Odor motion sensing enables complex plume navigation

ABSTRACTInsects can detect bilateral differences in odor concentration between their two antennae, enabling them to sense odor gradients. While gradients aid navigation in simple odor environments like static ribbons, their role in navigating complex plumes remains unknown. Here, we use a virtual reality paradigm to show that Drosophila use bilateral sensing for a distinct computation: detecting the motion of odor signals. Such odor direction sensing is computationally equivalent to motion detection algorithms underlying motion detection in vision. Simulations of natural plumes reveal that odor motion contains valuable directional information absent from the airflow, which Drosophila indeed exploit when navigating natural plumes. Olfactory studies dating back a century have stressed the critical role of wind sensing for insect navigation (Flügge, 1934; Kennedy and Marsh, 1974); we reveal an entirely orthogonal direction cue used by flies in natural environments, and give theoretical arguments suggesting that this cue may be of broad use across the animal kingdom.

Navigating a diversity of turbulent plumes is enhanced by sensing complementary temporal features of odor signals

We and others have shown that during odor plume navigation, walking Drosophila melanogaster bias their motion upwind in response to both the frequency of their encounters with the odor (Demir et al., 2020), and the intermittency of the odor signal, i.e. the fraction of time the signal is above a detection threshold (Alvarez-Salvado et al., 2018). Here we combine and simplify previous mathematical models that recapitulated these data to investigate the benefits of sensing both of these temporal features, and how these benefits depend on the spatiotemporal statistics of the odor plume. Through agent-based simulations, we find that navigators that only use frequency or intermittency perform well in some environments – achieving maximal performance when gains are near those inferred from experiment – but fail in others. Robust performance across diverse environments requires both temporal modalities. However, we also find a steep tradeoff when using both sensors simultaneously, suggesting a strong benefit to modulating how much each sensor is weighted, rather than using both in a fixed combination across plumes.

Odor Blocking Of Stress

ABSTRACTScents have been employed for millennia to allay fear and stress, but whether they do so is poorly understood. In response to fear and stress, hypothalamic corticotropin releasing hormone neurons (CRHNs) induce increases in blood stress hormones. Here, we find that certain structurally and perceptually dissimilar odorants can block mouse stress hormone responses to three potent stressors: physical restraint, predator odor, and male-male social confrontation. Both odorants activate GABAergic inhibitory neurons presynaptic to CRHNs in the hypothalamic ventromedial nucleus (VMH). Stimulation of those neurons inhibits restraint-induced activation of CRHNs and stress hormone increase, mimicking a blocking odorant. Conversely, their silencing prevents odorant blocking of both responses. Notably, we also observed odor blocking of stressor activation in neurons presynaptic to CRHNs in the bed nucleus of the stria terminalis (BNST). Together, these findings indicate that selected odorants can indeed block stress responses, and that odor blocking can occur via two routes: a direct route in which blocking odor signals directly inhibit CRHNs and an indirect route in which they inhibit stressor activation of neurons presynaptic to CRHNs and prevent them from transmitting stress signals to CRHNs.

Olfactory Circuitry and Behavioral Decisions

In mammals, odor information detected by olfactory sensory neurons is converted to a topographic map of activated glomeruli in the olfactory bulb. Mitral cells and tufted cells transmit signals sequentially to the olfactory cortex for behavioral outputs. To elicit innate behavioral responses, odor signals are directly transmitted by distinct subsets of mitral cells from particular functional domains in the olfactory bulb to specific amygdala nuclei. As for the learned decisions, input signals are conveyed by tufted cells as well as by mitral cells to the olfactory cortex. Behavioral scene cells link the odor information to the valence cells in the amygdala to elicit memory-based behavioral responses. Olfactory decision and perception take place in relation to the respiratory cycle. How is the sensory quality imposed on the olfactory inputs for behavioral outputs? How are the two types of odor signals, innate and learned, processed during respiration? Here, we review recent progress on the study of neural circuits involved in decision making in the mouse olfactory system. Expected final online publication date for the Annual Review of Physiology, Volume 83 is February 10, 2021. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.

Tuning of olfactory cortex ventral tenia tecta neurons to distinct task elements of goal-directed behavior

The ventral tenia tecta (vTT) is a component of the olfactory cortex and receives both bottom-up odor signals and top-down signals. However, the roles of the vTT in odor-coding and integration of inputs are poorly understood. Here, we investigated the involvement of the vTT in these processes by recording the activity from individual vTT neurons during the performance of learned odor-guided reward-directed tasks in mice. We report that individual vTT cells are highly tuned to a specific behavioral epoch of learned tasks, whereby the duration of increased firing correlated with the temporal length of the behavioral epoch. The peak time for increased firing among recorded vTT cells encompassed almost the entire temporal window of the tasks. Collectively, our results indicate that vTT cells are selectively activated during a specific behavioral context and that the function of the vTT changes dynamically in a context-dependent manner during goal-directed behaviors.

Bi-directional encoding of context-based odor signals and behavioral states by the nucleus of the lateral olfactory tract neurons

The nucleus of the lateral olfactory tract (nLOT) is not only a part of the olfactory cortex that receives olfactory sensory inputs from the olfactory bulb, but also one of the cortical amygdala areas that regulates motivational behaviors. To examine how the neural ensemble activity of the nLOT is modulated by motivational processes that occur during various states of learned goal-directed behaviors, we recorded nLOT spike activities of mice performing odor-guided go/no-go tasks for obtaining a water reward. We found that the majority of the nLOT neurons exhibited sharp go-cue excitation and persistent no-go-cue inhibition responses triggered by an odor onset. The bi-directional cue encoding introduced nLOT population response dynamics and provided a high odor decoding accuracy before executing cue-odor-evoked behaviors. The go-cue preferred neurons were also activated in the reward drinking state, indicating context-based odor-outcome associations. These findings suggest that the nLOT neurons play an important role in the translation from context-based odor information to appropriate behavioral motivation.

Controlling and measuring dynamic odorant stimuli in the laboratory

Animals experience complex odorant stimuli that vary widely in composition, intensity and temporal properties. However, stimuli used to study olfaction in the laboratory are much simpler. This mismatch arises from the challenges in measuring and controlling them precisely and accurately. Even simple pulses can have diverse kinetics that depend on their molecular identity. Here, we introduce a model to describe how stimulus kinetics depend on the molecular identity of the odorant and the geometry of the delivery system. We describe methods to deliver dynamic odorant stimuli of several types, including broadly distributed stimuli that reproduce some of the statistics of naturalistic plumes, in a reproducible and precise manner. Finally, we introduce a method to calibrate a Photo-Ionization Detector to any odorant it can detect, using no additional components. Our approaches are affordable and flexible and can be used to advance our understanding of how olfactory neurons encode real-world odor signals.

Front-end Weber-Fechner gain control enhances the fidelity of combinatorial odor coding

We showed previously (Gorur-Shandilya et al., 2017) that Drosophila olfactory receptor neurons (ORNs) expressing the co-receptor Orco scale their gain inversely with mean odor intensity according to Weber-Fechner’s law. Here, we show that this front-end adaptation promotes the reconstruction of odor identity from dynamic odor signals, even in the presence of confounding background odors and rapid intensity fluctuations. These enhancements are further aided by known downstream transformations in the antennal lobe and mushroom body. Our results, which are applicable to various odor classification and reconstruction schemes, stem from the fact that this adaptation mechanism is not intrinsic to the identity of the receptor involved. Instead, a feedback mechanism adjusts receptor sensitivity based on the activity of the receptor-Orco complex, according to Weber-Fechner’s law. Thus, a common scaling of the gain across Orco-expressing ORNs may be a key feature of ORN adaptation that helps preserve combinatorial odor codes in naturalistic landscapes.

The Olfactory System of Zebrafish as a Model for the Study of Neurotoxicity and Injury: Implications for Neuroplasticity and Disease

The olfactory system, composed of the olfactory organs and the olfactory bulb, allows organisms to interact with their environment and through the detection of odor signals. Olfaction mediates behaviors pivotal for survival, such as feeding, mating, social behavior, and danger assessment. The olfactory organs are directly exposed to the milieu, and thus are particularly vulnerable to damage by environmental pollutants and toxicants, such as heavy metals, pesticides, and surfactants, among others. Given the widespread occurrence of olfactory toxicants, there is a pressing need to understand the effects of these harmful compounds on olfactory function. Zebrafish (Danio rerio) is a valuable model for studying human physiology, disease, and toxicity. Additionally, the anatomical components of the zebrafish olfactory system are similar to those of other vertebrates, and they present a remarkable degree of regeneration and neuroplasticity, making it an ideal model for the study of regeneration, reorganization and repair mechanisms following olfactory toxicant exposure. In this review, we focus on (1) the anatomical, morphological, and functional organization of the olfactory system of zebrafish; (2) the adverse effects of olfactory toxicants and injury to the olfactory organ; and (3) remodeling and repair neuroplasticity mechanisms following injury and degeneration by olfactory toxicant exposure.