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.
Highlights
It is generally accepted that hippocampal mechanisms are involved in novelty detection, attention, spatial navigation, and associative learning [1]–[4]
As described previously [1], [39]–[41], fPSPs evoked in the CA1 area by electrical stimulation of Schaffer collaterals presented three components: one with a positive phase due to activation of glutamate receptors, and two subsequent negative components corresponding to the successive activation of GABAA, and GABAB receptors, respectively (Figure 1F)
The present results suggest that the information transmitted by the septo-hippocampal GABAergic pathway is essential for both the associative learning and the processing of the reward value, modulating hippocampal mechanisms that probably encode the behaviors involved in brain stimulation reward (BSR)
Summary
It is generally accepted that hippocampal mechanisms are involved in novelty detection, attention, spatial navigation, and associative learning [1]–[4]. Changes in fEPSPs recorded at the CA3-CA1 synapse have been associated with the acquisition and/or execution of different types of associative learning task [5]–[9] Another well-accepted mechanism is the involvement of hippocampal rhythmic activities in learning processes, changes in the different frequency bands (mainly theta and gamma), and their relationships with the observed behaviors, are still under debate [10]–[12]. To determine the preferred frequency of medial septum stimulation, animals were trained with a twochoice frequency reinforcement preference task We used this procedure to determine the effects of different frequencies, with different rewarding values, on the power spectra of LFPs. In subsequent experiments, animals received intrahippocampal injections of selected cholinergic- and GABAB-receptor agonists and antagonists to determine their involvement in the acquisition of self-stimulation behaviors
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