison at 0.1 μM was not possible because of the absence of spfps in DH slices
Mentions: Forty-five adult (2–4 months old) male Wistar rats (Athens Pasteur Institute) were used in this study. Animals were obtained from the Animal Facility of the Medical School of the University of Patras. All experimental treatment and procedures were conducted in accordance with the European Communities Council Directive Guidelines (86/609/EEC, JL 358, 1, December, 12, 1987) for the care and use of Laboratory animals and they have been approved by the Prefectural Animal Care and Use Committee (No: EL 13BIO04). In addition, all efforts have been made to minimize the number and the suffering of animals used. Animals were housed in a room with a controlled light–dark cycle (12 h light–12 h dark) and free access to food and water. Slices from the two hippocampal poles were prepared as follows. The animals after deep anesthesia with diethyl ether were decapitated with a guillotine and their brain was removed and submerged in chilled (2–4 °C) standard medium containing (in mM): 124 NaCl; 4 KCl; 2 MgSO4; 2 CaCl2; 1.25 NaH2PO4; 26 NaHCO3; 10 glucose; at pH 7.4, and the two hippocampi were excised free. Using a McIlwain tissue chopper, 500–550 µm thick slices, transverse to the long axis of hippocampus, were prepared from the ventral (temporal) and the dorsal (septal) parts of the structure. In particular, slices were prepared from the regions extending between about 0.1 and 4.5 mm from the dorsal and the ventral ends of the hippocampus (Fig. 1a). These slices will be referred to as dorsal (DH) and ventral (VH) hippocampal slices. In each experiment, slices from both DH and VH from the same hippocampus or from the hippocampi of the same animal were used. In particular, 227 DH and 233 VH slices were studied. Immediately after sectioning, the slices were transferred to an interface type recording chamber where they were maintained at a constant temperature of 31 ± 0.5 °C, continuously humidified with a mixed gas containing 95 % O2 and 5 % CO2 and perfused with standard artificial cerebrospinal fluid.Fig. 1

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