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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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Spectral power analysis of EEGs recorded in the hippocampal CA1 area during shaping sessions and BSR performance.Data collected from a representative mouse during the previously defined time windows (A, B, and C) were analyzed each day along shaping and BSR protocols. From top to bottom, the three time windows are represented in three panels by semi-overlapped averaged spectral power profiles. The upper section of each panel represents high frequencies (60–120 Hz) and the bottom one the lower frequencies (1–40 Hz) during shaping (−2, −1 and 0) and brain stimulation (1–6) sessions. The session in which criterion was reached (day 0) is represented in solid blue. The color code corresponding to each illustrated session (from −2 to 6) is illustrated at the bottom. Code bars at the top are defined in Figure 1.
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pone-0113787-g007: Spectral power analysis of EEGs recorded in the hippocampal CA1 area during shaping sessions and BSR performance.Data collected from a representative mouse during the previously defined time windows (A, B, and C) were analyzed each day along shaping and BSR protocols. From top to bottom, the three time windows are represented in three panels by semi-overlapped averaged spectral power profiles. The upper section of each panel represents high frequencies (60–120 Hz) and the bottom one the lower frequencies (1–40 Hz) during shaping (−2, −1 and 0) and brain stimulation (1–6) sessions. The session in which criterion was reached (day 0) is represented in solid blue. The color code corresponding to each illustrated session (from −2 to 6) is illustrated at the bottom. Code bars at the top are defined in Figure 1.

Mentions: According to the present results, there is a negative trend in fEPSP amplitudes across BSR sessions, an occurrence not observed for fIPSP values (Figure 2C, D). These results could be a reflection of a similar mechanism previously described with regard to hippocampal rhythmic activities. This suggestion is in agreement with previous studies describing the relationship between fPSPs and theta rhythm—considering a complete band of 3–12 Hz. In 1990, Núñez and colleagues [71] reported that the participation of fEPSPs is important in the generation of the theta rhythm, whereas that of fIPSPs is not so necessary. Furthermore, in 2000, Wyble and colleagues, recording in CA1, reported a significant suppression of evoked fEPSP (single pulse in CA3 or dentate gyrus) when theta rhythm in the dentate gyrus was the dominant frequency (>75%). For this, they evaluated the power spectra density in epochs lasting three seconds prior to the stimulation [72]. Finally, in 2002 Seager and colleagues reported a facilitatory effect of theta rhythm during classical conditioning [68]. Although there are some differences in the experimental procedures, we can speculate that a similar relationship is reproduced in our results. We noticed a progressive decrease in fEPSP amplitudes across BSR sessions, a fact that could facilitate the observed increase in the power of the theta band. In addition, the decrease of fEPSP amplitudes was accompanied by an increasing trend of the main peak in the spectral power within the theta band (around 8–9 Hz) in time window C (Figure 7).


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

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

Spectral power analysis of EEGs recorded in the hippocampal CA1 area during shaping sessions and BSR performance.Data collected from a representative mouse during the previously defined time windows (A, B, and C) were analyzed each day along shaping and BSR protocols. From top to bottom, the three time windows are represented in three panels by semi-overlapped averaged spectral power profiles. The upper section of each panel represents high frequencies (60–120 Hz) and the bottom one the lower frequencies (1–40 Hz) during shaping (−2, −1 and 0) and brain stimulation (1–6) sessions. The session in which criterion was reached (day 0) is represented in solid blue. The color code corresponding to each illustrated session (from −2 to 6) is illustrated at the bottom. Code bars at the top are defined in Figure 1.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0113787-g007: Spectral power analysis of EEGs recorded in the hippocampal CA1 area during shaping sessions and BSR performance.Data collected from a representative mouse during the previously defined time windows (A, B, and C) were analyzed each day along shaping and BSR protocols. From top to bottom, the three time windows are represented in three panels by semi-overlapped averaged spectral power profiles. The upper section of each panel represents high frequencies (60–120 Hz) and the bottom one the lower frequencies (1–40 Hz) during shaping (−2, −1 and 0) and brain stimulation (1–6) sessions. The session in which criterion was reached (day 0) is represented in solid blue. The color code corresponding to each illustrated session (from −2 to 6) is illustrated at the bottom. Code bars at the top are defined in Figure 1.
Mentions: According to the present results, there is a negative trend in fEPSP amplitudes across BSR sessions, an occurrence not observed for fIPSP values (Figure 2C, D). These results could be a reflection of a similar mechanism previously described with regard to hippocampal rhythmic activities. This suggestion is in agreement with previous studies describing the relationship between fPSPs and theta rhythm—considering a complete band of 3–12 Hz. In 1990, Núñez and colleagues [71] reported that the participation of fEPSPs is important in the generation of the theta rhythm, whereas that of fIPSPs is not so necessary. Furthermore, in 2000, Wyble and colleagues, recording in CA1, reported a significant suppression of evoked fEPSP (single pulse in CA3 or dentate gyrus) when theta rhythm in the dentate gyrus was the dominant frequency (>75%). For this, they evaluated the power spectra density in epochs lasting three seconds prior to the stimulation [72]. Finally, in 2002 Seager and colleagues reported a facilitatory effect of theta rhythm during classical conditioning [68]. Although there are some differences in the experimental procedures, we can speculate that a similar relationship is reproduced in our results. We noticed a progressive decrease in fEPSP amplitudes across BSR sessions, a fact that could facilitate the observed increase in the power of the theta band. In addition, the decrease of fEPSP amplitudes was accompanied by an increasing trend of the main peak in the spectral power within the theta band (around 8–9 Hz) in time window C (Figure 7).

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.

Show MeSH