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Involvement of the GABAergic septo-hippocampal pathway in brain stimulation reward.

Vega-Flores G, Gruart A, Delgado-García JM - PLoS ONE (2014)

Bottom Line: The successive BSR sessions evoked a progressive increase of the performance in inverse relationship with a decrease in the amplitude of fEPSPs, but not of fIPSPs.We corroborate a clear preference for BSR at 100 Hz (in comparison with BSR at 20 Hz or 8 Hz), in parallel with an increase in the spectral power of the low theta band, and a decrease in the gamma.These results were replicated by intrahippocampal injections of a GABAB antagonist.

View Article: PubMed Central - PubMed

Affiliation: Division of Neurosciences, Pablo de Olavide University, Seville, Spain.

ABSTRACT
The hippocampus is a structure related to several cognitive processes, but not very much is known about its putative involvement in positive reinforcement. In its turn, the septum has been related to instrumental brain stimulation reward (BSR) by its electrical stimulation with trains of pulses. Although the anatomical relationships of the septo-hippocampal pathway are well established, the functional relationship between these structures during rewarding behaviors remains poorly understood. To explore hippocampal mechanisms involved in BSR, CA3-evoked field excitatory and inhibitory postsynaptic potentials (fEPSPs, fIPSPs) were recorded in the CA1 area during BSR in alert behaving mice. The synaptic efficiency was determined from changes in fEPSP and fIPSP amplitudes across the learning of a BSR task. The successive BSR sessions evoked a progressive increase of the performance in inverse relationship with a decrease in the amplitude of fEPSPs, but not of fIPSPs. Additionally, we evaluated CA1 local field potentials (LFPs) during a preference task, comparing 8-, 20-, and 100-Hz trains of septal BSR. We corroborate a clear preference for BSR at 100 Hz (in comparison with BSR at 20 Hz or 8 Hz), in parallel with an increase in the spectral power of the low theta band, and a decrease in the gamma. These results were replicated by intrahippocampal injections of a GABAB antagonist. Thus, the GABAergic septo-hippocampal pathway seems to carry information involved in the encoding of reward properties, where GABAB receptors seem to play a key role. With regard to the dorsal hippocampus, fEPSPs evoked at the CA3-CA1 synapse seem to reflect the BSR learning process, while hippocampal rhythmic activities are more related to reward properties.

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Effects of intrahippocampal injection of CGP 35348 on BSR performance and the associated fPSP changes.(A) The upper panel shows representative fPSPs (averaged 15 times) evoked at the CA3-CA1 synapse before injection (black solid line), in the presence of vehicle (gray dotted line) or following CGP injection (gray solid line). The bottom histograms illustrate the averaged fPSP amplitudes corresponding to glutamate- (GLU) and GABA-related components (GABAA and GABAB). Comparisons were made vs. vehicle injection (horizontal dashed line). (B) CGP effects on animals' BSR determined as (number of reinforcements obtained)/(maximum number of available reinforcements) x 100. Illustrated data range from two days before to two days after (white circles) an intrahippocampal single injection (black circle) of CGP. (C) Quantitative effects of CGP injection on fEPSP amplitude. Two sessions prior to (−2, −1) and two sessions after (1, 2) the injection day (black dot) are illustrated. The statistical comparisons are represented vs. BL values (dashed line in 100%). (D) As in C, same quantitative representation of effects induced by CGP injection but for fIPSP (GABAB) amplitude. The statistical comparisons are indicated vs. BL values (dashed line in 100%) (*) P<0.05; (**) P<0.01; (***) P<0.001. Code bars at the top in each section are defined in Figure 1.
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pone-0113787-g003: Effects of intrahippocampal injection of CGP 35348 on BSR performance and the associated fPSP changes.(A) The upper panel shows representative fPSPs (averaged 15 times) evoked at the CA3-CA1 synapse before injection (black solid line), in the presence of vehicle (gray dotted line) or following CGP injection (gray solid line). The bottom histograms illustrate the averaged fPSP amplitudes corresponding to glutamate- (GLU) and GABA-related components (GABAA and GABAB). Comparisons were made vs. vehicle injection (horizontal dashed line). (B) CGP effects on animals' BSR determined as (number of reinforcements obtained)/(maximum number of available reinforcements) x 100. Illustrated data range from two days before to two days after (white circles) an intrahippocampal single injection (black circle) of CGP. (C) Quantitative effects of CGP injection on fEPSP amplitude. Two sessions prior to (−2, −1) and two sessions after (1, 2) the injection day (black dot) are illustrated. The statistical comparisons are represented vs. BL values (dashed line in 100%). (D) As in C, same quantitative representation of effects induced by CGP injection but for fIPSP (GABAB) amplitude. The statistical comparisons are indicated vs. BL values (dashed line in 100%) (*) P<0.05; (**) P<0.01; (***) P<0.001. Code bars at the top in each section are defined in Figure 1.

Mentions: Recording sessions started one week after surgery. Field PSP recordings were carried out with Grass P511 differential amplifiers through a high-impedance probe (2×1012 Ω, 10 pF). The electrical stimulus presented to Schaffer collaterals consisted of a 100 µs, square, biphasic, single pulse (Figures 1–3). The evoking stimulus intensity for fPSPs (from 0.02 mA to 0.5 mA) was set usually at 35% of the intensity necessary to generate a maximum fEPSP response [6], [29].


Involvement of the GABAergic septo-hippocampal pathway in brain stimulation reward.

Vega-Flores G, Gruart A, Delgado-García JM - PLoS ONE (2014)

Effects of intrahippocampal injection of CGP 35348 on BSR performance and the associated fPSP changes.(A) The upper panel shows representative fPSPs (averaged 15 times) evoked at the CA3-CA1 synapse before injection (black solid line), in the presence of vehicle (gray dotted line) or following CGP injection (gray solid line). The bottom histograms illustrate the averaged fPSP amplitudes corresponding to glutamate- (GLU) and GABA-related components (GABAA and GABAB). Comparisons were made vs. vehicle injection (horizontal dashed line). (B) CGP effects on animals' BSR determined as (number of reinforcements obtained)/(maximum number of available reinforcements) x 100. Illustrated data range from two days before to two days after (white circles) an intrahippocampal single injection (black circle) of CGP. (C) Quantitative effects of CGP injection on fEPSP amplitude. Two sessions prior to (−2, −1) and two sessions after (1, 2) the injection day (black dot) are illustrated. The statistical comparisons are represented vs. BL values (dashed line in 100%). (D) As in C, same quantitative representation of effects induced by CGP injection but for fIPSP (GABAB) amplitude. The statistical comparisons are indicated vs. BL values (dashed line in 100%) (*) P<0.05; (**) P<0.01; (***) P<0.001. Code bars at the top in each section are defined in Figure 1.
© Copyright Policy
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC4263242&req=5

pone-0113787-g003: Effects of intrahippocampal injection of CGP 35348 on BSR performance and the associated fPSP changes.(A) The upper panel shows representative fPSPs (averaged 15 times) evoked at the CA3-CA1 synapse before injection (black solid line), in the presence of vehicle (gray dotted line) or following CGP injection (gray solid line). The bottom histograms illustrate the averaged fPSP amplitudes corresponding to glutamate- (GLU) and GABA-related components (GABAA and GABAB). Comparisons were made vs. vehicle injection (horizontal dashed line). (B) CGP effects on animals' BSR determined as (number of reinforcements obtained)/(maximum number of available reinforcements) x 100. Illustrated data range from two days before to two days after (white circles) an intrahippocampal single injection (black circle) of CGP. (C) Quantitative effects of CGP injection on fEPSP amplitude. Two sessions prior to (−2, −1) and two sessions after (1, 2) the injection day (black dot) are illustrated. The statistical comparisons are represented vs. BL values (dashed line in 100%). (D) As in C, same quantitative representation of effects induced by CGP injection but for fIPSP (GABAB) amplitude. The statistical comparisons are indicated vs. BL values (dashed line in 100%) (*) P<0.05; (**) P<0.01; (***) P<0.001. Code bars at the top in each section are defined in Figure 1.
Mentions: Recording sessions started one week after surgery. Field PSP recordings were carried out with Grass P511 differential amplifiers through a high-impedance probe (2×1012 Ω, 10 pF). The electrical stimulus presented to Schaffer collaterals consisted of a 100 µs, square, biphasic, single pulse (Figures 1–3). The evoking stimulus intensity for fPSPs (from 0.02 mA to 0.5 mA) was set usually at 35% of the intensity necessary to generate a maximum fEPSP response [6], [29].

Bottom Line: The successive BSR sessions evoked a progressive increase of the performance in inverse relationship with a decrease in the amplitude of fEPSPs, but not of fIPSPs.We corroborate a clear preference for BSR at 100 Hz (in comparison with BSR at 20 Hz or 8 Hz), in parallel with an increase in the spectral power of the low theta band, and a decrease in the gamma.These results were replicated by intrahippocampal injections of a GABAB antagonist.

View Article: PubMed Central - PubMed

Affiliation: Division of Neurosciences, Pablo de Olavide University, Seville, Spain.

ABSTRACT
The hippocampus is a structure related to several cognitive processes, but not very much is known about its putative involvement in positive reinforcement. In its turn, the septum has been related to instrumental brain stimulation reward (BSR) by its electrical stimulation with trains of pulses. Although the anatomical relationships of the septo-hippocampal pathway are well established, the functional relationship between these structures during rewarding behaviors remains poorly understood. To explore hippocampal mechanisms involved in BSR, CA3-evoked field excitatory and inhibitory postsynaptic potentials (fEPSPs, fIPSPs) were recorded in the CA1 area during BSR in alert behaving mice. The synaptic efficiency was determined from changes in fEPSP and fIPSP amplitudes across the learning of a BSR task. The successive BSR sessions evoked a progressive increase of the performance in inverse relationship with a decrease in the amplitude of fEPSPs, but not of fIPSPs. Additionally, we evaluated CA1 local field potentials (LFPs) during a preference task, comparing 8-, 20-, and 100-Hz trains of septal BSR. We corroborate a clear preference for BSR at 100 Hz (in comparison with BSR at 20 Hz or 8 Hz), in parallel with an increase in the spectral power of the low theta band, and a decrease in the gamma. These results were replicated by intrahippocampal injections of a GABAB antagonist. Thus, the GABAergic septo-hippocampal pathway seems to carry information involved in the encoding of reward properties, where GABAB receptors seem to play a key role. With regard to the dorsal hippocampus, fEPSPs evoked at the CA3-CA1 synapse seem to reflect the BSR learning process, while hippocampal rhythmic activities are more related to reward properties.

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