Biology subjects

Sachse, S.

Publications and source records attributed to Sachse, S..

9 recordsLinked to original sources

bioRxiv2023

Olfactory learning modulates a neural circuit mediating innate odor-guided behavior in Drosophila

Behavior is often categorized as being innate or learned, with the specific circuits being assigned to one of these categories. In Drosophila, neural circuits mediating an innate behavioral response are considered as being "hard-wired", as activation of these neuronal pathways leads to stereotyped behaviors. However, only a limited number of studies assessed whether innate behaviors and their underlying neural circuits are plastic or show experience-dependent modulation. Here, we show that experience modulates second-order olfactory neurons involved in innate behavioral responses. We focus on the neural circuit defined by multiglomerular projection neurons (mPNs) that target the lateral horn, a structure relevant in the genesis of innate behavior. We show that mPNs, coding for odor attraction, are bidirectionally modulated after olfactory associative learning: when an olfactory stimulus is paired with an aversive electric shock, the activity of these neurons is decreased, while when the odor is paired with a sucrose-reward they are potentiated. We further show that this modulation requires glutamate and serotonin signaling, and that downstream third-order neurons are consequently affected. The bidirectional nature of the plasticity in these neurons is reflected in behavior: silencing mPN activity leads to odor avoidance, while artificial activation induces approach. While output from the mPNs is not required in aversive olfactory conditioning, silencing these neurons during retrieval of appetitive memories leads to a significant memory impairment. Artificially activating these neurons during odor presentation is sufficient to generate a 3 h appetitive memory. Our study in flies shows that a neural circuit coding for innate odor attraction can contribute to learned behavior, is modulated by olfactory learning and can provide reward-like reinforcement.

neuroscience↗

bioRxiv2023

Experience-dependent plasticity of a highly specific olfactory circuit in Drosophila melanogaster

Drosophila melanogaster encounters a variety of odor cues signaling potentially harmful threats through-out its life, which are detected by highly specialized olfactory circuits enabling the animal to avoid them. We studied whether such crucial neuronal pathways are hard-wired or can be modulated by experience. Using long-term exposure to high concentrations of geosmin, an indicator of potentially lethal microorganisms, we demonstrate at the single-cell level that the underlying neuronal circuitry undergoes structural changes in the antennal lobe, while higher brain centers remain unaffected. In particular, second-order neurons show neurite extensions and synaptic remodeling after the exposure period, whereas olfactory sensory neurons and glia cells remain unaffected. Flies that were exposed to geosmin tolerate this innately aversive odorant in general choice and oviposition assays. We show that even a highly specific olfactory circuit is plastic and adaptable to environmental changes. HIGHLIGHTSO_LIThe highly specific geosmin circuit is modulated by experience-dependent plasticity C_LIO_LIPN dendritic extensions cause a volumetric increase of the geosmin-detecting glomerulus C_LIO_LILNs are remodeled while OSNs and glia cells remain unaffected by long-term exposure C_LIO_LIFlies adapt their behavior to an odorant signaling a potential lethal threat C_LI

neuroscience↗

bioRxiv2022

Aversive bimodal associations impact visual and olfactory memory performance in Drosophila

Insects rely heavily on sampling information from their environment for survival and fitness. Different sensory channels with dedicated downstream neural substrates are programmed to fine tune these signals and translate them into usable instructions to mediate complex behaviors. Sensory information can also be learned and stored as memories that influence decisions in the future. The learning of unimodal sensory signals, especially olfaction, has been studied extensively in different conditioning paradigms in different insects. Using the Drosophila melanogaster model in our work, we first investigated differences in the efficiencies of aversive associative visual and olfactory learning using sensory cues that are innately very attractive, such as blue or green light as well as food odors found in fruits or yeast. We then combined the presentation of visual and olfactory sensory stimuli during training to study the effect of bimodal integration on learning performance. When trained unimodally, flies did not easily learn visual stimuli, but when trained bimodally, they developed a significant short-term visual memory after a single learning trial. The bimodal training also suppressed the phototaxis response of the flies to near abolishment. However, a similar training did not enhance the short-term olfactory memory and in some cases, even caused reduction in strength. An enhancement after bimodal training was only seen with a weak long-term olfactory memory retrieved after 24h. Our study demonstrates that bimodal sensory integration is not always synergistic, but is conditional upon the training paradigm and inherent learning abilities of the sensory modalities involved.

animal behavior and cognition↗

bioRxiv2021

Higher-order olfactory neurons in the lateral horn supports odor valence and odor identity coding in Drosophila

Understanding neuronal representations of odor-evoked activities and their progressive transformation from the sensory level to higher brain centers features one of the major aims in olfactory neuroscience. Here, we investigated how odor information is transformed and represented in higher-order neurons of the lateral horn, one of the higher olfactory centers implicated in determining innate behavior, using Drosophila melanogaster. We focused on a subset of third-order glutamatergic lateral horn neurons (LHNs) and characterized their odor coding properties in relation to their presynaptic partner neurons, the projection neurons (PNs) by two-photon functional imaging. We found that odors evoke reproducible, stereotypic and odor-specific response patterns in LHNs. Notably, odor-evoked responses in these neurons are valence-specific in a way that their response amplitude is positively correlated with innate odor preferences. We postulate that this valence-specific activity is the result of integrating inputs from multiple olfactory channels through second-order neurons. GRASP and micro-lesioning experiments provide evidence that glutamatergic LHNs obtain their major excitatory input from uniglomerular PNs, while they receive an odor-specific inhibition through inhibitory multiglomerular PNs. In summary, our study indicates that odor representations in glutamatergic LHNs encode hedonic valence and odor identity and primarily retain the odor coding properties of second-order neurons.

neuroscience↗

bioRxiv2021

An ammonium transporter is a non-canonical olfactory receptor for ammonia

Two families of ligand-gated ion channels function as olfactory receptors in insects. Here, we show that these canonical olfactory receptors are not necessary for responses to ammonia, a key ecological odor that is attractive to many insects including disease vectors and agricultural pests. Instead, we show that a member of the ancient electrogenic ammonium transporter family, Amt, is a new type of olfactory receptor. We report two hitherto unidentified olfactory neuron populations that mediate neuronal and behavioral responses to ammonia. Their endogenous ammonia responses are Amt-dependent, and ectopic expression of either Drosophila or Anopheles Amt confers ammonia sensitivity. Amt is the first transporter known to function as an olfactory receptor in animals, and its role may be conserved across insect species.

neuroscience↗

bioRxiv2021

Comparative dissection of the peripheral olfactory system of the Chagas disease vectors Rhodnius prolixus and Rhodnius brethesi

American trypanosomiasis or Chagas disease is thought to be transmitted by both domestic and sylvatic species of Triatominae. These haematophagous insects use sensory cues to find their vertebrate hosts. Among them, odorants have been shown to play a key role. Previous work revealed morphological differences in the sensory apparatus of sylvatic and domestic species of Triatomines, but to date a functional study of the olfactory system is not available. After examining the antennal sensilla with scanning electronic microscopy (SEM), we compared olfactory responses of the domestic Rhodnius prolixus and the sylvatic Rhodnius brethesi with an electrophysiological approach. In electroantennogram (EAG) recordings, we first show that the antenna of R. prolixus shows high responses to carboxylic acids, compounds found in their habitat and headspace of hosts. We then compared responses from olfactory sensory neurons (OSNs) housed in the grooved peg sensilla of both species as these are tuned to these compounds using single-sensillum recordings (SSR). In R. prolixus, the SSR responses revealed a narrower tuning breath than its sylvatic counterpart, with the latter showing responses to a broader range of chemical classes. Additionally, we observed significant differences between these two species in their response to particular volatiles, such as amyl acetate and butyryl chloride. In summary, the closely related, but ecologically differentiated R. prolixus and R. brethesi display distinct differences in their olfactory functions. Considering the ongoing rapid destruction of the natural habitat of sylvatic species and likely shifts towards environments shaped by humans, we expect that our results will contribute to the design of efficient vector control strategies in the future. Author SummaryAmerican Tripanosomiasis, also known as Chagas disease, is a disease which no one speaks out, although there are up to eight million people infected worldwide. Its causative agent is the protozoan Tripanosoma cruzi which is transmitted by triatomine insects, alias kissing bugs. Several studies have highlighted the importance of olfaction for host-seeking behavior in these insects, which enables them to target their vertebrate hosts, and to get their vital blood meal, while infecting them at the same time. Vector control strategies have been the most efficient policy to combat the spread of Chagas disease by triatomine insects. However, recent changes in the natural habitats of these insects challenge their effectiveness, as species so far thought to be exclusive to sylvatic environments are now frequently found in peridomestic areas. In this context, to understand how sylvatic and domestic kissing bugs detect odors to locate their host and choose their habitats is highly relevant. In this study, we compare the olfactory system of the domestic kissing bug Rhodnius prolixus and its sylvatic counterpart Rhodnius brethesi at a morphological and functional level. We reveal that detection of host and habitat volatiles share many similarities, but also exhibit pronounced differences between both species.

ecology↗

bioRxiv2020

Alcohol boosts pheromone production in male flies and makes them sexier

The attraction of Drosophila melanogaster towards byproducts of alcoholic fermentation, especially ethanol, has been extensively studied 1-4. However, the adaptive value of this behavior has not been elucidated. Previous studies have suggested anthropomorphic interpretations of D. melanogaster behavior towards alcohols 5,6. Here, we instead assert that there exists a simple yet vital biological rationale for alcohol contact and consumption by these insects. We show that exposure to alcohols, especially methanol, results in an immediate amplification of fatty acid ester pheromone levels, which in turn elevates the probability that a male will successfully compete for a female during courtship. We proceed to identify three types of olfactory sensory neurons that detect ethanol and methanol. Moreover, we trace the ensuing neural circuits and reveal their role in controlling both attraction and aversion, where valence is balanced around mating status. Based on our results, we deduce that male flies associate with sources of alcohol as a biological imperative related to reproduction, and we provide an assessment of how and why D. melanogaster is associated with alcohol using a sound ecological and natural history approach to this previously enigmatic biological phenomenon. One sentence summaryFlies gain pheromone and courtship advantages with alcohol, but methanol is toxic, thus flies must balance risk versus reward.

neuroscience↗

bioRxiv2019

Mate discrimination among subspecies through a conserved olfactory pathway

Signaling mechanisms underlying the sexual isolation of species are poorly understood. Using four subspecies of Drosophila mojavensis as a model, we identify two behaviorally active male-specific pheromones. One functions as a conserved male anti-aphrodisiac in all subspecies and acts via gustation. The second induces female receptivity via olfaction exclusively in the two subspecies that produce it. Genetic analysis of the cognate receptor for the olfactory pheromone indicates an important role for this sensory pathway in promoting sexual isolation of subspecies, in collaboration with auditory signals. Surprisingly, the peripheral sensory pathway detecting this pheromone is conserved molecularly, physiologically and anatomically across subspecies. These observations imply that subspecies-specific behaviors arise from differential interpretation of the same peripheral cue, reminiscent of sexually conserved detection but dimorphic interpretation of male pheromones in D. melanogaster. Our results reveal that, during incipient speciation, pheromone production, detection and interpretation do not necessarily evolve in a coordinate manner.

neuroscience↗

bioRxiv2019

Optimization of insect odorant receptor trafficking and functional expression via transient transfection in HEK293 cells

Insect odorant receptors show a limited functional expression in various heterologous expression systems including insect and mammalian cells. This may be in part due to the absence of key components driving the release of these proteins from the endoplasmic reticulum and directing them to the plasma membrane. In order to mitigate this problem we took advantage of small export signals within the human HCN1 and Rhodopsin that have been shown to promote protein release from the endoplasmic reticulum and the trafficking of post-Golgi vesicles, respectively. Moreover, we designed a new vector based on a bidirectional expression cassette to drive the functional expression of the insect odorant receptor co-receptor (Orco) and an odor-binding odorant receptor, simultaneously. We show that this new method can be used to reliably express insect odorant receptors in HEK293 cells via transient transfection and that is highly suitable for downstream applications using automated and high-throughput imaging platforms.

zoology↗