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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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Power spectra in the low theta band evoked by the different reinforcement frequencies and by the local injection of CGP 35348 during time window C, and their relationship with the number of lever presses.(A) Power spectra values collected from a representative animal. From top to bottom are illustrated lever presses (Lever), the reward train (Reward), and the power value corresponding to the low theta (3–5.8 Hz) band. Two frequencies of reward tested (100 Hz, 20 Hz) are shown in relation to lever-press activity. Each section (panels 4 s long) corresponds to 30 overlapped sweeps (the lever trace remains high for the time that the lever is held down) as well as their corresponding power values in the low theta band. Gray squares indicate time window C. Note the increase in power spectrum values related to the preferred frequency of reinforcement (100 Hz). This increase was not associated with lever activity. (B) Power values collected—always using 100 Hz of reward—from a representative mouse in two different sessions: vehicle and CGP injections. Traces are displayed as in A. Note that the increase in power values during vehicle administration sessions was clearly larger than during CGP sessions. Again, no relationship with lever activity was noticed. Code bars at the top in A and B are defined in Figure 1.
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pone-0113787-g005: Power spectra in the low theta band evoked by the different reinforcement frequencies and by the local injection of CGP 35348 during time window C, and their relationship with the number of lever presses.(A) Power spectra values collected from a representative animal. From top to bottom are illustrated lever presses (Lever), the reward train (Reward), and the power value corresponding to the low theta (3–5.8 Hz) band. Two frequencies of reward tested (100 Hz, 20 Hz) are shown in relation to lever-press activity. Each section (panels 4 s long) corresponds to 30 overlapped sweeps (the lever trace remains high for the time that the lever is held down) as well as their corresponding power values in the low theta band. Gray squares indicate time window C. Note the increase in power spectrum values related to the preferred frequency of reinforcement (100 Hz). This increase was not associated with lever activity. (B) Power values collected—always using 100 Hz of reward—from a representative mouse in two different sessions: vehicle and CGP injections. Traces are displayed as in A. Note that the increase in power values during vehicle administration sessions was clearly larger than during CGP sessions. Again, no relationship with lever activity was noticed. Code bars at the top in A and B are defined in Figure 1.

Mentions: A complementary analysis was carried out within window C in order to rule out the possible interaction in these results with a walking state of the recorded mice. Figure 5 shows the power spectra of the low theta band (3 Hz to 6 Hz) in two experimental situations: during the preference test (Figure 5A) and during vehicle and CGP sessions (Figure 5B) associated with the pattern of lever presses. The increased power in the theta band was not associated to locomotor behaviors, because it was present even during repeated lever presses and when the mouse kept the lever pressed for an extended period (even>2 s).


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

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

Power spectra in the low theta band evoked by the different reinforcement frequencies and by the local injection of CGP 35348 during time window C, and their relationship with the number of lever presses.(A) Power spectra values collected from a representative animal. From top to bottom are illustrated lever presses (Lever), the reward train (Reward), and the power value corresponding to the low theta (3–5.8 Hz) band. Two frequencies of reward tested (100 Hz, 20 Hz) are shown in relation to lever-press activity. Each section (panels 4 s long) corresponds to 30 overlapped sweeps (the lever trace remains high for the time that the lever is held down) as well as their corresponding power values in the low theta band. Gray squares indicate time window C. Note the increase in power spectrum values related to the preferred frequency of reinforcement (100 Hz). This increase was not associated with lever activity. (B) Power values collected—always using 100 Hz of reward—from a representative mouse in two different sessions: vehicle and CGP injections. Traces are displayed as in A. Note that the increase in power values during vehicle administration sessions was clearly larger than during CGP sessions. Again, no relationship with lever activity was noticed. Code bars at the top in A and B are defined in Figure 1.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0113787-g005: Power spectra in the low theta band evoked by the different reinforcement frequencies and by the local injection of CGP 35348 during time window C, and their relationship with the number of lever presses.(A) Power spectra values collected from a representative animal. From top to bottom are illustrated lever presses (Lever), the reward train (Reward), and the power value corresponding to the low theta (3–5.8 Hz) band. Two frequencies of reward tested (100 Hz, 20 Hz) are shown in relation to lever-press activity. Each section (panels 4 s long) corresponds to 30 overlapped sweeps (the lever trace remains high for the time that the lever is held down) as well as their corresponding power values in the low theta band. Gray squares indicate time window C. Note the increase in power spectrum values related to the preferred frequency of reinforcement (100 Hz). This increase was not associated with lever activity. (B) Power values collected—always using 100 Hz of reward—from a representative mouse in two different sessions: vehicle and CGP injections. Traces are displayed as in A. Note that the increase in power values during vehicle administration sessions was clearly larger than during CGP sessions. Again, no relationship with lever activity was noticed. Code bars at the top in A and B are defined in Figure 1.
Mentions: A complementary analysis was carried out within window C in order to rule out the possible interaction in these results with a walking state of the recorded mice. Figure 5 shows the power spectra of the low theta band (3 Hz to 6 Hz) in two experimental situations: during the preference test (Figure 5A) and during vehicle and CGP sessions (Figure 5B) associated with the pattern of lever presses. The increased power in the theta band was not associated to locomotor behaviors, because it was present even during repeated lever presses and when the mouse kept the lever pressed for an extended period (even>2 s).

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