Adult-born neurons adjust olfactory bulb (OB) network functioning in response to changing environmental conditions by the formation, retraction and/or stabilization of new synaptic contacts. While some changes in the odour environment are rapid, the synaptogenesis of adult-born neurons occurs over a longer time scale. It remains unknown how the bulbar network functions when rapid and persistent changes in environmental conditions occur but when new synapses have not been formed. Here we reveal a new form of structural remodelling where mature spines of adult-born but not early-born neurons relocate in an activity-dependent manner. Principal cell activity induces directional growth of spine head filopodia (SHF) followed by spine relocation. Principal cell-derived glutamate and BDNF regulate SHF motility and directional spine relocation, respectively; and spines with SHF are selectively preserved following sensory deprivation. Our three-dimensional model suggests that spine relocation allows fast reorganization of OB network with functional consequences for odour information processing.

International audienceGranule cells (GCs) in the olfactory bulb (OB) play an important role in odor information processing. Although they have been classified into various neurochemical subtypes, the functional roles of these subtypes remain unknown. We used in vivo two-photon Ca2+ imaging combined with cell-type-specific identification of GCs in the mouse OB to examine whether functionally distinct GC subtypes exist in the bulbar network. We showed that half of GCs express Ca2+/calmodulin-dependent protein kinase IIα (CaMKIIα+) and that these neurons are preferentially activated by olfactory stimulation. The higher activity of CaMKIIα+ neurons is due to the weaker inhibitory input that they receive compared to their CaMKIIα-immunonegative (CaMKIIα−) counterparts. In line with these functional data, immunohistochemical analyses showed that 75%–90% of GCs expressing the immediate early gene cFos are CaMKIIα+ in naive animals and in mice that have been exposed to a novel odor and go/no-go operant conditioning, or that have been subjected to long-term associative memory and spontaneous habituation/dishabituation odor discrimination tasks. On the other hand, a perceptual learning task resulted in increased activation of CaMKIIα− cells

The adult mouse olfactory bulb is continuously supplied with new neurons that mostly differentiate into granule cells (GCs). Different subtypes of adult-born GCs have been identified, but their maturational profiles and their roles in bulbar network functioning and odor behavior remain elusive. It is also not known whether the same subpopulations of GCs born during early postnatal life (early-born) or during adulthood (adult-born) differ in their morpho-functional properties. Here, we show that adult-born calretinin-expressing (CR+) and non-expressing (CR−) GCs, as well as early-born CR+ GCs, display distinct inhibitory inputs but indistinguishable excitatory inputs and similar morphological characteristics. The frequencies of inhibitory post-synaptic currents were lower in early-born and adult-born CR+ GCs than in adult-born CR− neurons. These findings were corroborated by the reduced density of gephyrin+ puncta on CR+ GCs. CR+ GCs displayed a higher level of activation following olfactory tasks based on odor discrimination, as determined by an immediate early gene expression analysis. Pharmacogenetic inhibition of CR+ GCs diminished the ability of the mice to discriminate complex odor mixtures. Altogether, our results indicate that distinct inhibitory inputs are received by adult-born CR+ and CR− GCs, that early- and adult-born CR+ neurons have similar morpho-functional properties, and that CR+ GCs are involved in complex odor discrimination tasks.

The adult olfactory bulb (OB) continuously receives new interneurons that integrate into the functional neuronal network and that play an important role in odor information processing and olfactory behavior. Adult neuronal progenitors are derived from neural stem cells in the subventricular zone (SVZ) bordering the lateral ventricle. They migrate long distances along the rostral migratory stream (RMS) toward the OB where they differentiate into interneurons, mature, and establish synapses with tufted or mitral cells (MC), the principal neurons in the OB. The plasticity provided by both adult-born and pre-existing early-born neurons depends on the formation and pruning of new synaptic contacts that adapt the functioning of the bulbar network to changing environmental conditions. However, the formation of new synapses occurs over a long time scale (hours-days), whereas some changes in environmental conditions can occur more rapidly, requiring a much faster adjustment of neuronal networks. A new form of structural remodeling of adult-born, but not early-born, neurons was recently brought to light. This plasticity, which is based on the activity-dependent relocation of mature spines of GCs toward the dendrites of active principal cells, may allow a more rapid adjustment of the neuronal network in response to quick and persistent changes in sensory inputs. In this mini-review we discuss the different forms of structural plasticity displayed by adult-born and early-born neurons and the possibility that these different forms of structural remodeling may fulfill distinct roles in odor information processing.