Hippocampally-driven oscillatory activity at theta frequency is found in the diencephalon, but an understanding of the fundamental role of theta in the hippocampo-diencephalic circuit remains elusive. An important strategy in determining how activity modifies oscillatory properties of hippocampo-diencephalic circuitry comprises investigations of anterior thalamic responses to their main inputs: the descending dorsal fornix and the ascending mammillothalamic tract. Here, we show that the amplitude of thalamic theta spectral power selectively increases after plasticityinducing stimulation of the dorsal fornix, but not of the mammillothalamic tract in urethaneanaesthetized young male rats. Furthermore, we show that low-frequency stimulation (LFS) significantly augments the fornix-driven theta ratio (theta over delta power, T-ratio), in parallel with depressing thalamic synaptic responses. However, the mammillothalamic synaptic response after LFS did not correlate with the slow band of theta oscillation (low T-ratio), but did correlate positively with the fast band of theta oscillation (high T-ratio). Our data demonstrate that the descending direct fornix projection is a pathway that modulates theta rhythm in the hippocampodiencephalic circuit, resulting in dynamic augmentation of thalamic neuronal responsiveness. These findings suggest that hippocampal theta differentially affects synaptic integration in the different structures with which the hippocampus is reciprocally connected.
Keywordsanterior thalamic nuclei; fornix; mammillothalamic tract; synaptic plasticity; theta oscillation; LTP The functioning of the thalamus and the hippocampus cannot be fully elucidated without considering them as a unified network (Steriade, 2001;Warburton et al., 2001). In this context, hippocampal oscillations would be expected to have an impact on the neuronal activity of the anterior thalamic nuclei (ATN) but how the signals are actually processed through the hippocampo-diencephalic loop remains poorly understood. Large neuronal populations in ATN oscillate with frequency of 6-11 Hz, in the range of theta rhythm (Vertes et al., 2001;Tsanov et al., 2011a). Theta oscillations are a characteristic feature also of the main regions providing anterior thalamic inputs: the hippocampal formation and the medial mammillary bodies, that is the "medial" hippocampo-diencephalic system Theta rhythm has been especially related to the processes of episodic memory formation in the extended hippocampal system (Buzsáki, 2005). The hippocampus receives two main types of input: the first one is the theta input from the medial septum, which reverberates through hippocampo-diencephalic loop (Fig. 1A). The second hippocampal input is a highly-processed sensory information originating from multiple neocortical regions. The temporal convergence of activity from neocortical and diencephalic inputs would result in long-term storage of the encoded information. Because theta activity induces a fluctuation in cellular excitability, the probability tha...