Theta synchronization between the hippocampus and the nucleus incertus in urethane-anesthetized rats

Abstract

Oscillatory coupling between distributed areas can constitute a mechanism for neuronal integration. Theta oscillations provide temporal windows for hippocampal processing and only appear during certain active states of animals. Since previous studies have demonstrated that nucleus incertus (NI) contributes to the generation of hippocampal theta activity, in this paper, we evaluated the oscillatory coupling between both structures. We compared hippocampal and NI field potentials that were simultaneously recorded in urethane-anesthetized rats. Electrical and cholinergic stimulations of the reticularis pontis oralis nucleus have been used as hippocampal theta generation models. The spectral analyses reveal that electrical stimulation induced an increase in theta oscillations in both channels, whose frequencies depended on the intensity of stimulation. The intensity range used simultaneously increased the normalized spectral energy in the fast theta band (6-12 Hz) in HPC and NI. Frequencies within the theta range were found to be very similar in both channels. In order to validate coupling, spectral coherence was inspected. The data reveal that coherence in the high theta band also increased while stimuli were applied. Cholinergic activation progressively increased the main frequency in both structures to reach an asymptotic period with stable peak frequency in the low theta range (3-6 Hz), which could be first observed in NI and lasted about 1,500 s. Coherence in this band reached values close to 1. Taken together, these results support an electrophysiological and functional coupling between the hippocampus and the reticular formation, suggesting NI to be part of a distributed network working at theta frequencies.

Updating temporal expectancy of an aversive event engages striatal plasticity under amygdala control

“…When normalized to pre-CS baselines, which were similar for 30 and 10 s conditions (Supplementary Fig. 1), the relative power spectral density (PSD) revealed changes in oscillations during the CS in the theta frequency band with two delimited sub-bands corresponding to low- (3–6 Hz) and high- (6–9 Hz) theta rhythm252627 (Fig. 2b heat plots in the upper panel), the lower band showing the strongest increase in power centred ∼30 s (the expected time of US arrival).…”

Heterogeneous responses of nucleus incertus neurons to corticotrophin‐releasing factor and coherent activity with hippocampal theta rhythm in the rat

“…The reticular pontine oralis, which lacks direct projections to the septum or hippocampus, innervates the NI that in turn innervates the primary theta pacemaker region of the medial septum (Teruel‐Marti et al 2008). A recent study identified strong coherence between NI and hippocampal local field potentials, where theta activity of the NI preceded that of the hippocampus (Cervera‐Ferri et al 2011). Furthermore, we have demonstrated that NI‐ and RLN3‐containing afferent fibres form dense plexuses in the medial septum and RLN3 is localized in symmetric terminals that synapse on hippocampal‐projecting neurons immunopositive for choline acetyltransferase, neuronal nitric oxide synthase, calbindin, calretinin and parvalbumin (Olucha‐Bordonau et al 2012).…”

“…Coherence analysis of the nucleus incertus neuron firing with hippocampal EEG The integrity of the NI has been demonstrated to be important in the brainstem generation of hippocampal theta rhythm (Nunez et al 2006); and as local field potentials of the NI and hippocampus show strong coherence at theta frequency (Cervera‐Ferri et al 2011), we assessed the coherence of firing of NI neurons during hippocampal theta epochs. From 28 urethane‐anaesthetized rats, we recorded the spontaneous firing of NI neurons in two different states: one associated with large amplitude irregular activity in the hippocampus and the other characterized by the presence of sustained, rhythmic theta oscillations ∼4 Hz.…”

Distribution and targets of the relaxin‐3 innervation of the septal area in the rat

“…In fact, the nucleus incertus is presumed to be the major relay station of RPO inputs to the medial septum (and hippocampus), as there are no direct projections from the RPO to hippocampus (Teruel-Marti et al, 2008). Additionally, RPO stimulation results in theta synchronization in the hippocampus and nucleus incertus, at the same frequency and with a high degree of coherence (Cervera-Ferri et al, 2011). Furthermore, because the nucleus incertus is a RLN3 locus in the brain, we hypothesized that RLN3 might contribute to these effects.…”