Hippocampal inputs mediate theta-related plasticity in anterior thalamus

Abstract

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...

Segregation of parallel inputs to the anteromedial and anteroventral thalamic nuclei of the rat

“…Whereas many of the inputs to the ATN have a weak contralateral contribution, the LDTg input was distinctive; the contralateral input was unusually prominent but was still less than the ipsilateral input (see also Shibata, ). All of these properties suggest that this cholinergic input does not convey high‐resolution information, but rather has a nonselective role across ATN that presumably involves modulating its activity and plasticity (Tsanov et al, 2011). The importance of the cholinergic projections from LDTg for ATN function is underscored by the finding that infusions of scopolamine into the AV region are sufficient to impair radial‐arm maze performance (Mitchell et al, ); i.e., these LDTg inputs are vital for normal spatial memory.…”

The anterior thalamus is critical for overcoming interference in a context-dependent odor discrimination task.

“…As mentioned above, neurons in the AT and retrosplenial cortex exhibit context specific response patterns during instrumental discrimination learning and these firing patterns are degraded by fornix lesions (Smith et al ., 2004). Other studies have shown that AT neurons fire in synchrony with the hippocampal theta rhythm (Tsanov, Chah, Vann , et al ., 2011; Tsanov, Chah, Wright , et al ., 2011; Tsanov, Wright , et al ., 2011) and direct hippocampal projections to the AT exhibit long term potentiation while indirect projections (via the mammillary bodies) exhibit long term depression (Tsanov, Vann , et al ., 2011). These interactions are bi-directional.…”

Anterior thalamic nuclei lesions and recovery of function: Relevance to cognitive thalamus

“…Reinstatement of theta rhythmicity can recover memory function (McNaughton et al, 2006) and prefrontal coupling with hippocampal theta may produce stronger memory traces (Colgin, 2011;Fell and Axmacher, 2011;Hyman et al, 2010;Jones and Wilson, 2005). The MD and the anteroventral nucleus of the ATN (and anteromedial nucleus) are key nodes in two separate and potentially mutually supportive theta pathways that may coordinate information processing across the prefrontal cortex, retrosplenial cortex and hippocampal formation (Kirk and Mackay, 2003;Tsanov et al, 2011). Preliminary data (Ulrich et al, in preparation) suggest that improved anterior cingulate-CA1 communication, as measured by coherence, occurs in enriched rats, even superimposed on the effects of an ATN lesion (the ATN lesion reduced theta power while enrichment tended to increase power in lesioned rats and decrease it in sham rats).…”