Sensory collectives in natural systems.

Groups of animals inhabit vastly different sensory worlds, or umwelten, which shape fundamental aspects of their behaviour. Yet the sensory ecology of species is rarely incorporated into the emerging field of collective behaviour, which studies the movements, population-level behaviours, and emergent properties of animal groups. Here, we review the contributions of sensory ecology and collective behaviour to understanding how animals move and interact within the context of their social and physical environments. Our goal is to advance and bridge these two areas of inquiry and highlight the potential for their creative integration. To achieve this goal, we organise our review around the following themes: (1) identifying the promise of integrating collective behaviour and sensory ecology; (2) defining and exploring the concept of a 'sensory collective'; (3) considering the potential for sensory collectives to shape the evolution of sensory systems; (4) exploring examples from diverse taxa to illustrate neural circuits involved in sensing and collective behaviour; and (5) suggesting the need for creative conceptual and methodological advances to quantify 'sensescapes'. In the final section, (6) applications to biological conservation, we argue that these topics are timely, given the ongoing anthropogenic changes to sensory stimuli (e.g. via light, sound, and chemical pollution) which are anticipated to impact animal collectives and group-level behaviour and, in turn, ecosystem composition and function. Our synthesis seeks to provide a forward-looking perspective on how sensory ecologists and collective behaviourists can both learn from and inspire one another to advance our understanding of animal behaviour, ecology, adaptation, and evolution.

Regularly occurring bouts of retinal movements suggest an REM sleep-like state in jumping spiders.

Sleep and sleep-like states are present across the animal kingdom, with recent studies convincingly demonstrating sleep-like states in arthropods, nematodes, and even cnidarians. However, the existence of different sleep phases across taxa is as yet unclear. In particular, the study of rapid eye movement (REM) sleep is still largely centered on terrestrial vertebrates, particularly mammals and birds. The most salient indicator of REM sleep is the movement of eyes during this phase. Movable eyes, however, have evolved only in a limited number of lineages-an adaptation notably absent in insects and most terrestrial arthropods-restricting cross-species comparisons. Jumping spiders, however, possess movable retinal tubes to redirect gaze, and in newly emerged spiderlings, these movements can be directly observed through their temporarily translucent exoskeleton. Here, we report evidence for an REM sleep-like state in a terrestrial invertebrate: periodic bouts of retinal movements coupled with limb twitching and stereotyped leg curling behaviors during nocturnal resting in a jumping spider. Observed retinal movement bouts were consistent, including regular durations and intervals, with both increasing over the course of the night. That these characteristic REM sleep-like behaviors exist in a highly visual, long-diverged lineage further challenges our understanding of this sleep state. Comparisons across such long-diverged lineages likely hold important questions and answers about the visual brain as well as the origin, evolution, and function of REM sleep.

Olfactory Strategies in the Defensive Behaviour of Insects.

Most animals must defend themselves in order to survive. Defensive behaviour includes detecting predators or intruders, avoiding them by staying low-key or escaping or deterring them away by means of aggressive behaviour, i.e., attacking them. Responses vary across insect species, ranging from individual responses to coordinated group attacks in group-living species. Among different modalities of sensory perception, insects predominantly use the sense of smell to detect predators, intruders, and other threats. Furthermore, social insects, such as honeybees and ants, communicate about danger by means of alarm pheromones. In this review, we focus on how olfaction is put to use by insects in defensive behaviour. We review the knowledge of how chemical signals such as the alarm pheromone are processed in the insect brain. We further discuss future studies for understanding defensive behaviour and the role of olfaction.

Neural and behavioural responses of the pollen-specialist bee Andrena vaga to Salix odours.

An effective means of finding food is crucial for organisms. Whereas specialized animals select a small number of potentially available food sources, generalists use a broader range. Specialist (oligolectic) bees forage on a small range of flowering plants for pollen and use primarily olfactory and visual cues to locate their host flowers. So far, however, little is known about the specific cues oligoleges use to discriminate between hosts and non-hosts and how floral scent compounds of hosts and non-hosts are processed in the bees' olfactory system. In this study, we recorded physiological responses of the antennae (electroantennographic detection coupled to gas chromatography; GC-EAD) and in the brain (optical imaging; GC imaging), and studied host-finding behaviour of oligolectic Andrena vaga bees, a specialist on Salix plants. In total, we detected 37 physiologically active compounds in host and non-host scents. 4-Oxoisophorone, a common constituent in the scent of many Salix species, evoked strong responses in the antennal lobe glomeruli of A. vaga, but not the generalist honeybee Apis mellifera. The specific glomerular responses to 4-oxoisophorone in natural Salix scents reveals a high degree of specialization in A. vaga for this typical Salix odorant component. In behavioural experiments, we found olfactory cues to be the key attractants for A. vaga to Salix hosts, which are also used to discriminate between hosts and non-hosts, and A. vaga demonstrated a behavioural activity for 4-oxoisophorone. A high sensitivity to floral scents enables the specialized bees to effectively find flowers and it appears that A. vaga bees are highly tuned to 4-oxoisophorone at a very low concentration.

Social modulation of individual preferences in cockroaches.

In social species, decision-making is both influenced by, and in turn influences, the social context. This reciprocal feedback introduces coupling across scales, from the neural basis of sensing, to individual and collective decision-making. Here, we adopt an integrative approach investigating decision-making in dynamical social contexts. When choosing shelters, isolated cockroaches prefer vanillin-scented (food-associated) shelters over unscented ones, yet in groups, this preference is inverted. We demonstrate that this inversion can be replicated by replacing the full social context with social odors: presented alone food and social odors are attractive, yet when presented as a mixture they are avoided. Via antennal lobe calcium imaging, we show that neural activity in vanillin-responsive regions reduces as social odor concentration increases. Thus, we suggest that the mixture is evaluated as a distinct olfactory object with opposite valence, providing a mechanism that would naturally result in individuals avoiding what they perceive as recently exploited resources.

Complexity and plasticity in honey bee phototactic behaviour.

The ability to move towards or away from a light source, namely phototaxis, is essential for a number of species to find the right environmental niche and may have driven the appearance of simple visual systems. In this study we ask if the later evolution of more complex visual systems was accompanied by a sophistication of phototactic behaviour. The honey bee is an ideal model organism to tackle this question, as it has an elaborate visual system, demonstrates exquisite abilities for visual learning and performs phototaxis. Our data suggest that in this insect, phototaxis has wavelength specific properties and is a highly dynamical response including multiple decision steps. In addition, we show that previous experience with a light (through exposure or classical aversive conditioning) modulates the phototactic response. This plasticity is dependent on the wavelength used, with blue being more labile than green or ultraviolet. Wavelength, intensity and past experience are integrated into an overall valence for each light that determines phototactic behaviour in honey bees. Thus, our results support the idea that complex visual systems allow sophisticated phototaxis. Future studies could take advantage of these findings to better understand the neuronal circuits underlying this processing of the visual information.

Coding of odour and space in the hemimetabolous insect Periplaneta americana.

The general architecture of the olfactory system is highly conserved from insects to humans, but neuroanatomical and physiological differences can be observed across species. The American cockroach, inhabiting dark shelters with a rather stable olfactory landscape, is equipped with long antennae used for sampling the surrounding air-space for orientation and navigation. The antennae's exceptional length provides a wide spatial working range for odour detection; however, it is still largely unknown whether and how this is also used for mapping the structure of the olfactory environment. By selectively labelling antennal lobe projection neurons with a calcium-sensitive dye, we investigated the logic of olfactory coding in this hemimetabolous insect. We show that odour responses are stimulus specific and concentration dependent, and that structurally related odorants evoke physiologically similar responses. By using spatially confined stimuli, we show that proximal stimulations induce stronger and faster responses than distal ones. Spatially confined stimuli of the female pheromone periplanone B activate a subregion of the male macroglomerulus. Thus, we report that the combinatorial logic of odour coding deduced from holometabolous insects applies also to this hemimetabolous species. Furthermore, a fast decrease in sensitivity along the antenna, not supported by a proportionate decrease in sensillar density, suggests a neural architecture that strongly emphasizes neuronal inputs from the proximal portion of the antenna.

Aversive Training of Honey Bees in an Automated Y-Maze.

Honeybees have remarkable learning abilities given their small brains, and have thus been established as a powerful model organism for the study of learning and memory. Most of our current knowledge is based on appetitive paradigms, in which a previously neutral stimulus (e.g., a visual, olfactory, or tactile stimulus) is paired with a reward. Here, we present a novel apparatus, the yAPIS, for aversive training of walking honey bees. This system consists in three arms of equal length and at 120° from each other. Within each arm, colored lights (λ = 375, 465 or 520 nm) or odors (here limonene or linalool) can be delivered to provide conditioned stimuli (CS). A metal grid placed on the floor and roof delivers the punishment in the form of mild electric shocks (unconditioned stimulus, US). Our training protocol followed a fully classical procedure, in which the bee was exposed sequentially to a CS paired with shocks (CS+) and to another CS not punished (CS-). Learning performance was measured during a second phase, which took advantage of the Y-shape of the apparatus and of real-time tracking to present the bee with a choice situation, e.g., between the CS+ and the CS-. Bees reliably chose the CS- over the CS+ after only a few training trials with either colors or odors, and retained this memory for at least a day, except for the shorter wavelength (λ = 375 nm) that produced mixed results. This behavior was largely the result of the bees avoiding the CS+, as no evidence was found for attraction to the CS-. Interestingly, trained bees initially placed in the CS+ spontaneously escaped to a CS- arm if given the opportunity, even though they could never do so during the training. Finally, honey bees trained with compound stimuli (color + odor) later avoided either components of the CS+. Thus, the yAPIS is a fast, versatile and high-throughput way to train honey bees in aversive paradigms. It also opens the door for controlled laboratory experiments investigating bimodal integration and learning, a field that remains in its infancy.

Corrigendum: Calcium in Kenyon Cell Somata as a Substrate for an Olfactory Sensory Memory in Drosophila.

[This corrects the article on p. 128 in vol. 12, PMID: 29867361.].

Calcium in Kenyon Cell Somata as a Substrate for an Olfactory Sensory Memory in Drosophila.

Animals can form associations between temporally separated stimuli. To do so, the nervous system has to retain a neural representation of the first stimulus until the second stimulus appears. The neural substrate of such sensory stimulus memories is unknown. Here, we search for a sensory odor memory in the insect olfactory system and characterize odorant-evoked Ca2+ activity at three consecutive layers of the olfactory system in Drosophila: in olfactory receptor neurons (ORNs) and projection neurons (PNs) in the antennal lobe, and in Kenyon cells (KCs) in the mushroom body. We show that the post-stimulus responses in ORN axons, PN dendrites, PN somata, and KC dendrites are odor-specific, but they are not predictive of the chemical identity of past olfactory stimuli. However, the post-stimulus responses in KC somata carry information about the identity of previous olfactory stimuli. These findings show that the Ca2+ dynamics in KC somata could encode a sensory memory of odorant identity and thus might serve as a basis for associations between temporally separated stimuli.

Neuroscience: An Olfactory Homunculus in the Insect Brain.

Animals can follow olfactory traces to find food, detect a sexual mate, or avoid predators. A new study reveals that pheromone-specific projection neurons in the cockroach have a spatially tuned receptive field, and allow encoding spatial information of an odorant.

The Role of the Sucrose-Responsive IR60b Neuron for Drosophila melanogaster: A Hypothesis.

In a recent paper, Joseph and colleagues (Joseph et al. 2017) have characterized an IR60b receptor-expressing neuron in Drosophila. They showed that it responds to sucrose and serves to limit sucrose consumption, and proposed that it may thereby act to prevent overfeeding. Here, we propose an alternative hypothesis for the functional role of sucrose feeding control, and for how this limitation of sucrose uptake is accomplished. Adult fruit flies feed by excreting saliva onto the food, and imbibing the predigested liquefied food, or by filling the crop, where the food is predigested. Enzymes in the saliva hydrolyze starch and disaccharides into absorbable monosaccharides. Premature ingestion into the midgut would not give the enzymes in the saliva enough time to predigest the food. Thus, IR60b neurons might serve as a sensor to monitor the digestive state of external food or crop content: when disaccharides (sucrose) concentration is high, ingestion to the gut is inhibited, keeping a low concentration of starch and disaccharides in the midgut.

Normalizing brain activity across individuals using functional reference mapping.

Neural activity can be mapped across individuals using brain atlases, but when spatial relationships are not equal, these techniques collapse. We map activity across individuals using functional registration, based on physiological responses to predetermined reference stimuli. Data from several individuals are integrated into a common multidimensional stimulus space, where dimensionality and axes are defined by these reference stimuli. We used this technique to discriminate volatile compounds with a cohort of Drosophila flies, by recording odor responses in receptor neurons on the flies' antennae. We propose this technique for the development of reliable biological sensors when activity raw data cannot be calibrated. In particular, this technique will be useful for evaluating physiological measurements in natural chemosensory systems, and therefore will allow to exploit the sensitivity and selectivity of olfactory receptors present in the animal kingdom for analytical purposes.

Take time: odor coding capacity across sensory neurons increases over time in Drosophila.

Due to the highly efficient olfactory code, olfactory sensory systems are able to reliably encode enormous numbers of olfactory stimuli. The olfactory code consists of combinatorial activation patterns across sensory neurons, thus its capacity exceeds the number of involved classes of sensory neurons by a manifold. Activation patterns are not static but vary over time, caused by the temporally complex response dynamics of the individual sensory neuron responses. We systematically analyzed the temporal dynamics of olfactory sensory neuron responses to a diverse set of odorants. We find that response dynamics depend on the combination of sensory neuron and odorant and that information about odorant identity can be extracted from the time course of the response. We also show that new response dynamics can arise when mixing two odorants. Our data show that temporal dynamics of odorant responses are able to significantly enhance the coding capacity of olfactory sensory systems.

Trace Conditioning in Drosophila Induces Associative Plasticity in Mushroom Body Kenyon Cells and Dopaminergic Neurons.

Dopaminergic neurons (DANs) signal punishment and reward during associative learning. In mammals, DANs show associative plasticity that correlates with the discrepancy between predicted and actual reinforcement (prediction error) during classical conditioning. Also in insects, such as Drosophila, DANs show associative plasticity that is, however, less understood. Here, we study associative plasticity in DANs and their synaptic partners, the Kenyon cells (KCs) in the mushroom bodies (MBs), while training Drosophila to associate an odorant with a temporally separated electric shock (trace conditioning). In most MB compartments DANs strengthened their responses to the conditioned odorant relative to untrained animals. This response plasticity preserved the initial degree of similarity between the odorant- and the shock-induced spatial response patterns, which decreased in untrained animals. Contrary to DANs, KCs (α'/ß'-type) decreased their responses to the conditioned odorant relative to untrained animals. We found no evidence for prediction error coding by DANs during conditioning. Rather, our data supports the hypothesis that DAN plasticity encodes conditioning-induced changes in the odorant's predictive power.

Different Roles for Honey Bee Mushroom Bodies and Central Complex in Visual Learning of Colored Lights in an Aversive Conditioning Assay.

The honey bee is an excellent visual learner, but we know little about how and why it performs so well, or how visual information is learned by the bee brain. Here we examined the different roles of two key integrative regions of the brain in visual learning: the mushroom bodies and the central complex. We tested bees' learning performance in a new assay of color learning that used electric shock as punishment. In this assay a light field was paired with electric shock. The other half of the conditioning chamber was illuminated with light of a different wavelength and not paired with shocks. The unrestrained bee could run away from the light stimulus and thereby associate one wavelength with punishment, and the other with safety. We compared learning performance of bees in which either the central complex or mushroom bodies had been transiently inactivated by microinjection of the reversible anesthetic procaine. Control bees learned to escape the shock-paired light field and to spend more time in the safe light field after a few trials. When ventral lobe neurons of the mushroom bodies were silenced, bees were no longer able to associate one light field with shock. By contrast, silencing of one collar region of the mushroom body calyx did not alter behavior in the learning assay in comparison to control treatment. Bees with silenced central complex neurons did not leave the shock-paired light field in the middle trials of training, even after a few seconds of being shocked. We discussed how mushroom bodies and the central complex both contribute to aversive visual learning with an operant component.

Coincidence of pheromone and plant odor leads to sensory plasticity in the heliothine olfactory system.

Male moths possess a highly specialized olfactory system comprised of two segregated sub-arrangements dedicated to processing information about plant odors and pheromones, respectively. Communication between these two sub-systems has been described at the peripheral level, but relatively little is known about putative interactions at subsequent synaptic relays. The male moth faces the challenge of seeking out the conspecific female in a highly dynamic odor world. The female-produced pheromone blend, which is a limited resource serving as guidance for the male, will reach his antennae in intermittent pockets of odor filaments mixed with volatiles from various plants. In the present study we performed calcium imaging for measuring odor-evoked responses in the uni-glomerular antennal-lobe projection neurons (analog to mitral cells in the vertebrate olfactory bulb) of Helicoverpa armigera. In order to investigate putative interactions between the two sub-systems tuned to plant volatiles and pheromones, respectively, we performed repeated stimulations with a selection of biologically relevant odors. We found that paired stimulation with a plant odor and the pheromone led to suppressed responses in both sub-systems as compared to those evoked during initial stimulation including application of each odor stimulus alone. The fact that the suppression persisted also after pairing, indicates the existence of a Hebbian-like plasticity in the primary olfactory center established by temporal pairing of the two odor stimulation categories.

DNA methylation mediates neural processing after odor learning in the honeybee.

DNA methyltransferases (Dnmts) - epigenetic writers catalyzing the transfer of methyl-groups to cytosine (DNA methylation) - regulate different aspects of memory formation in many animal species. In honeybees, Dnmt activity is required to adjust the specificity of olfactory reward memories and bees' relearning capability. The physiological relevance of Dnmt-mediated DNA methylation in neural networks, however, remains unknown. Here, we investigated how Dnmt activity impacts neuroplasticity in the bees' primary olfactory center, the antennal lobe (AL) an equivalent of the vertebrate olfactory bulb. The AL is crucial for odor discrimination, an indispensable process in forming specific odor memories. Using pharmacological inhibition, we demonstrate that Dnmt activity influences neural network properties during memory formation in vivo. We show that Dnmt activity promotes fast odor pattern separation in trained bees. Furthermore, Dnmt activity during memory formation increases both the number of responding glomeruli and the response magnitude to a novel odor. These data suggest that Dnmt activity is necessary for a form of homoeostatic network control which might involve inhibitory interneurons in the AL network.

A High-Bandwidth Dual-Channel Olfactory Stimulator for Studying Temporal Sensitivity of Olfactory Processing.

Animals encounter fine-scale temporal patterns of odorant mixtures that contain information about the distance and number of odorant sources. To study the role of such temporal cues for odorant detection and source localization, one needs odorant delivery devices that are capable of mimicking the temporal stimulus statistics of natural odor plumes. However, current odorant delivery devices either lack temporal resolution or are limited to a single odorant channel. Here, we present an olfactory stimulator that features precise control of high-bandwidth stimulus dynamics, which allows generating arbitrary fluctuating binary odorant mixtures. We provide a comprehensive characterization of the stimulator's performance and use it to demonstrate that odor background affects the temporal resolution of insect olfactory receptor neurons, and we present a hitherto unknown odor pulse-tracking capability of up to 60 Hz in Kenyon cells, which are higher order olfactory neurons of the insect brain. This stimulator might help investigating whether and how animals use temporal stimulus cues for odor detection and source localization. Because the stimulator is easy to replicate it can facilitate generating the same odor stimulus dynamics at different experimental setups and across different labs.