Olfactory imprinting enhances associative learning and memory in C. elegans.

Learning and memory are fundamental processes for an organism's normal physiological function. Learning can occur at any stage of the organism's physiological development. Imprinted memories formed during the early developmental stage, unlike learning and memory, can last a lifetime. It is not clear whether these two types of memories are interlinked. In this study, we investigated whether imprinted memory influences adult learning and memory in a C. elegans model system. We trained the worms for short-term (STAM) and long-term associated memory (LTAM) towards butanone (BT) after conditioning them for imprinted memory towards isoamyl alcohol (IAA). We observed that these worms had improved learning abilities. However, functional imaging revealed that the worms had a long-term depression in the firing pattern in the AIY interneuron, indicating that there were significant changes in neuronal excitation pattern after imprinting, which could explain the enhanced behavioural alterations in animals after imprinting.

The Olfactory Organ Is a Unique Site for Neutrophils in the Brain.

In the vertebrate olfactory tract new neurons are continuously produced throughout life. It is widely believed that neurogenesis contributes to learning and memory and can be regulated by immune signaling molecules. Proteins originally identified in the immune system have subsequently been localized to the developing and adult nervous system. Previously, we have shown that olfactory imprinting, a specific type of long-term memory, is correlated with a transcriptional response in the olfactory organs that include up-regulation of genes associated with the immune system. To better understand the immune architecture of the olfactory organs we made use of cell-specific fluorescent reporter lines in dissected, intact adult brains of zebrafish to examine the association of the olfactory sensory neurons with neutrophils and blood-lymphatic vasculature. Surprisingly, the olfactory organs contained the only neutrophil populations observed in the brain; these neutrophils were localized in the neural epithelia and were associated with the extensive blood vasculature of the olfactory organs. Damage to the olfactory epithelia resulted in a rapid increase of neutrophils both within the olfactory organs as well as the central nervous system. Analysis of cell division during and after damage showed an increase in BrdU labeling in the neural epithelia and a subset of the neutrophils. Our results reveal a unique population of neutrophils in the olfactory organs that are associated with both the olfactory epithelia and the lymphatic vasculature suggesting a dual olfactory-immune function for this unique sensory system.

Gene expression of neuronal soluble N-ethylmaleimide-sensitive factor attachment protein receptor complex components in the olfactory organ and brain during seaward and homeward migration by pink salmon (Oncorhynchus gorbuscha).

The expression of synaptic vesicle exocytosis-regulator SNARE complex component genes (snap25, stx1 and vamp2) was examined in the olfactory nervous system during seaward and homeward migration by pink salmon (Oncorhynchus gorbuscha). The expression levels of snares in the olfactory organ were higher in seaward fry than in feeding and homeward adults, reflecting the development of the olfactory nervous system. The expression of snap25a, b and stx1a was upregulated or stable in the adult olfactory bulb and telencephalon. This upregulated expression suggested alterations in olfactory neuronal plasticity that may be related to the discrimination of natal rivers. The expression of stx1b was downregulated in the adult olfactory bulb, but remained stable in the adult telencephalon. The expression of vamp2 was initially strong in seaward fry, but was downregulated in adults in both the olfactory bulb and telencephalon. Pink salmon has the lowest diversity of maturation age, the largest population, and the most evolutional position in Pacific salmon (genus Oncorhynchus). The expression of snares in the olfactory center of pink salmon reflected the timing of sexual maturation and homeward migration. The present results and our previous studies indicate that snares show distinct expression patterns between two salmon species that depend on physiological and ecological features of migration.

Molecular characterization and gene expression of syntaxin-1 and VAMP2 in the olfactory organ and brain during both seaward and homeward migrations of chum salmon, Oncorhynchus keta.

Anadromous Pacific salmon (Genus Oncorhynchus) imprint odorants from their natal streams during their seaward migration, and adult salmon use olfaction to identify their natal streams during their homeward migration. However, little is known about the molecular mechanisms of olfactory imprinting in the salmon nervous system. Our previous study suggested that the snap25s gene (encoding a soluble N-ethylmaleimide-sensitive factor attachment protein receptor [SNARE] protein) is involved in pre-synaptic functions for olfactory imprinting and/or olfactory memory retrieval in chum salmon (O. keta). In this study, the expression of other SNARE proteins was analyzed in chum salmon brains. Three cDNAs, encoding salmon SNARE proteins (STX-1a, STX-1b, and VAMP2), were isolated and sequenced, which are well-conserved among vertebrates. Quantitative PCR detected the expression of stx1s and vamp2 in all regions of the brain, and especially highly in the olfactory bulb (OB) and telencephalon. The expression levels of snares in the olfactory rosette (OR) were higher during seaward migration than in adult life stages, subsequently vamp2 in the OB and telencephalon increased during seaward migration, corresponding well with development of the olfactory nervous system. Both stx1s in the OB and stx1b in the telencephalon were elevated in the seaward period, whereas stx1a in the telencephalon increased continuously until the feeding period. Both stx1s in the telencephalon increased in the last phase of upriver migration, possibly related to the retrieval of imprinted memory. Our results indicated the involvement and distinct roles of upregulated snares in synaptic plasticity for olfactory imprinting and/or olfactory memory retrieval in Pacific salmon.

Molecular characterization and gene expression of synaptosome-associated protein-25 (SNAP-25) in the brain during both seaward and homeward migrations of chum salmon Oncorhynchus keta.

It is generally accepted that information about some of the odorants in the natal streams of anadromous Pacific salmon (Genus Oncorhynchus) is imprinted during their seaward migration, and that anadromous Pacific salmon use olfaction to identify their natal streams during the homeward migration. However, little is known about the molecular mechanisms of the various pre-synaptic functions that are important for olfactory imprinting and memory retrieval in the salmon brain. Synaptosome-associated protein-25 (SNAP-25) mediates pre-synaptic vesicle exocytosis and regulates synaptic transmission and neuronal plasticity. Despite the importance of synaptic plasticity for memorization, the expression of SNAP-25 in the salmon brain is not well understood. In this study, snap25 expression was detected in chum salmon (O. keta) brains using molecular biological techniques. Two cDNAs encoding salmon SNAP-25 were isolated and sequenced (SNAP-25a and SNAP-25b). These cDNAs encoded proteins with 204 amino acid residues, which showed marked homology with each other (97%). The protein and nucleotide sequences demonstrated a high level of homology between salmon SNAP-25s and those of other teleost species. By quantitative PCR, the expression of snap25a and snap25b was detected in all regions of the salmon brain, especially in the telencephalon. The expression levels of snap25a in the olfactory blub were higher during seaward migration than in upriver and post-upriver migrations, reflecting synaptogenesis in the olfactory nervous system, and snap25b in the telencephalon was increased during upriver period. Our results indicated that snap25s gene is involved in synaptic plasticity for olfactory imprinting and/or olfactory memory retrieval in Pacific salmon.

Newborn interneurons in the accessory olfactory bulb promote mate recognition in female mice.

In the olfactory bulb of adult rodents, local interneurons are constantly replaced by immature precursors derived from the subventricular zone. Whether any olfactory sensory process specifically relies on this cell renewal remains largely unclear. By using the well known model of mating-induced imprinting to avoid pregnancy block, which requires accessory olfactory bulb (AOB) function, we demonstrate that this olfactory memory formation critically depends on the presence of newborn granule neurons in this brain region. We show that, in adult female mice, exposure to the male urine compounds involved in mate recognition increases the number of new granule cells surviving in the AOB. This process is modulated by male signals sensed through the vomeronasal organ and, in turn, changes the activity of the downstream amygdaloid and hypothalamic nuclei involved in the pregnancy block response. Chemical depletion of newly generated bulbar interneurons causes strong impairment in mate recognition, thus resulting in a high pregnancy failure rate to familiar mating male odors. Taken together, our results indicate that adult neurogenesis is essential for specific brain functions such as persistent odor learning and mate recognition.