Main olfactory bulb reconfiguration by prolonged passive olfactory experience correlates with increased brain‐derived neurotrophic factor and improved innate olfaction

Abstract

The main olfactory bulb (MOB) is highly plastic and constantly reconfiguring its function and structure depending on sensory experience. Despite the extensive evidence of anatomical, functional and behavioural changes in the olfactory system induced by highly variable olfactory experiences, it is still unknown whether prolonged passive odour experience could reconfigure the MOB at its input and network activity levels and whether these changes impact innate olfaction. Here, by measuring odour-induced glomerular activation, MOB network activity and innate olfactory behaviours, we described a profound MOB reconfiguration induced by prolonged passive olfactory experience in adult animals that impacts MOB input integration at the glomerular layer including an increase in the activated glomerular area and signal intensity, which is combined with a refinement in the number of activated glomeruli and less-overlapped glomerular maps. We also found that prolonged passive olfactory experience dramatically changes MOB population activity in the presence and absence of odours, which is reflected as a decrease in slow oscillations (<12 Hz) and an increase in fast oscillations (>12 Hz). All these functional changes in awake and anaesthetized mice correlate with an increase in brain-derived neurotrophic factor (BDNF) and with improved innate olfactory responses such as habituation/dishabituation and innate preference/avoidance. Our study shows that prolonged passive olfactory experience in adult animals produces a dramatic reconfiguration of the MOB network, possibly driven by BDNF, that improves innate olfactory responses.

The Role of the Stimulus in Olfactory Plasticity

“…Similar results were subsequently confirmed in mice [131,137,165]. In another noteworthy recent study, one of the rare cases of true olfactory environmental enrichment, adult mice were exposed to 21 different natural or synthetic odorant blends in two one-hour sessions per day using a different odorant each day for 21 days [135]. Enriched mice were compared to non-enriched controls using habituation/dishabituation tests and a predator odor avoidance test.…”

“…Most of these results were qualitatively similar in the awake mice, if quantitatively less robust, such that some statistical differences were not significant. In addition, local field potential recordings showed that enrichment led to an increase in slow wave network activity (<12 Hz) and a decrease in fast oscillations (>12 Hz) compared to unenriched controls, though the significance of this result is unclear [135].…”

“…In this study, adult mice were exposed for two hours per day for 21 days to a different complex natural odorant (e.g., cinnamon leaf oil, citral oil, etc.) each day [135][136][137]. Among other measurements, these authors examined the effects of enrichment on the IOS imaging of the bulb in anesthetized and awake mice.…”

Morphological differentiation of peritumoral brain zone microglia

“…Body temperature was preserved at 37˚C using a warm water circulation system. The animal's respiration was continuously monitored with a piezoelectric sensor (40-60 breaths/minute; [45][46][47][48]). Anesthesia was stopped at the end of the session and animals were observed until complete recovery before being transported back to their place of accommodation to later be processed for histochemical studies [2,[46][47][48][49].…”