Abstract
Hippocampal theta activity is related to spatial information processing, and high-frequency theta activity, in particular, has been linked to efficient spatial memory performance. Theta activity is regulated by the synchronizing ascending system (SAS), which includes mesencephalic and diencephalic relays. The supramamillary nucleus (SUMn) is located between the reticularis pontis oralis and the medial septum (MS), in close relation with the posterior hypothalamic nucleus (PHn), all of which are part of this ascending system. It has been proposed that the SUMn plays a role in the modulation of hippocampal theta-frequency; this could occur through direct connections between the SUMn and the hippocampus or through the influence of the SUMn on the MS. Serotonergic raphe neurons prominently innervate the hippocampus and several components of the SAS, including the SUMn. Serotonin desynchronizes hippocampal theta activity, and it has been proposed that serotonin may regulate learning through the modulation of hippocampal synchrony. In agreement with this hypothesis, serotonin depletion in the SUMn/PHn results in deficient spatial learning and alterations in CA1 theta activity-related learning in a Morris water maze. Because it has been reported that SUMn inactivation with lidocaine impairs the consolidation of reference memory, we asked whether changes in hippocampal theta activity related to learning would occur through serotonin depletion in the SUMn, together with deficiencies in memory. We infused 5,7-DHT bilaterally into the SUMn in rats and evaluated place learning in the standard Morris water maze task. Hippocampal (CA1 and dentate gyrus), septal and SUMn EEG were recorded during training of the test. The EEG power in each region and the coherence between the different regions were evaluated. Serotonin depletion in the SUMn induced deficient spatial learning and altered the expression of hippocampal high-frequency theta activity. These results provide evidence in support of a role for serotonin as a modulator of hippocampal learning, acting through changes in the synchronicity evoked in several relays of the SAS.
Highlights
Hippocampal theta activity has been related to processing of spatial information in different behavioral paradigms in various animal species (Ammassari-Teule et al, 1991; McNaughton et al, 2006) as well as in human beings (Klimesch et al, 1994; Klimesch, 1999; Caplan et al, 2001; Ekstrom et al, 2005; Lega et al, 2014)
It was reported that lidocaine infusion into the supramamillary nucleus (SUMn) did not affect the acquisition of an avoidance task retention was impaired when lidocaine was infused before training
The present results showed severe impairment in spatial reference memory after SUMn serotonin depletion such that no significant reduction in the distances traveled was achieved by this group, and the animals eventually attained a significant reduction in their escape pathways, this group searched throughout the four quadrants in the probe trial
Summary
Hippocampal theta activity has been related to processing of spatial information in different behavioral paradigms in various animal species (Ammassari-Teule et al, 1991; McNaughton et al, 2006) as well as in human beings (Klimesch et al, 1994; Klimesch, 1999; Caplan et al, 2001; Ekstrom et al, 2005; Lega et al, 2014). Because of to the tonic firing of RPOn neurons, the rhythmical firing of SUMn cells, and the result from inactivating SUMn, it was proposed that SUMn convert the tonic input received from the RPOn into a rhythmical pattern, which is relayed to the medial septum (MS), considered the pacemarker of the theta activity (Gogolak et al, 1968; Petsche et al, 1968; Andersen et al, 1979; Kirk and McNaughton, 1991; Kirk and Mackay, 2003) In support of this hypothesis, procaine infusions into (medial) SUMn induce a decrease in the frequency of hippocampal theta activity elicited by stimulation of RPOn in awake or in anesthetized rats (Kirk and McNaughton, 1993; McNaughton et al, 1995). An efferent influence from MS, which induce the deceleration of theta frequency-related firing in SUMn neurons, was observed (Kocsis, 2006; Kocsis and Kaminski, 2006); this influence could originate in the reciprocal connections between the two nuclei (Vertes, 1992), possibly through a GABAergic, input from the lateral septum (LS) on the (lateral) SUMn (Leranth and Kiss, 1996)
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