Direct excitatory loop and theta resonance in the anterior cingulate-mediodorsal thalamic circuit.

Interactions between the prefrontal cortex and the thalamus are critical for cognitive processing, including working memory and attention. Specifically, theta oscillations in the anterior cingulate cortex (ACC) and mediodorsal thalamic nucleus (MDT) during cognitive tasks are associated with persistent neural activity during working memory; however, the cellular mechanisms underlying the theta oscillations remain unclear. Using targeted patch-clamp recordings combined with neuronal projection identification in rats, we demonstrate that there is a subcircuit of monosynaptically interconnected ACC and MDT neurons to form a positive feedback loop. Synaptic transmission from the ACC to the MDT exhibits short-term facilitation, particularly within the theta frequency range. Moreover, MDT-projecting ACC neurons display a membrane potential resonance at theta frequencies. The results show that the ACC-MDT pathway exhibits synaptic facilitation and membrane resonance preferentially at theta frequencies, indicating that the circuit is tuned to theta dynamics.