Memory In Invertebrates Research Articles

The plasticity of immune memory in invertebrates.

Whether specific immune protection after initial pathogen exposure (immune memory) occurs in invertebrates has long been uncertain. The absence of antibodies, B-cells and T-cells, and the short lifespans of invertebrates led to the hypothesis that immune memory does not occur in these organisms. However, research in the past two decades has supported the existence of immune memory in several invertebrate groups, including Ctenophora, Cnidaria, Nematoda, Mollusca and Arthropoda. Interestingly, some studies have demonstrated immune memory that is specific to the parasite strain. Nonetheless, other work does not provide support for immune memory in invertebrates or offers only partial support. Moreover, the expected biphasic immune response, a characteristic of adaptive immune memory in vertebrates, varies within and between invertebrate species. This variation may be attributed to the influence of biotic or abiotic factors, particularly parasites, on the outcome of immune memory. Despite its critical importance for survival, the role of phenotypic plasticity in immune memory has not been systematically examined in the past two decades. Additionally, the features of immune responses occurring in diverse environments have yet to be fully characterized.

Metabolism and immune memory in invertebrates: are they dissociated?

Since the discovery of specific immune memory in invertebrates, researchers have investigated its immune response to diverse microbial and environmental stimuli. Nevertheless, the extent of the immune system's interaction with metabolism, remains relatively enigmatic. In this mini review, we propose a comprehensive investigation into the intricate interplay between metabolism and specific immune memory. Our hypothesis is that cellular endocycles and epigenetic modifications play pivotal roles in shaping this relationship. Furthermore, we underscore the importance of the crosstalk between metabolism and specific immune memory for understanding the evolutionary costs. By evaluating these costs, we can gain deeper insights into the adaptive strategies employed by invertebrates in response to pathogenic challenges. Lastly, we outline future research directions aimed at unraveling the crosstalk between metabolism and specific immune memory. These avenues of inquiry promise to illuminate fundamental principles governing host-pathogen interactions and evolutionary trade-offs, thus advancing our understanding of invertebrate immunology.

Parental training with phloroglucinol protects their offspring from biotic and abiotic stressors in Macrobrachium rosenbergii

Being one of the fastest growing high protein animal foods producing sector, shrimp and prawn aquaculture has increased in demand worldwide. However, disease outbreak is considered one of the most limiting factors in this industry. Among shrimp bacterial diseases, vibriosis is one of the most important bacterial diseases. Additionally, acute hepatopancreatic necrosis disease (AHPND) in shrimp has been responsible for significant losses globally for the past ten years or so. Hence, for future sustainable shrimp farming, broodstock management and production of high-quality shrimp seed becomes a prerequisite for this industry, as it is considered to contribute to health management in general. Being invertebrates, shrimp and prawn solely depend on their innate immune system to combat the invading pathogens. However, in recent years, there is an increasing number of studies claiming innate immune memory in invertebrates. This implies that priming with pathogens or environmental stress or immune elicitors could induce increased resistance. In a previous study using a brine shrimp model, it was demonstrated that phloroglucinol, a plant-derived heat-shock protein inducing compound increased stress resistance in the parental generation, a phenotype that was passed on to the next generations. Intrigued by this, the present study was conducted to expand and validate these observations in commercial prawn Macrobrachium rosenbergii. First, following exposure of M. rosenbergii animals (juveniles) to phloroglucinol, improved survival, later on in life, was observed. Most interestingly, in the next generation, M. rosenbergii F1 animals originating from phloroglucinol-treated parents showed an increased resistance against AHPND causing Vibrio parahaemolyticus and abiotic stress (lethal heat shock and ammonia stress). To the best of our knowledge, this is the first validation study of parental conditioning in any commercial shrimp/prawn species. It is anticipated that this study will facilitate future research and application of parental conditioning as a unique and powerful management strategy against prophylaxis of infectious diseases in the shrimp farming industry.

Induction of transgenerational innate immune memory against Vibrio infections in a brine shrimp (Artemia franciscana) model

The occurrence of transgenerational innate immune memory in invertebrates possibly offers an opportunity for the creation of offspring with increased resistance against infectious diseases. Shrimps, being invertebrates rely on their innate immune system as the main defence mechanism to combat invading pathogens. Thus, creating transgenerational innate immune memory could be used for disease prevention in shrimp farming. However, the mechanisms behind the induction of transgenerational innate immune memory and the creation of a broad spectrum protective immune memory are still not fully understood. Here, the creation of transgenerational innate immune memory and the mechanisms involved were studied using the brine shrimp (Artemia franciscana) as a model for shrimps. Hereto, a parental generation was primed by exposure to a live or dead Vibrio parahaemolyticus PV1 while another parental generation was primed with live or dead Vibrio campbellii LMG21363. Both Vibrio strains are known to cause diseases in farmed shrimps, resulting in significant economic losses. Axenic larvae of three subsequent generations were exposed either to the homologous or heterologous (viable) Vibrio species and their survival was recorded. In general, progenies from primed F0 parents developed innate immune memory as compared to offspring of non-primed control F0 parents as they were significantly protected against a subsequent Vibrio infection. Protection in the infected offspring was more pronounced when they were infected with the homologous Vibrio strain. Disease resistance was associated with significantly increased transcription of especially peroxinectin (pxn), prophenoloxidase (proPO), lipopolysaccharide and β-1,3-glucan-binding protein (LGBP), high mobility group box 1 (HMGB1) and heat shock protein 90 (hsp90) genes and significant changes in histone H3 and H4 acetylation and m6A RNA methylation. Overall, results might lead to procedures at shrimp brood stock level for parental conditioning and creation of transgenerational innate immune memory in offspring.

Insulin and Memory in Invertebrates.

Insulin and insulin-like peptides (ILP) help to maintain glucose homeostasis, whereas insulin-like growth factor (IGF) promotes the growth and differentiation of cells in both vertebrates and invertebrates. It is sometimes difficult to distinguish between ILP and IGF in invertebrates, however, because in some cases ILP has the same function as IGF. In the present review, therefore, we refer to these peptides as ILP/IGF signaling (IIS) in invertebrates, and discuss the role of IIS in memory formation after classical conditioning in invertebrates. In the arthropod Drosophila melanogaster, IIS is involved in aversive olfactory memory, and in the nematode Caenorhabditis elegans, IIS controls appetitive/aversive response to NaCl depending on the duration of starvation. In the mollusk Lymnaea stagnalis, IIS has a critical role in conditioned taste aversion. Insulin in mammals is also known to play an important role in cognitive function, and many studies in humans have focused on insulin as a potential treatment for Alzheimer’s disease. Although analyses of tissue and cellular levels have progressed in mammals, the molecular mechanisms, such as transcriptional and translational levels, of IIS function in cognition have been far advanced in studies using invertebrates. We anticipate that the present review will help to pave the way for studying the effects of insulin, ILPs, and IGFs in cognitive function across phyla.

Benefits and costs of immune memory in Rhodnius prolixus against Trypanosoma cruzi

There is increasing evidence supporting the immune memory in invertebrates, but the studies are relatively neglected in insect vectors other than mosquitoes. Therefore, we tested two hypotheses: 1) Rhodnius prolixus insects possess immune memory against Trypanosoma cruzi, and 2) their immune memory is costly. The Dm28c and Y strains of T. cruzi were used, the former being more infective than the latter. On the one hand, the triatomines subjected to dual challenges with the Dm28c strain did not show significant differences in survival than those of the heterologous challenge groups control-Dm28c and Y-Dm28c. On the other hand, the insects survived longer after a dual Y–Y challenge than after the corresponding heterologous challenge (control-Y). The Y–Y, Dm28c-Y, and naïve groups showed similar survival. There was more prolonged survival following the Y–Y versus Dm28c-Dm28c dual challenge. The Dm28c-Dm28c group exhibited moulting sooner than the control-Dm28c or naïve group. In contrast, there were no differences in the probability of moulting between the Y–Y and naïve groups. The results suggest that triatomines have immune memory against the Y but not the Dm28c strain. Further investigation on triatomine and T. cruzi interaction is needed to determine if infectivity accelerates or delay growth due to innate immune memory.

The Elevated Expressions of Anti-lipopolysaccharide Factors After Priming Stimulation Confer Lastingly Humoral Protection in Crab Eriocheir sinensis.

Evidence of immune memory in invertebrates (immune priming) has accumulated in various organisms, and both cellular and humoral immune reactions are speculated to be involved in immune priming. However, there is a lack of understanding of the molecular mechanisms involved. In the present study, the protective effect of primed haemolymph was further validated by the increased survival rate of naïve crabs receiving a transfusion of primed haemolymph. By proteomic analysis, there were 474 proteins identified from the primed haemolymph, and most of them were functionally annotated in transport and metabolism classes. A total of 70 proteins were found to be differentially expressed in haemolymph at 12 hours and 7 days after priming stimulation with Aeromonas hydrophila, among which anti-lipopolysaccharide factor 1 (EsALF-1) and 3 (EsALF-3) were identified as the most significant (p < 0.05). After being challenged with A. hydrophila, EsALF-1 and EsALF-3 were highly expressed at both mRNA (in haemocytes) and protein (in haemolymph) levels compared with blank crabs, and the mRNA expressions of components in the EsTLR1-EsMyd88-EsPelle-EsALF pathway also increased significantly (p < 0.05). The EsALF-3 and EsMyd88 were even significantly higher expressed in response to the second A. hydrophila challenge, but their expressions all decreased (p < 0.05) when EsTLR1 was knocked down by RNAi. After the naïve crabs received an injection with the recombinant protein of EsALF-1 (rEsALF-1) or EsALF-3 (rEsALF-3), their survival rate increased significantly (p < 0.05) upon A. hydrophila stimulation. In contrast, the survival rate of the primed crabs reduced significantly (p < 0.05) after they received an injection with the antibody of EsALF-1 or EsALF-3. The enhanced expressions of EsALF-1 and EsALF-3 after A. hydrophilap riming stimulation could sustain for four weeks. All the results suggested that the EsTLR1-mediated productions of EsALF-1 and EsALF-3 in haemolymph played an indispensable role in the month-long humoral immune protection induced by A. hydrophila, which provides solid evidence of immune priming in crabs and a valuable reference for further understanding immune memory in invertebrates.

Long noncoding RNAs: Emerging players regulating innate immune memory in the red flour beetle

A variety of strategies have been evolved to eradicate invading microbes. Phagocytes have developed in vertebrates and invertebrates to confer a non-specific immune response to pathogens. Besides, vertebrates have evolved lymphocytes to develop memory cells that can quickly respond upon the next exposure to the same pathogen. Although lymphocytes are absent in invertebrates, historical evidence, dating back to the 1920s, indicated the presence of immune memory in invertebrates. However, the concept of long-lasting non-specific defense predominated until recent evidence has been introduced in the first decade of the 21st century. Although more evidence has been introduced later, the molecular mechanism underlying the innate immune memory is largely undefined in invertebrates. Long noncoding RNAs (lncRNAs) have demonstrated a role in regulating various biological processes, including immune response. In this review, we will explore the potential role of lncRNAs in developing innate immune memory in the red flour beetle (Tribolium castaneum).

Current understanding and perspectives on the potential mechanisms of immune priming in beetles

Beetles are the most diverse group of insects in Insecta which can be found in almost every habitat and environment on Earth. The possessing of the rapid and effective immune defenses is one of the important factors for their success. It is generally recognized that beetles only rely on the non-specific innate immune defense, without immunological memory, to fight against pathogens. However, there was cumulative evidence for the innate immune memory in invertebrates, including beetles, over the last decades, implying that insect innate immunity is more complex and has more features than previously thought. In beetles, it has been well documented that the specific or nonspecific enhanced immunocompetence can persist throughout development within generations and can even be transferred to the descendents in the next generation. Although insect immune priming might be shaped by epigenetic modifications and transferring effectors, mRNA and microbial signals, the solid experimental evidence to support the causal relationship between any of them and immune priming is still scarce. The combined usage of ‘omics’ approaches and CRISPR/Cas9 in the appropriate insect models with well-known genetic background, Tribolium castaneum and Tenebrio molitor, will help us to decipher the molecular mechanisms by which immune priming occurs in beetles in depth.

Innate immune memory in invertebrates: Concept and potential mechanisms

Invertebrates are the protagonists of a recent paradigm shift because they now show that vertebrates are not the only group with immune memory. This review discusses the concept of immune priming, its characteristics, and differences with trained immunity and immune enhancement. We include an update of the current status of immune priming within generations in different groups of invertebrates which now include work in 5 Phyla: Ctenophora, Cnidaria, Mollusca, Nematoda, and Arthropoda. Clearly, few Phyla have been studied. We also resume and discuss the effector mechanism related to immune memory, including integrating viral elements into the genome, endoreplication, and epigenetics. The roles of other elements are incorporated, such as hemocytes, immune pathways, and metabolisms. We conclude that taking care of the experimental procedure will discern if results provide or do not support the invertebrates' immune memory and that regarding mechanisms, indeed, there are no studies on the immune memory mechanisms, this is how specificity is reached, and how and where the immune memory is stored and how is recall upon subsequent encounters. Finally, we discuss the possibility of having more than one mechanism working in different groups of invertebrates depending on the environmental conditions.

Neuromodulatory pathways in learning and memory: Lessons from invertebrates

In an ever-changing environment, animals have to continuously adapt their behaviour. The ability to learn from experience is crucial for animals to increase their chances of survival. It is therefore not surprising that learning and memory evolved early in evolution and are mediated by conserved molecular mechanisms. A broad range of neuromodulators, in particular monoamines and neuropeptides, have been found to influence learning and memory, although our knowledge on their modulatory functions in learning circuits remains fragmentary. Many neuromodulatory systems are evolutionarily ancient and well-conserved between vertebrates and invertebrates. Here, we highlight general principles and mechanistic insights concerning the actions of monoamines and neuropeptides in learning circuits that have emerged from invertebrate studies. Diverse neuromodulators have been shown to influence learning and memory in invertebrates, which can have divergent or convergent actions at different spatiotemporal scales. In addition, neuromodulators can regulate learning dependent on internal and external states, such as food and social context. The strong conservation of neuromodulatory systems, the extensive toolkit and the compact learning circuits in invertebrate models make these powerful systems to further deepen our understanding of neuromodulatory pathways involved in learning and memory.

A trade-off switch of two immunological memories in Caenorhabditis elegans reinfected by bacterial pathogens

Recent studies have suggested that innate immune responses exhibit characteristics associated with memory linked to modulations in both vertebrates and invertebrates. However, the diverse evolutionary paths taken, particularly within the invertebrate taxa, should lead to similarly diverse innate immunity memory processes. Our understanding of innate immune memory in invertebrates primarily comes from studies of the fruit fly Drosophila melanogaster, the generality of which is unclear. Caenorhabditis elegans typically inhabits soil harboring a variety of fatal microbial pathogens; for this invertebrate, the innate immune system and aversive behavior are the major defensive strategies against microbial infection. However, their characteristics of immunological memory remains infantile. Here we discovered an immunological memory that promoted avoidance and suppressed innate immunity during reinfection with bacteria, which we revealed to be specific to the previously exposed pathogens. During this trade-off switch of avoidance and innate immunity, the chemosensory neurons AWB and ADF modulated production of serotonin and dopamine, which in turn decreased expression of the innate immunity-associated genes and led to enhanced avoidance via the downstream insulin-like pathway. Therefore, our current study profiles the immune memories during C. elegans reinfected by pathogenic bacteria and further reveals that the chemosensory neurons, the neurotransmitter(s), and their associated molecular signaling pathways are responsible for a trade-off switch between the two immunological memories.

MicroRNA-210 Regulates Dendritic Morphology and Behavioural Flexibility in Mice.

MicroRNAs are known to be critical regulators of neuronal plasticity. The highly conserved, hypoxia-regulated microRNA-210 (miR-210) has been shown to be associated with long-term memory in invertebrates and dysregulated in neurodevelopmental and neurodegenerative disease models. However, the role of miR-210 in mammalian neuronal function and cognitive behaviour remains unexplored. Here we generated Nestin-cre-driven miR-210 neuronal knockout mice to characterise miR-210 regulation and function using in vitro and in vivo methods. We identified miR-210 localisation throughout neuronal somas and dendritic processes and increased levels of mature miR-210 in response to neural activity in vitro. Loss of miR-210 in neurons resulted in higher oxidative phosphorylation and ROS production following hypoxia and increased dendritic arbour density in hippocampal cultures. Additionally, miR-210 knockout mice displayed altered behavioural flexibility in rodent touchscreen tests, particularly during early reversal learning suggesting processes underlying updating of information and feedback were impacted. Our findings support a conserved, activity-dependent role for miR-210 in neuroplasticity and cognitive function.

A Sustained Immune Response Supports Long-Term Antiviral Immune Priming in the Pacific Oyster, Crassostrea gigas.

Over the last decade, innate immune priming has been evidenced in many invertebrate phyla. If mechanistic models have been proposed, molecular studies aiming to substantiate these models have remained scarce. We reveal here the transcriptional signature associated with immune priming in the oyster Crassostrea gigas Oysters were fully protected against Ostreid herpesvirus 1 (OsHV-1), a major oyster pathogen, after priming with poly(I·C), which mimics viral double-stranded RNA. Global analysis through RNA sequencing of oyster and viral genes after immune priming and viral infection revealed that poly(I·C) induces a strong antiviral response that impairs OsHV-1 replication. Protection is based on a sustained upregulation of immune genes, notably genes involved in the interferon pathway and apoptosis, which control subsequent viral infection. This persistent antiviral alert state remains active over 4 months and supports antiviral protection in the long term. This acquired resistance mechanism reinforces the molecular foundations of the sustained response model of immune priming. It further opens the way to applications (pseudovaccination) to cope with a recurrent disease that causes dramatic economic losses in the shellfish farming industry worldwide.IMPORTANCE In the last decade, important discoveries have shown that resistance to reinfection can be achieved without a functional adaptive immune system, introducing the concept of innate immune memory in invertebrates. However, this field has been constrained by the limited number of molecular mechanisms evidenced to support these phenomena. Taking advantage of an invertebrate species, the Pacific oyster (Crassostrea gigas), in which we evidenced one of the longest and most effective periods of protection against viral infection observed in an invertebrate, we provide the first comprehensive transcriptomic analysis of antiviral innate immune priming. We show that priming with poly(I·C) induced a massive upregulation of immune-related genes, which control subsequent viral infection, and it was maintained for over 4 months after priming. This acquired resistant mechanism reinforces the molecular foundations of the sustained response model of immune priming. It opens the way to pseudovaccination to prevent the recurrent diseases that currently afflict economically or ecologically important invertebrates.

The Effects of Roundup and its Chemical Constituents on Learning and Long-Term Memory Consolidation in Lymnaea palustris

Environmental contamination from herbicide use is a prevalent problem. Roundup is a widely used herbicide that consists of two active ingredients: Glyphosate and Diquat Dibromide (DD). Previous work has shown that these compounds have negative impacts on development, fecundity, and other processes. We analyzed the effects of chronic exposure to Roundup, Glyphosate, and DD on learning and memory in the pond snail, Lymnaea palustris. L. palustris was treated with Roundup, Glyphosate, or DD for 1-2 weeks. Snails were operantly conditioned according to standard procedures. The results indicated that at concentrations of Roundup and DD legally allowed in human drinking water for a 1-week treatment, learning was not inhibited; however, memory formation was impaired. At the same concentration for 2 weeks, or at a 5-fold higher concentration for 1- and 2-week treatments, both learning and memory are significantly impaired. A 1-week treatment with Glyphosate impairs memory but not learning. Western Blot analysis was conducted to detect changes in Protein Kinase C (PKC) abundance, which has been shown to be linked to learning and memory. Previous work in our laboratory has shown a positive correlation between the abundance of PKC and memory consolidation in control snails; this increase is abolished upon exposure to Roundup or its constituents. Our findings suggest that Roundup and its constituents have damaging effects on learning and memory in invertebrates. Similar effects may occur in vertebrates because of the high level of conservation of learning and memory processes across species.

Innate Immune Memory in Invertebrate Metazoans: A Critical Appraisal.

The ability of developing immunological memory, a characteristic feature of adaptive immunity, is clearly present also in innate immune responses. In fact, it is well known that plants and invertebrate metazoans, which only have an innate immune system, can mount a faster and more effective response upon re-exposure to a stimulus. Evidence of immune memory in invertebrates comes from studies in infection immunity, natural transplantation immunity, individual, and transgenerational immune priming. These studies strongly suggest that environment and lifestyle take part in the development of immunological memory. However, in several instances the formal correlation between the phenomenon of immune memory and molecular and functional immune parameters is still missing. In this review, we have critically examined the cellular and humoral aspects of the invertebrate immune memory responses. In particular, we have focused our analysis on studies that have addressed immune memory in the most restrictive meaning of the term, i.e., the response to a challenge of a quiescent immune system that has been primed in the past. These studies highlight the central role of an increase in the number of immune cells and of their epigenetic re-programming in the establishment of sensu stricto immune memory in invertebrates.

Tyraminergic modulation of agonistic outcomes in crayfish.

Octopamine, a biogenic amine, modulates various behaviors, ranging from locomotion and aggression to learning and memory in invertebrates. Several studies recently demonstrated that tyramine, the biological precursor of octopamine, also affects behaviors independent of octopamine. Here we investigated the involvement of tyramine in agonistic interaction of the male crayfish Procambarus clarkii. When male crayfish fight, larger animals (3-7% difference in body length) are more likely to win. By contrast, direct injection of tyramine or octopamine counteracted the physical advantage of larger animals. Tyramine or octopamine-injected naive large animals were mostly beaten by untreated smaller naive animals. This pharmacological effect was similar to the loser effect in which subordinate larger animals are frequently beaten by smaller animals. Furthermore, loser effects were partly eliminated by either injection of epinastine, an octopamine blocker, or yohimbine, a tyramine blocker, and significantly diminished by injection of a mixture of both blockers. We also observed that tyramine levels in the subesophageal ganglion were remarkably increased in subordinate crayfish after losing a fight. These results suggest that tyramine modulates aggressive levels of crayfish and contributes to the loser effect in parallel with octopamine.

Cu,Zn Superoxide Dismutase Genes in Tribolium castaneum: Evolution, Molecular Characterisation, and Gene Expression during Immune Priming.

The production of reactive oxygen species (ROS) is a normal consequence of the aerobic cell metabolism. Despite their high and potentially detrimental reactivity with various biomolecules, the endogenous production of ROS is a vital part of physiological, immunological, and molecular processes that contribute to fitness. The role of ROS in host–parasite interactions is frequently defined by their contribution to innate immunity as effectors, promoting parasite death during infections. In vertebrates, ROS and antioxidant system enzymes, such as superoxide dismutase (SOD) are also involved in acquired immune memory, where they are responsible for T-cell signalling, activation, proliferation, and viability. Based on recent findings, ROS are now also assumed to play a role in immune priming, i.e., a form of memory in invertebrates. In this study, the potential involvement of Cu,Zn SODs in immunity of the red flour beetle Tribolium castaneum is described for the first time, applying an approach that combines an in silico gene characterisation with an in vivo immune priming experiment using the Gram-positive entomopathogen Bacillus thuringiensis. We identified an unusually high number of three different transcripts for extracellular SOD and found that priming leads to a fine-tuned modulation of SOD expression, highlighting the potential of physiological co-adaptations for immune phenotypes.

What vaccination studies tell us about immunological memory within the innate immune system of cultured shrimp and crayfish

The possibility of immunological memory in invertebrates is a topic that has recently attracted a lot of attention. Today, even vertebrates are known to exhibit innate immune responses that show memory-like properties, and since these responses are triggered by cells that are involved in the innate immune system, it seems that immune specificity and immune memory do not necessarily require the presence of B cells and T cells after all. This kind of immune response has been called “immune priming” or “trained immunity”. In this report, we review recent observations and our current understanding of immunological memory within the innate immune system in cultured shrimp and crayfish after vaccination with live vaccine, killed vaccine and subunit vaccines. We also discuss the possible mechanisms involved in this immune response.

Octopaminergic system in the central nervous system of the terrestrial slug Limax.

The terrestrial slug Limax can learn to avoid the odor of some food (e.g., carrot juice) by the simultaneous presentation of an aversive stimulus (e.g., bitterness of quinidine). This type of associative memory critically depends on the higher olfactory center, the procerebrum in the central nervous system. The modulation of the local field potential (LFP) oscillation recorded on the procerebrum has been thought to reflect the information processing of the odor that elicits the behavioral change, such as avoidance of the aversively learned odor or approaching an attractive food's odor. Here we focused on octopamine, an important neuromodulator involved in learning and memory in invertebrates, and considered to be the invertebrate equivalent of noradrenaline. We identified a few octopaminergic neurons in the subesophageal and buccal ganglia, and a larger number near the procerebrum in the cerebral ganglia, using immunohistochmical staining and in situ hybridization of tyramine β-hydroxylase, an octopamine-synthesizing enzyme. Application of octopamine reduced the frequency of LFP oscillation in a dose-dependent manner, and this effect was inhibited by preincubation with phentolamine. High-performance liquid chromatography analysis revealed the presence of octopamine, noradrenaline, and adrenaline in the central nervous system. Unexpectedly, noradrenaline and adrenaline both accelerated the LFP oscillation, in contrast to octopamine. Our results suggest that octopamine and noradrenaline have distinct functions in olfactory information processing, in spite of their structural similarity. J. Comp. Neurol. 524:3849-3864, 2016. © 2016 Wiley Periodicals, Inc.