Slow oscillations at frequencies less than 1 Hz manifest in many brain regions as discrete transitions between a depolarized UP state and a hyperpolarized DOWN state of the membrane potential. These slow oscillations have been observed during slow wave sleep, under anesthesia or during quiet wakefulness. Even in awake and behaving animals, similar sub-threshold membrane potential dynamics were observed.
The slow oscillations in many brain regions interact strongly with sensory-evoked responses. However, whether and how they are modulated by sensory stimuli are not well understood. In the present study, intracellular recording in anesthetized guinea pigs showed that membrane potentials of non-lemniscal auditory thalamic neurons exhibited spontaneous UP/DOWN transitions at random intervals in the range of 2-30 s. The frequency of spontaneous UP/DOWN transitions could be entrained to a regular interval by repetitive sound stimuli with intervals ranging 3-12 sec, in which each sound stimulus effectively induced a UP-to-DOWN transition. Further experiments suggested that those sound-induced DOWN-states were likely caused by the activation of GABAA receptor-medicated inhibitory synaptic inputs from TRN. Strikingly, after termination of the entraining stimulation (ES), regular UP/DOWN transitions persisted for several cycles at the ES interval. Furthermore, the efficacy of weak sound stimuli in triggering the UP-to-DOWN transition was potentiated specifically at the ES interval for at least 10 min. Extracellular recordings in the auditory thalamus of un-anesthetized guinea pigs also showed apparent entrainment of slow oscillations by rhythmic sound stimuli during slow wave sleep. These results demonstrate a novel form of network plasticity, which could help to retain the information of stimulus interval on the order of seconds.