Not since Paul the octopus became famous during the 2010 soccer world cup have scientists realized that decision-making is not a capacity exclusive to the so-called 'higher' animals. Invertebrate animals show an amazing capacity for making decisions even if the external circumstances provide little or no information. This Research Topic celebrates the diversity of decision-making by showcasing the most well-studied cases in a range of invertebrate species.

University of Regensburg

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Frontiers in Neuroscience

Decision Neuroscience

Frontiers in Psychology

Decision-making in invertebrates

Invertebrates have always been the reductionist neuroscientist&apos;s favorite. After all, are their nervous systems not simpler, their behavior not more stereotyped and reproducible than those of vertebrates, unfettered by cognition, and intelligence which would only serve to complicate the already tricky study of how neurons do the things they do? Until not too long ago, neurobiological study of invertebrate behavior seemed, by and large, to corroborate this view. We now believe we understand the giant fibers giving rise to fast escape behaviors from crustaceans, mollusks, or insects. We have discovered the central pattern generators controlling swimming in leeches, flying in locusts, feeding in mollusks, digesting in crustaceans, and walking in stick insects. We can now identify and characterize many of the neurons that process the visual stimuli prompting flies to turn, the courtship sounds attracting crickets and grasshoppers, or the olfactory stimuli enticing bees to extend their proboscis.However, the apparent relative (to vertebrates) simplicity started to disappear, once scientists began to either omit parameters from the traditional experiments, add additional ones, or simply look more closely. This research topic highlights a selection of experiments which serve to demonstrate the kind of decision-making that is taking place even in invertebrates as soon as the experiment allows for sufficient degrees of freedom.A mind-blowing list of recent examples of the kind of revelations scientists discover when they start to look in greater detail at phenomena we thought we understood is provided in <a href="#B3">Herberholz and Marquart (2012)</a>. Starting from the well-known giant fiber escape circuits in crustaceans, mollusks and insects, they show that today the role of these giant fiber systems is either questionable or only a small part of a range of different escape maneuvers with a large variety of different neural systems subserving them.The uncrowned champions of reducing simple systems even more by eliminating as many confounding factors as possible must be the mollusks. In their riveting, neuron-by-neuron account of how even isolated ganglia of the marine snail Aplysia make spontaneous decisions and incorporate environmental feedback in this process of adaptive behavioral choice, <a href="#B8">Nargeot and Simmers (2012)</a> elucidate principles of operant conditioning, habit formation, and compulsivity at a level of biological detail that will take decades to reach in most other systems.Experiments in which parameters have been added to the traditional stimulus and its response can be grouped into two classes, those in which the internal state of the animal is taken into account and those in which stimuli are provided such as to establish a choice situation. The former class includes experiments described by <a href="#B2">Heinrich et al. (2012)</a> on the neuronal and hormonal mechanisms influencing the decision to sing in different stages but under otherwise identical external circumstances in grasshoppers. <a href="#B1">Gaudry and Kristan (2012)</a> explain in impressive detail the mechanisms by which different states of the medicinal leech exert their top-down influence on the processing of sensory stimuli at different stages of sensory processing, depending on the state of the animal. Far from simply being relayed to “higher” centers of the nervous system, from the sensory neurons onwards, other information is constantly being cross-correlated with and related to the sensory stream. While the coding properties of sensory neurons are the focus of <a href="#B7">Marsat and Pollack's (2012)</a> review on ultrasound avoidance in crickets—neuronal bursts encode a “danger signal” from ultrasound often emitted by hunting bats—the work they review also shows that the final decision to initiate evasion behavior in crickets is formed in the brain of the animals, two to four synapses downstream of the sensory neurons that encode the “danger signal.” Analogously, <a href="#B4">Hirayama et al.'s (2012)</a> contribution on the predatory sea-slug Pleurobranchea details the neural processes by which the animal's satiation state regulates approach/avoidance behavior.The simplest way to add a second parameter to a traditional stimulus-response experiment is to choose a stimulus that allows two different responses, even if the state of the animal is not altered. <a href="#B9">Ritzmann et al. (2012)</a> describe such experiments in which cockroaches must decide on which side (left vs. right or above vs. below) of an obstacle to proceed. The behavior of the animals is best being described as a value-based decision in which the needs of the animal (e.g., shelter) are negotiated with the ease of mastering the barrier. This value-based negotiation of rivaling incentives for an animal was also described in <a href="#B3">Herberholz and Marquart's (2012)</a> account of crayfish negotiating simultaneous appetitive (food) and aversive (predator) stimuli of different relative value. This well-known cost/benefit tradeoff often encountered by animals in non-laboratory circumstances was also explicitly modeled in <a href="#B4">Hirayama et al. (2012)</a>. A further step away from the simpler, traditional experiments is to not only provide choices between stimuli or behaviors, but to integrate these with variations in the state of the animal. <a href="#B5">Itskov and Ribeiro (2013)</a> describe experiments with fruit flies deciding about whether, what and when to eat. Due to rigorous behavioral experiments combined with Drosophila's genetic tool arsenal, the neuronal and molecular mechanisms underlying the processes with which various external stimuli interact with different satiation states are slowly unraveling. Probably the most complex, most difficult to control and hence most challenging class of experiments are those where the outcome of the experiment determines the state of the animal and the stimuli are attached to other animals. <a href="#B10">Stevenson and Rillich's (2012)</a> review of their work in cricket aggression begins to elucidate some of the neuronal components involved in mediating the simultaneous influence of experience, motivation, and sensory stimuli on the decision to fight or flee.Perhaps to some the least surprising, but nevertheless most impressive decision-making performance can be reported from hymenopterans, arguably one of the smartest classes of invertebrates, perhaps only with a close rival in cephalopods (which are sadly not represented in this research topic). <a href="#B11">Wolf et al. (2012)</a> remind us that the well-known navigational capabilities of desert ants are only a small aspect of their sophisticated and flexible food search and retrieval strategies. Of course, a research topic on invertebrate decision-making would not be complete without everybody's poster child for arthropod intelligence, the honey bee. In a tour de force, <a href="#B12">Zhang et al. (2012)</a> lead us through a maze of different experiments showcasing the many levels of abstraction these animals can deploy in order to make adaptive foraging decisions. Probably among the conceptually deepest contributions is <a href="#B6">Jeanson et al.'s (2012)</a> overview on collective decisions. Analogous to the super-organism concept of eusocial insects, it is tempting to transfer the factors guiding the emergence of a collective decision of individual invertebrates (e.g., noise amplified by positive feedback) and test if neurons in a decision-making circuit in a brain follow analogous rules when generating decisions such as the ones described above. Bringing us back to reductionism, as documented by <a href="#B6">Jeanson et al. (2012)</a>, these factors were identified mainly by reducing the contribution of the environment and relying only on the decision-making capabilities inherent in the individual animals themselves.

Invertebrate behavior—actions or responses?

To survive and successfully reproduce animals need to maintain a balanced intake of nutrients and energy. The nervous system of insects has evolved multiple mechanisms to regulate feeding behavior. When animals are faced with the choice to feed, several decisions must be made: whether or not to eat, how much to eat, what to eat, and when to eat. Using Drosophila melanogaster substantial progress has been achieved in understanding the neuronal and molecular mechanisms controlling feeding decisions. These feeding decisions are implemented in the nervous system on multiple levels, from alterations in the sensitivity of peripheral sensory organs to the modulation of memory systems. This review discusses methodologies developed in order to study insect feeding, the effects of neuropeptides and neuromodulators on feeding behavior, behavioral evidence supporting the existence of internal energy sensors, neuronal and molecular mechanisms controlling protein intake, and finally the regulation of feeding by circadian rhythms and sleep. From the discussed data a conceptual framework starts to emerge which aims to explain the molecular and neuronal processes maintaining the stability of the internal milieu.

To survive and successfully reproduce animals need to maintain a balanced intake of nutrients and energy. The nervous system of insects has evolved multiple mechanisms to regulate feeding behavior. When animals are faced with the choice to feed, several decisions must be made: whether or not to eat, how much to eat, what to eat, and when to eat. Using Drosophila melanogaster substantial progress has been achieved in understanding the neuronal and molecular mechanisms controlling feeding decisions. These feeding decisions are implemented in the nervous system on multiple levels, from alterations in the sensitivity of peripheral sensory organs to the modulation of memory systems. This review discusses methodologies developed in order to study insect feeding, the effects of neuropeptides and neuromodulators on feeding behavior, behavioral evidence supporting the existence of internal energy sensors, neuronal and molecular mechanisms controlling protein intake, and finally the regulation of feeding by circadian rhythms and sleep. From the discussed data a conceptual framework starts to emerge which aims to explain the molecular and neuronal processes maintaining the stability of the internal milieu.

The Dilemmas of the Gourmet Fly: The Molecular and Neuronal Mechanisms of Feeding and Nutrient Decision Making in Drosophila

A simple circuit for cost-benefit decision derived from behavioral and neural studies of the predatory sea-slug Pleurobranchaea may closely resemble that upon which the more complex valuation and decision processes of the social vertebrates are built. The neuronal natures of the pathways in the connectionist model comprise classic central pattern generators, bipolar switch mechanisms, and neuromodulatory state regulation. Marked potential exists for exploring more complex neuroeconomic behavior by appending appropriate circuitry in simulo.

A simple circuit for cost-benefit decision derived from behavioral and neural studies of the predatory sea-slug Pleurobranchaea may closely resemble that upon which the more complex valuation and decision processes of the social vertebrates are built. The neuronal natures of the pathways in the connectionist model comprise classic central pattern generators, bipolar switch mechanisms, and neuromodulatory state regulation. Marked potential exists for exploring more complex neuroeconomic behavior by appending appropriate circuitry in simulo.

A Core Circuit Module for Cost/Benefit Decision

One of the most important decisions animals have to make is how to respond to an attack from a potential predator. The response must be prompt and appropriate to ensure survival. Invertebrates have been important models in studying the underlying neurobiology of the escape response due to their accessible nervous systems and easily quantifiable behavioral output. Moreover, invertebrates provide opportunities for investigating these processes at a level of analysis not available in most other organisms. Recently, there has been a renewed focus in understanding how value-based calculations are made on the level of the nervous system, i.e., when decisions are made under conflicting circumstances, and the most desirable choice must be selected by weighing the costs and benefits for each behavioral choice. This article reviews samples from the current literature on anti-predator decision making in invertebrates, from single neurons to complex behaviors. Recent progress in understanding the mechanisms underlying value-based behavioral decisions is also discussed.

One of the most important decisions animals have to make is how to respond to an attack from a potential predator. The response must be prompt and appropriate to ensure survival. Invertebrates have been important models in studying the underlying neurobiology of the escape response due to their accessible nervous systems and easily quantifiable behavioral output. Moreover, invertebrates provide opportunities for investigating these processes at a level of analysis not available in most other organisms. Recently, there has been a renewed focus in understanding how value-based calculations are made on the level of the nervous system, i.e., when decisions are made under conflicting circumstances, and the most desirable choice must be selected by weighing the costs and benefits for each behavioral choice. This article reviews samples from the current literature on anti-predator decision making in invertebrates, from single neurons to complex behaviors. Recent progress in understanding the mechanisms underlying value-based behavioral decisions is also discussed.

Decision Making and Behavioral Choice during Predator Avoidance

Ritualized fighting between conspecifics is an inherently dangerous behavioral strategy, optimized to secure limited resources at minimal cost and risk. To be adaptive, potential rewards, and costs of aggression must be assessed to decide when it would be more opportune to fight or flee. We summarize insights into the proximate mechanisms underlying this decision-making process in field crickets. As in other animals, cricket aggression is enhanced dramatically by motor activity, winning, and the possession of resources. Pharmacological manipulations provide evidence that these cases of experience dependent enhancement of aggression are each mediated by octopamine, the invertebrate counterpart to adrenaline/noradrenaline. The data suggest that both physical exertion and rewarding aspects of experiences can activate the octopaminergic system, which increases the propensity to fight. Octopamine thus represents the motivational component of aggression in insects. For the decision to flee, animals are thought to assess information from agonistic signals exchanged during fighting. Cricket fights conform to the cumulative assessment model, in that they persist in fighting until the sum of their opponent’s actions accumulates to some threshold at which they withdraw. We discuss evidence that serotonin, nitric oxide, and some neuropeptides may promote an insect’s tendency to flee. We propose that the decision to fight or flee in crickets is controlled simply by relative behavioral thresholds. Rewarding experiences increase the propensity to fight to a level determined by the modulatory action of octopamine. The animal will then flee only when the accumulated sum of the opponent’s actions surpasses this level; serotonin and nitric oxide may be involved in this process. This concept is in line with the roles proposed for noradrenaline, serotonin, and nitric oxide in mammals and suggests that basic mechanisms of aggressive modulation may be conserved in phylogeny.

Ritualized fighting between conspecifics is an inherently dangerous behavioral strategy, optimized to secure limited resources at minimal cost and risk. To be adaptive, potential rewards, and costs of aggression must be assessed to decide when it would be more opportune to fight or flee. We summarize insights into the proximate mechanisms underlying this decision-making process in field crickets. As in other animals, cricket aggression is enhanced dramatically by motor activity, winning, and the possession of resources. Pharmacological manipulations provide evidence that these cases of experience dependent enhancement of aggression are each mediated by octopamine, the invertebrate counterpart to adrenaline/noradrenaline. The data suggest that both physical exertion and rewarding aspects of experiences can activate the octopaminergic system, which increases the propensity to fight. Octopamine thus represents the motivational component of aggression in insects. For the decision to flee, animals are thought to assess information from agonistic signals exchanged during fighting. Cricket fights conform to the cumulative assessment model, in that they persist in fighting until the sum of their opponent&#x2019;s actions accumulates to some threshold at which they withdraw. We discuss evidence that serotonin, nitric oxide, and some neuropeptides may promote an insect&#x2019;s tendency to flee. We propose that the decision to fight or flee in crickets is controlled simply by relative behavioral thresholds. Rewarding experiences increase the propensity to fight to a level determined by the modulatory action of octopamine. The animal will then flee only when the accumulated sum of the opponent&#x2019;s actions surpasses this level; serotonin and nitric oxide may be involved in this process. This concept is in line with the roles proposed for noradrenaline, serotonin, and nitric oxide in mammals and suggests that basic mechanisms of aggressive modulation may be conserved in phylogeny.

The Decision to Fight or Flee – Insights into Underlying Mechanism in Crickets

In many species of group living invertebrates, in particular arthropods, collective decisions can emerge from the combined actions of individuals and the direct or indirect interactions between individuals. These decisions allow groups of individuals to respond quickly and accurately to changes that occur in their environment. Examples of such decisions are found in a variety of invertebrate taxa and in many different contexts, e.g., exploring a new territory, foraging for food, finding a suitable location where to aggregate or to establish a nest, defending oneself against predators, etc. In this paper we review the collective decisions that have been documented in different invertebrate taxa where individuals are known to live temporarily or permanently in social or gregarious groups. We first present some simple examples of collective decisions involving the choice between two alternatives. We then define the fundamental rules required for these collective decisions to emerge throughout the invertebrate taxon, from simple organisms such as caterpillars, to animals endowed with highly developed perceptive and cognitive capacities such as ants and bees. The presentation of these rules gives us the opportunity to illustrate one of the pitfalls of the study of collective choice in animals by showing through computer simulations how a choice between two alternatives can be misinterpreted as the result of the action of self-organized mechanisms. In the second part, we discuss the peculiarities of collective decisions in invertebrates, their properties, and characteristics. We conclude by discussing the issue of individual complexity in collective decision-making process.

In many species of group living invertebrates, in particular arthropods, collective decisions can emerge from the combined actions of individuals and the direct or indirect interactions between individuals. These decisions allow groups of individuals to respond quickly and accurately to changes that occur in their environment. Examples of such decisions are found in a variety of invertebrate taxa and in many different contexts, e.g., exploring a new territory, foraging for food, finding a suitable location where to aggregate or to establish a nest, defending oneself against predators, etc. In this paper we review the collective decisions that have been documented in different invertebrate taxa where individuals are known to live temporarily or permanently in social or gregarious groups. We first present some simple examples of collective decisions involving the choice between two alternatives. We then define the fundamental rules required for these collective decisions to emerge throughout the invertebrate taxon, from simple organisms such as caterpillars, to animals endowed with highly developed perceptive and cognitive capacities such as ants and bees. The presentation of these rules gives us the opportunity to illustrate one of the pitfalls of the study of collective choice in animals by showing through computer simulations how a choice between two alternatives can be misinterpreted as the result of the action of self-organized mechanisms. In the second part, we discuss the peculiarities of collective decisions in invertebrates, their properties, and characteristics. We conclude by discussing the issue of individual complexity in collective decision-making process.

Key Factors for the Emergence of Collective Decision in Invertebrates

Whereas major insights into the neuronal basis of adaptive behavior have been gained from the study of automatic behaviors, including reflexive and rhythmic motor acts, the neural substrates for goal-directed behaviors in which decision-making about action selection and initiation are crucial, remain poorly understood. However, the mollusk Aplysia is proving to be increasingly relevant to redressing this issue. The functional properties of the central circuits that govern this animal’s goal-directed feeding behavior and particularly the neural processes underlying the selection and initiation of specific feeding actions are becoming understood. In addition to relying on the intrinsic operation of central networks, goal-directed behaviors depend on external sensory inputs that through associative learning are able to shape decision-making strategies. Here, we will review recent findings on the functional design of the central network that generates Aplysia’s feeding-related movements and the sensory-derived plasticity that through learning can modify the selection and initiation of appropriate action. The animal’s feeding behavior and the implications of decision-making will be briefly described. The functional design of the underlying buccal network will then be used to illustrate how cellular diversity and the coordination of neuronal burst activity provide substrates for decision-making. The contribution of specific synaptic and neuronal membrane properties within the buccal circuit will also be discussed in terms of their role in motor pattern selection and initiation. The ability of learning to “rigidify” these synaptic and cellular properties so as to regularize network operation and lead to the expression of stereotyped rhythmic behavior will then be described. Finally, these aspects will be drawn into a conceptual framework of how Aplysia’s goal-directed circuitry compares to the central pattern generating networks for invertebrate rhythmic behaviors.

Whereas major insights into the neuronal basis of adaptive behavior have been gained from the study of automatic behaviors, including reflexive and rhythmic motor acts, the neural substrates for goal-directed behaviors in which decision-making about action selection and initiation are crucial, remain poorly understood. However, the mollusk Aplysia is proving to be increasingly relevant to redressing this issue. The functional properties of the central circuits that govern this animal’s goal-directed feeding behavior and particularly the neural processes underlying the selection and initiation of specific feeding actions are becoming understood. In addition to relying on the intrinsic operation of central networks, goal-directed behaviors depend on external sensory inputs that through associative learning are able to shape decision-making strategies. Here, we will review recent findings on the functional design of the central network that generates Aplysia’s feeding-related movements and the sensory-derived plasticity that through learning can modify the selection and initiation of appropriate action. The animal’s feeding behavior and the implications of decision-making will be briefly described. The functional design of the underlying buccal network will then be used to illustrate how cellular diversity and the coordination of neuronal burst activity provide substrates for decision-making. The contribution of specific synaptic and neuronal membrane properties within the buccal circuit will also be discussed in terms of their role in motor pattern selection and initiation. The ability of learning to “rigidify” these synaptic and cellular properties so as to regularize network operation and lead to the expression of stereotyped rhythmic behavior will then be described. Finally, these aspects will be drawn into a conceptual framework of how Aplysia’s goal-directed circuitry compares to the central pattern generating networks for invertebrate rhythmic behaviors.

Functional Organization and Adaptability of a Decision-Making Network in Aplysia

Animals must routinely deal with barriers as they move through their natural environment. These challenges require directed changes in leg movements and posture performed in the context of ever changing internal and external conditions. In particular, cockroaches use a combination of tactile and visual information to evaluate objects in their path in order to effectively guide their movements in complex terrain. When encountering a large block, the insect uses its antennae to evaluate the object’s height then rears upward accordingly before climbing. A shelf presents a choice between climbing and tunneling that depends on how the antennae strike the shelf; tapping from above yields climbing, while tapping from below causes tunneling. However, ambient light conditions detected by the ocelli can bias that decision. Similarly, in a T-maze turning is determined by antennal contact but influenced by visual cues. These multi-sensory behaviors led us to look at the central complex as a center for sensori-motor integration within the insect brain. Visual and antennal tactile cues are processed within the central complex and, in tethered preparations, several central complex units changed firing rates in tandem with or prior to altered step frequency or turning, while stimulation through the implanted electrodes evoked these same behavioral changes. To further test for a central complex role in these decisions, we examined behavioral effects of brain lesions. Electrolytic lesions in restricted regions of the central complex generated site specific behavioral deficits. Similar changes were also found in reversible effects of procaine injections in the brain. Finally, we are examining these kinds of decisions made in a large arena that more closely matches the conditions under which cockroaches forage. Overall, our studies suggest that CC circuits may indeed influence the descending commands associated with navigational decisions, thereby making them more context dependent.

Animals must routinely deal with barriers as they move through their natural environment. These challenges require directed changes in leg movements and posture performed in the context of ever changing internal and external conditions. In particular, cockroaches use a combination of tactile and visual information to evaluate objects in their path in order to effectively guide their movements in complex terrain. When encountering a large block, the insect uses its antennae to evaluate the object&#x2019;s height then rears upward accordingly before climbing. A shelf presents a choice between climbing and tunneling that depends on how the antennae strike the shelf; tapping from above yields climbing, while tapping from below causes tunneling. However, ambient light conditions detected by the ocelli can bias that decision. Similarly, in a T-maze turning is determined by antennal contact but influenced by visual cues. These multi-sensory behaviors led us to look at the central complex as a center for sensori-motor integration within the insect brain. Visual and antennal tactile cues are processed within the central complex and, in tethered preparations, several central complex units changed firing rates in tandem with or prior to altered step frequency or turning, while stimulation through the implanted electrodes evoked these same behavioral changes. To further test for a central complex role in these decisions, we examined behavioral effects of brain lesions. Electrolytic lesions in restricted regions of the central complex generated site specific behavioral deficits. Similar changes were also found in reversible effects of procaine injections in the brain. Finally, we are examining these kinds of decisions made in a large arena that more closely matches the conditions under which cockroaches forage. Overall, our studies suggest that CC circuits may indeed influence the descending commands associated with navigational decisions, thereby making them more context dependent.

Deciding Which Way to Go: How Do Insects Alter Movements to Negotiate Barriers?

The decision to feed is a complex task that requires making several small independent choices. Am I hungry? Where do I look for food? Is there something better I’d rather be doing? When should I stop? With all of these questions, it is no wonder that decisions about feeding depend on several sensory modalities and that the influences of these sensory systems would be evident throughout the nervous system. The leech is uniquely well suited for studying these complicated questions due to its relatively simple nervous system, its exceptionally well-characterized behaviors and neural circuits, and the ease with which one can employ semi-intact preparations to study the link between physiology and decision-making. We will begin this review by discussing the cellular substrates that govern the decision to initiate and to terminate a bout of feeding. We will then discuss how feeding temporarily blocks competing behaviors from being expressed while the animal continues to feed. Then we will review what is currently known about how feeding affects long-term behavioral choices of the leech. Finally, we conclude with a short discussion of the advantages of the leech’s decision-making circuit’s design and how this design might be applicable to all decision circuits.

The decision to feed is a complex task that requires making several small independent choices. Am I hungry? Where do I look for food? Is there something better I&#x2019;d rather be doing? When should I stop? With all of these questions, it is no wonder that decisions about feeding depend on several sensory modalities and that the influences of these sensory systems would be evident throughout the nervous system. The leech is uniquely well suited for studying these complicated questions due to its relatively simple nervous system, its exceptionally well-characterized behaviors and neural circuits, and the ease with which one can employ semi-intact preparations to study the link between physiology and decision-making. We will begin this review by discussing the cellular substrates that govern the decision to initiate and to terminate a bout of feeding. We will then discuss how feeding temporarily blocks competing behaviors from being expressed while the animal continues to feed. Then we will review what is currently known about how feeding affects long-term behavioral choices of the leech. Finally, we conclude with a short discussion of the advantages of the leech&#x2019;s decision-making circuit&#x2019;s design and how this design might be applicable to all decision circuits.

Decision Points: The Factors Influencing the Decision to Feed in the Medicinal Leech

North African desert ants, Cataglyphis fortis, are established model organisms in animal navigation research. Cataglyphis re-visit plentiful feeding sites, but their decision to return to a feeder and the organization of food searches has been little studied. Here we provide a review of recent advances regarding this topic. At least two parameters determine the ants’ assessment of site quality, namely, amount of food available and reliability of food encounter on subsequent visits. The amount of food appears to be judged by the concentration of items at the food uptake site. Initially the amount of food in a feeder dominates the foragers’ decision to return, whereas learning about reliability takes precedence in the course of a few visits. The location of a worthwhile site is determined by the animals’ path integration system. In particular, the distance of the feeding site is memorized as the arithmetic average of the distances covered during the previous outbound and homebound journeys. Feeding sites that are small and inconspicuous cannot be approached directly with sufficient certainty, due to inevitable inaccuracies of the path integrator. Instead, desert ants steer downwind of the goal to encounter the odor plume emanating from the food and they follow this plume to the feeder. The angle steered downwind reflects the animals’ maximal navigation error and is adjusted according to experience. In summary, food searches of desert ants provide an unexpected wealth of features that may advance our understanding of search, navigation, and decision strategies. There are several aspects that warrant further scrutiny.

North African desert ants, Cataglyphis fortis, are established model organisms in animal navigation research. Cataglyphis re-visit plentiful feeding sites, but their decision to return to a feeder and the organization of food searches has been little studied. Here we provide a review of recent advances regarding this topic. At least two parameters determine the ants’ assessment of site quality, namely, amount of food available and reliability of food encounter on subsequent visits. The amount of food appears to be judged by the concentration of items at the food uptake site. Initially the amount of food in a feeder dominates the foragers’ decision to return, whereas learning about reliability takes precedence in the course of a few visits. The location of a worthwhile site is determined by the animals’ path integration system. In particular, the distance of the feeding site is memorized as the arithmetic average of the distances covered during the previous outbound and homebound journeys. Feeding sites that are small and inconspicuous cannot be approached directly with sufficient certainty, due to inevitable inaccuracies of the path integrator. Instead, desert ants steer downwind of the goal to encounter the odor plume emanating from the food and they follow this plume to the feeder. The angle steered downwind reflects the animals’ maximal navigation error and is adjusted according to experience. In summary, food searches of desert ants provide an unexpected wealth of features that may advance our understanding of search, navigation, and decision strategies. There are several aspects that warrant further scrutiny.

Re-Visiting of Plentiful Food Sources and Food Search Strategies in Desert Ants

Decision making in invertebrates often relies on simple neural circuits composed of only a few identified neurons. The relative simplicity of these circuits makes it possible to identify the key computation and neural properties underlying decisions. In this review, we summarize recent research on the neural basis of ultrasound avoidance in crickets, a response that allows escape from echolocating bats. The key neural property shaping behavioral output is high-frequency bursting of an identified interneuron, AN2, which carries information about ultrasound stimuli from receptor neurons to the brain. AN2’s spike train consists of clusters of spikes – bursts – that may be interspersed with isolated, non-burst spikes. AN2 firing is necessary and sufficient to trigger avoidance steering but only high-rate firing, such as occurs in bursts, evokes this response. AN2 bursts are therefore at the core of the computation involved in deciding whether or not to steer away from ultrasound. Bursts in AN2 are triggered by synaptic input from nearly synchronous bursts in ultrasound receptors. Thus the population response at the very first stage of sensory processing – the auditory receptor – already differentiates the features of the stimulus that will trigger a behavioral response from those that will not. Adaptation, both intrinsic to AN2 and within ultrasound receptors, scales the burst-generating features according to the stimulus statistics, thus filtering out background noise and ensuring that bursts occur selectively in response to salient peaks in ultrasound intensity. Furthermore AN2’s sensitivity to ultrasound varies adaptively with predation pressure, through both developmental and evolutionary mechanisms. We discuss how this key relationship between bursting and the triggering of avoidance behavior is also observed in other invertebrate systems such as the avoidance of looming visual stimuli in locusts or heat avoidance in beetles.

Decision making in invertebrates often relies on simple neural circuits composed of only a few identified neurons. The relative simplicity of these circuits makes it possible to identify the key computation and neural properties underlying decisions. In this review, we summarize recent research on the neural basis of ultrasound avoidance in crickets, a response that allows escape from echolocating bats. The key neural property shaping behavioral output is high-frequency bursting of an identified interneuron, AN2, which carries information about ultrasound stimuli from receptor neurons to the brain. AN2&#x2019;s spike train consists of clusters of spikes &#x2013; bursts &#x2013; that may be interspersed with isolated, non-burst spikes. AN2 firing is necessary and sufficient to trigger avoidance steering but only high-rate firing, such as occurs in bursts, evokes this response. AN2 bursts are therefore at the core of the computation involved in deciding whether or not to steer away from ultrasound. Bursts in AN2 are triggered by synaptic input from nearly synchronous bursts in ultrasound receptors. Thus the population response at the very first stage of sensory processing &#x2013; the auditory receptor &#x2013; already differentiates the features of the stimulus that will trigger a behavioral response from those that will not. Adaptation, both intrinsic to AN2 and within ultrasound receptors, scales the burst-generating features according to the stimulus statistics, thus filtering out background noise and ensuring that bursts occur selectively in response to salient peaks in ultrasound intensity. Furthermore AN2&#x2019;s sensitivity to ultrasound varies adaptively with predation pressure, through both developmental and evolutionary mechanisms. We discuss how this key relationship between bursting and the triggering of avoidance behavior is also observed in other invertebrate systems such as the avoidance of looming visual stimuli in locusts or heat avoidance in beetles.

Bursting Neurons and Ultrasound Avoidance in Crickets

The interplay of neural and hormonal mechanisms activated by entero- and extero-receptors biases the selection of actions by decision making neuronal circuits. The reproductive behavior of acoustically communicating grasshoppers, which is regulated by short-term neural and longer-term hormonal mechanisms, has frequently been used to study the cellular and physiological processes that select particular actions from the species-specific repertoire of behaviors. Various grasshoppers communicate with species- and situation-specific songs in order to attract and court mating partners, to signal reproductive readiness, or to fend off competitors. Selection and coordination of type, intensity, and timing of sound signals is mediated by the central complex, a highly structured brain neuropil known to integrate multimodal pre-processed sensory information by a large number of chemical messengers. In addition, reproductive activity including sound production critically depends on maturation, previous mating experience, and oviposition cycles. In this regard, juvenile hormone released from the corpora allata has been identified as a decisive hormonal signal necessary to establish reproductive motivation in grasshopper females. Both regulatory systems, the central complex mediating short-term regulation and the corpora allata mediating longer-term regulation of reproduction-related sound production mutually influence each other’s activity in order to generate a coherent state of excitation that promotes or suppresses reproductive behavior in respective appropriate or inappropriate situations. This review summarizes our current knowledge about extrinsic and intrinsic factors that influence grasshopper reproductive motivation, their representation in the nervous system and their integrative processing that mediates the initiation or suppression of reproductive behaviors.

The interplay of neural and hormonal mechanisms activated by entero- and extero-receptors biases the selection of actions by decision making neuronal circuits. The reproductive behavior of acoustically communicating grasshoppers, which is regulated by short-term neural and longer-term hormonal mechanisms, has frequently been used to study the cellular and physiological processes that select particular actions from the species-specific repertoire of behaviors. Various grasshoppers communicate with species- and situation-specific songs in order to attract and court mating partners, to signal reproductive readiness, or to fend off competitors. Selection and coordination of type, intensity, and timing of sound signals is mediated by the central complex, a highly structured brain neuropil known to integrate multimodal pre-processed sensory information by a large number of chemical messengers. In addition, reproductive activity including sound production critically depends on maturation, previous mating experience, and oviposition cycles. In this regard, juvenile hormone released from the corpora allata has been identified as a decisive hormonal signal necessary to establish reproductive motivation in grasshopper females. Both regulatory systems, the central complex mediating short-term regulation and the corpora allata mediating longer-term regulation of reproduction-related sound production mutually influence each other&#x2019;s activity in order to generate a coherent state of excitation that promotes or suppresses reproductive behavior in respective appropriate or inappropriate situations. This review summarizes our current knowledge about extrinsic and intrinsic factors that influence grasshopper reproductive motivation, their representation in the nervous system and their integrative processing that mediates the initiation or suppression of reproductive behaviors.

Reproduction-Related Sound Production of Grasshoppers Regulated by Internal State and Actual Sensory Environment

Honeybees can easily be trained to perform different types of discrimination tasks under controlled laboratory conditions. This review describes a range of experiments carried out with free-flying forager honeybees under such conditions. The research done over the past 30 or so years suggests that cognitive abilities (learning and perception) in insects are more intricate and flexible than was originally imagined. It has become apparent that honeybees are capable of a variety of visually guided tasks, involving decision making under challenging situations: this includes simultaneously making use of different sensory modalities, such as vision and olfaction, and learning to use abstract concepts such as “sameness” and “difference.” Many studies have shown that decision making in foraging honeybees is highly flexible. The trained animals learn how to solve a task, and do so with a high accuracy, but when they are presented with a new variation of the task, they apply the learnt rules from the earlier setup to the new situation, and solve the new task as well. Honeybees therefore not only feature a rich behavioral repertoire to choose from, but also make decisions most apt to the current situation. The experiments in this review give an insight into the environmental cues and cognitive resources that are probably highly significant for a forager bee that must continually make decisions regarding patches of resources to be exploited.

Honeybees can easily be trained to perform different types of discrimination tasks under controlled laboratory conditions. This review describes a range of experiments carried out with free-flying forager honeybees under such conditions. The research done over the past 30 or so years suggests that cognitive abilities (learning and perception) in insects are more intricate and flexible than was originally imagined. It has become apparent that honeybees are capable of a variety of visually guided tasks, involving decision making under challenging situations: this includes simultaneously making use of different sensory modalities, such as vision and olfaction, and learning to use abstract concepts such as &#x201c;sameness&#x201d; and &#x201c;difference.&#x201d; Many studies have shown that decision making in foraging honeybees is highly flexible. The trained animals learn how to solve a task, and do so with a high accuracy, but when they are presented with a new variation of the task, they apply the learnt rules from the earlier setup to the new situation, and solve the new task as well. Honeybees therefore not only feature a rich behavioral repertoire to choose from, but also make decisions most apt to the current situation. The experiments in this review give an insight into the environmental cues and cognitive resources that are probably highly significant for a forager bee that must continually make decisions regarding patches of resources to be exploited.