Sharp wave-associated synchronized inputs from the piriform cortex activate olfactory tubercle neurons during slow-wave sleep

Abstract

During slow-wave sleep, anterior piriform cortex neurons show highly synchronized discharges that accompany olfactory cortex sharp waves (OC-SPWs). The OC-SPW-related synchronized activity of anterior piriform cortex neurons travel down to the olfactory bulb and is thought to be involved in the reorganization of bulbar neuronal circuitry. However, influences of the OC-SPW-related activity on other regions of the central olfactory system are still unknown. Olfactory tubercle is an area of OC and part of ventral striatum that plays a key role in reward-directed motivational behaviors. In this study, we show that in freely behaving rats, olfactory tubercle receives OC-SPW-associated synchronized inputs during slow-wave sleep. Local field potentials in the olfactory tubercle showed SPW-like activities that were in synchrony with OC-SPWs. Single-unit recordings showed that a subpopulation of olfactory tubercle neurons discharged in synchrony with OC-SPWs. Furthermore, correlation analysis of spike activity of anterior piriform cortex and olfactory tubercle neurons revealed that the discharges of anterior piriform cortex neurons tended to precede those of olfactory tubercle neurons. Current source density analysis in urethane-anesthetized rats indicated that the current sink of the OC-SPW-associated input was located in layer III of the olfactory tubercle. These results indicate that OC-SPW-associated synchronized discharges of piriform cortex neurons travel to the deep layer of the olfactory tubercle and drive discharges of olfactory tubercle neurons. The entrainment of olfactory tubercle neurons in the OC-SPWs suggests that OC-SPWs coordinate reorganization of neuronal circuitry across wide areas of the central olfactory system including olfactory tubercle during slow-wave sleep.