Oscillatory entrainment of thalamic neurons by theta rhythm in freely moving rats

The anterior thalamic nuclei are assumed to support episodic memory with anterior thalamic dysfunction a core feature of diencephalic amnesia. To date, the electrophysiological characterization of this region in behaving rodents has been restricted to the anterodorsal nucleus. Here we compared single-unit spikes with population activity in the anteroventral nucleus (AV) of freely moving rats during foraging and during naturally occurring sleep. We identified AV units that synchronize their bursting activity in the 6-11 Hz range. We show for the first time in freely moving rats that a subgroup of AV neurons is strongly entrained by theta oscillations. This feature together with their firing properties and spike shape suggests they be classified as "theta" units. To prove the selectivity of AV theta cells for theta rhythm, we compared the relation of spiking rhythmicity to local field potentials during theta and non-theta periods. The most distinguishable non-theta oscillations in rodent anterior thalamus are sleep spindles. We therefore compared the firing properties of AV units during theta and spindle periods. We found that theta and spindle oscillations differ in their spatial distribution within AV, suggesting separate cellular sources for these oscillations. While theta-bursting neurons were related to the distribution of local field theta power, spindle amplitude was independent of the theta units' position. Slow- and fast-spiking bursting units that are selectively entrained to theta rhythm comprise 23.7% of AV neurons. Our results provide a framework for electrophysiological classification of AV neurons as part of theta limbic circuitry.