Top‐down inputs from the olfactory cortex in the postprandial period promote elimination of granule cells in the olfactory bulb

Abstract

Elimination of granule cells (GCs) in the olfactory bulb (OB) is not a continual event but is promoted during a short time window in the postprandial period, typically with postprandial sleep. However, the neuronal mechanisms for the enhanced GC elimination during the postprandial period are not understood. Here, we addressed the question of whether top-down inputs of centrifugal axons from the olfactory cortex (OC) during the postprandial period are involved in the enhanced GC elimination in the OB. Electrical stimulation of centrifugal axons from the OC of anesthetized mice increased GC apoptosis. Furthermore, pharmacological suppression of top-down inputs from the OC to the OB during the postprandial period of freely behaving mice by γ-aminobutyric acid (GABA)A receptor agonist injection in the OC significantly decreased GC apoptosis. Remarkable apoptotic GC elimination in the sensory-deprived OB was also suppressed by pharmacological blockade of top-down inputs. These results indicate that top-down inputs from the OC to the OB during the postprandial period are the crucial signal promoting GC elimination, and suggest that the life and death decision of GCs in the OB is determined by the interplay between bottom-up sensory inputs from the external world and top-down inputs from the OC.

Sharp wave‐associated activity patterns of cortical neurons in the mouse piriform cortex

“…Previous experiments have demonstrated that OC‐SPWs generated in the PC can be observed in other olfactory‐related brain areas, such as the olfactory tubercle (Narikiyo et al., ) and OB (Manabe et al., ). It has been reported that pharmacological and electrical manipulation of top‐down inputs from the PC to the OB during postprandial sleep affected plastic changes in intrabulbar circuits, by regulating the elimination of newly generated granule cells in the OB as a function of a prior waking experience (Komano‐Inoue et al., ; Yokoyama et al., ). As granule cells play an important role in odor discrimination by modulating secondary olfactory neurons (Shepherd, Chen, Willhite, Migliore, & Greer, ; Yokoi, Mori, & Nakanishi, ), re‐organization of granule cells through top‐down inputs from the PC during the postprandial sleep period may be important for olfactory information processing.…”

Functional Sub-Circuits of the Olfactory System Viewed from the Olfactory Bulb and the Olfactory Tubercle

“…Intriguingly, selection of new GCs occurs during specific behaviors, and is promoted by the centrifugal inputs from the OC during the behaviors (Figure 1). For example, elimination of new GCs is enhanced during the sleep period after eating, and is dependent on the centrifugal inputs from the OC during post-meal sleep (Yokoyama et al, 2011; Yamaguchi et al, 2013; Komano-Inoue et al, 2014). GC elimination is also enhanced by the delivery of an electrical foot shock, depending on the centrifugal inputs from the OC during startle and fearful responses (Komano-Inoue et al, 2015).…”

Sharp wave-associated activity patterns of olfactory cortical neurons in the mouse piriform cortex

“…reported that pharmacological and electrical manipulation of top-down inputs from the PC to the OB during postprandial sleep affected plastic changes in intrabulbar circuits, by regulating the elimination of newly generated granule cells in the OB as a function of a prior waking experience(Yokoyama et al, 2011;Komano-Inoue et al, 2014). As granule cells play an important role in odor discrimination by modulating secondary olfactory neurons(Yokoi et al, 1995;Shepherd et al, 2007) , re-organization of granule cells through top-down inputs from the PC during the postprandial sleep period may be important for olfactory information processing.…”