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.

Odor- and state-dependent olfactory tubercle local field potential dynamics in awake rats

“…Data taken for analyses from this rat include two epochs of 200 s each ("sleep"). During these times, OT LFP amplitude and the rate of sharp waves increased (Narikiyo et al 2014), while accelerometer movement ceased. Sleep states were further confirmed by video.…”

“…The epochs were taken from the freely exploring activity in the awake state (n ϭ 11 for OT, n ϭ 7 for OB), the sleep-like state (n ϭ 6 for OT, n ϭ 6 for OB), and before odor presentation when the animal was anesthetized (n ϭ 11 for OT, n ϭ 7 for OB). Sleep-like states were defined by minimal accelerometer movement, which was confirmed by video analysis, in addition to prominent changes in LFP amplitude, including the occurrence of sharp waves which are present in slow-wave sleep in the OT (Narikiyo et al 2014) (see Fig. 2).…”

“…2). To quantify sharp waves, full-band LFP was filtered to 2-20 Hz and events greater than 4 SDs below the mean were trough detected (Narikiyo et al 2014). The average of the power spectra for each rat in each state was normalized to the minimum/maximum and finally averaged across all rats to obtain a single mean power spectrum for spontaneous awake, sleep, and anesthetized states in both the OB and OT.…”

“…Odor information processing in the OT is also likely modulated by the internal state of the animal (Narikiyo et al 2014;. This may occur by means of noradrenergic locus coeruleus input (Inokuchi et al 1988;Solano-Flores et al 1980) and/or serotonergic input from the raphe nucleus (Hadley and Halliwell 2010).…”

“…This may occur by means of noradrenergic locus coeruleus input (Inokuchi et al 1988;Solano-Flores et al 1980) and/or serotonergic input from the raphe nucleus (Hadley and Halliwell 2010). Moreover, sleeplike states modulate activity in the olfactory cortex (Barnes et al 2011;Murakami et al 2005;Wilson and Yan 2010), and sleep states shape spontaneous OT activity (Narikiyo et al 2014). In addition, anesthesia impacts OB and piriform cortex network activity and functional connectivity (Fontanini and Bower 2005;Fontanini et al 2003;Murakami et al 2005;Wilson and Yan 2010), suggesting that odor information processing within the OT is likely dependent upon the internal state of the animal (i.e., sleep, anesthesia, arousal), although this has yet to be investigated.…”