Aversive social learning with a dead conspecific is achieved by Pavlovian conditioning in crickets.

Social learning, learning from other individuals, has been demonstrated in many animals, including insects, but its detailed neural mechanisms remain virtually unknown. We showed that crickets (Gryllus bimaculatus) exhibit aversive social learning with a dead conspecific. When a learner cricket was trained to observe a dead cricket on a drinking apparatus, the learner avoided the odor of that apparatus thereafter.

Independent operations of appetitive and aversive conditioning systems lead to simultaneous production of conflicting memories in an insect.

Pavlovian conditioning is a ubiquitous form of associative learning that enables animals to remember appetitive and aversive experiences. Animals possess appetitive and aversive conditioning systems that memorize and retrieve appetitive and aversive experiences. Here, we addressed a question of whether integration of competing appetitive and aversive information takes place during the encoding of the experience or during memory retrieval.

Interactive parallel sex pheromone circuits that promote and suppress courtship behaviors in the cockroach.

Many animals use multicomponent sex pheromones for mating, but the specific function and neural processing of each pheromone component remain unclear. The cockroach is a model for studying sex pheromone communication, and an adult female emits major and minor sex pheromone components, periplanone-B and -A (PB and PA), respectively. Attraction and courtship behaviors (wing-raising and abdominal extension) are strongly expressed when adult males are exposed to PB but weakly expressed when they are exposed to PA.

Critical roles of nicotinic acetylcholine receptors in olfactory memory formation and retrieval in crickets.

Acetylcholine (ACh) is a major excitatory neurotransmitter in the insect central nervous system, and insect neurons express several types of ACh receptors (AChRs). AChRs are classified into two subgroups, muscarinic AChRs and nicotinic AChRs (nAChRs). nAChRs are also divided into two subgroups by sensitivity to α-bungarotoxin (α-BGT).

Roles of octopamine neurons in the vertical lobe of the mushroom body for the execution of a conditioned response in cockroaches.

Aminergic neurons mediate reward signals in mammals and insects. In crickets, we showed that blockade of synaptic transmission from octopamine neurons (OANs) impairs conditioning of an odor (conditioned stimulus, CS) with water or sucrose (unconditioned stimulus, US) and execution of a conditioned response (CR) to the CS. It has not yet been established, however, whether findings in crickets can be applied to other species of insects.

acts with the transcription factor Creb to regulate long-term memory in crickets.

Novel genes have the potential to drive the evolution of new biological mechanisms, or to integrate into preexisting regulatory circuits and contribute to the regulation of older, conserved biological functions. One such gene, the novel insect-specific gene was first identified based on its role in establishing the germ line. We previously showed that this gene likely arose through an unusual domain transfer event involving bacterial endosymbionts and played a somatic role before evolving its well-known germ line function.

Octopamine neurons mediate reward signals in social learning in an insect.

Social learning is found in many animals, but its mechanisms are not understood. We previously showed that a cricket that was trained to observe a conspecific staying at a drinking apparatus exhibited an increased preference for the odor of that drinking apparatus. Here we investigated a hypothesis that this learning is achieved by second-order conditioning (SOC), i.

Spontaneous recovery from overexpectation in an insect.

In associative learning in mammals, it is widely accepted that learning is determined by the prediction error, i.e., the error between the actual reward and the reward predicted by the animal.

Conditioned taste aversion in the cricket Gryllus bimaculatus.

Conditioned taste aversion (CTA) is a form of classical conditioning in which animals associate the taste of a food with illness caused by toxin contained in the food. CTA in mammals is achieved with a long interval of up to several hours between food ingestion and illness induced by LiCl injection. Insects also exhibit CTA, but not much is known about its features.

Silencing the odorant receptor co-receptor impairs olfactory reception in a sensillum-specific manner in the cockroach.

Insects detect odors via a large variety of odorant receptors (ORs) expressed in olfactory sensory neurons (OSNs). The insect OR is a heteromeric complex composed of a ligand-specific receptor and the co-receptor (ORco). In this study, we identified the gene of the cockroach, (), and performed RNAi-based functional analysis of .

What Is Learned in Pavlovian Conditioning in Crickets? Revisiting the S-S and S-R Learning Theories.

In Pavlovian conditioning in mammals, two theories have been proposed for associations underlying conditioned responses (CRs). One theory, called S-S theory, assumes an association between a conditioned stimulus (CS) and internal representation of an unconditioned stimulus (US), allowing the animal to adjust the CR depending on the current value of the US. The other theory, called S-R theory, assumes an association or connection between the CS center and the CR center, allowing the CS to elicit the CR.

Reduction of contextual control of conditioned responses by extended Pavlovian training in an insect.

The effect of repetitive training on learned behavior has been an important subject in neuroscience. In instrumental conditioning in mammals, learned action early in training is often goal-driven and controlled by outcome expectancy, but as training progresses, it becomes more habitual and insensitive to outcome devaluation. Similarly, we recently showed in Pavlovian conditioning in crickets () that a conditioned response (CR) is initially sensitive to devaluation of the unconditioned stimulus but becomes insensitive to it after extended training.

Appetitive and aversive social learning with living and dead conspecifics in crickets.

Many animals acquire biologically important information from conspecifics. Social learning has been demonstrated in many animals, but there are few experimental paradigms that are suitable for detailed analysis of its associative processes. We established procedures for appetitive and aversive social learning with living and dead conspecifics in well-controlled stimulus arrangements in crickets, Gryllus bimaculatus.

Separate But Interactive Parallel Olfactory Processing Streams Governed by Different Types of GABAergic Feedback Neurons in the Mushroom Body of a Basal Insect.

The basic organization of the olfactory system has been the subject of extensive studies in vertebrates and invertebrates. In many animals, GABA-ergic neurons inhibit spike activities of higher-order olfactory neurons and help sparsening of their odor representations. In the cockroach, two different types of GABA-immunoreactive interneurons (calyceal giants [CGs]) mainly project to the base and lip regions of the calyces (input areas) of the mushroom body (MB), a second-order olfactory center.

Functional unification of sex pheromone-receptive glomeruli in the invasive Turkestan cockroach derived from the genus Periplaneta.

Female Periplaneta americana cockroaches emit two cooperatively working pheromone components, periplanone-B (PB) as a long-range attractant and periplanone-A (PA) as a short-range arrestant, and males develop enlarged glomeruli for processing them separately in the first-order olfactory center. Using intracellular recordings and neuronal labelings, we found that the Turkestan cockroach, Blatta lateralis, which is phylogenetically close to P. americana but having adapted to inground habitats, has an extraordinary large glomerulus.

Development of behavioural automaticity by extended Pavlovian training in an insect.

The effect of repetitive training on learned actions has been a major subject in behavioural neuroscience. Many studies of instrumental conditioning in mammals, including humans, suggested that learned actions early in training are goal-driven and controlled by outcome expectancy, but they become more automatic and insensitive to reduction in the value of the outcome after extended training. It was unknown, however, whether the development of value-insensitive behaviour also occurs by extended training of Pavlovian conditioning in any animals.

Tyrosine hydroxylase-immunoreactive neurons in the mushroom body of the field cricket, Gryllus bimaculatus.

The mushroom body of the insect brain participates in processing and integrating multimodal sensory information and in various forms of learning. In the field cricket, Gryllus bimaculatus, dopamine plays a crucial role in aversive memory formation. However, the morphologies of dopamine neurons projecting to the mushroom body and their potential target neurons, the Kenyon cells, have not been characterized.

Application of a Prediction Error Theory to Pavlovian Conditioning in an Insect.

Elucidation of the conditions in which associative learning occurs is a critical issue in neuroscience and comparative psychology. In Pavlovian conditioning in mammals, it is thought that the discrepancy, or error, between the actual reward and the predicted reward determines whether learning occurs. This theory stems from the finding of Kamin's blocking effect, in which after pairing of a stimulus with an unconditioned stimulus (US), conditioning of a second stimulus is blocked when the two stimuli are presented in compound and paired with the same US.

Signaling Pathways for Long-Term Memory Formation in the Cricket.

Unraveling the molecular mechanisms underlying memory formation in insects and a comparison with those of mammals will contribute to a further understanding of the evolution of higher-brain functions. As it is for mammals, insect memory can be divided into at least two distinct phases: protein-independent short-term memory and protein-dependent long-term memory (LTM). We have been investigating the signaling pathway of LTM formation by behavioral-pharmacological experiments using the cricket , whose olfactory learning and memory abilities are among the highest in insect species.

Spatial Receptive Fields for Odor Localization.

Animals rely on olfaction to navigate through complex olfactory landscapes, but the mechanisms that allow an animal to encode the spatial structure of an odorous environment remain unclear. To acquire information about the spatial distribution of an odorant, animals may rely on bilateral olfactory organs and compare side differences of odor intensity and timing [1-6] or may perform spatial and temporal signal integration of subsequent samplings [7]. The American cockroach can efficiently locate a source of sex pheromone even after the removal of one antenna, suggesting that bilateral comparison is not a prerequisite for odor localization in this species [8, 9].

Roles of Octopamine and Dopamine Neurons for Mediating Appetitive and Aversive Signals in Pavlovian Conditioning in Crickets.

Revealing neural systems that mediate appetite and aversive signals in associative learning is critical for understanding the brain mechanisms controlling adaptive behavior in animals. In mammals, it has been shown that some classes of dopamine neurons in the midbrain mediate prediction error signals that govern the learning process, whereas other classes of dopamine neurons control execution of learned actions. In this review, based on the results of our studies on Pavlovian conditioning in the cricket and by referring to the findings in honey bees and fruit-flies, we argue that comparable aminergic systems exist in the insect brain.

Calcium imaging method to visualize the spatial patterns of neural responses in the pygmy squid, Idiosepius paradoxus, central nervous system.

Background: Cephalopods exhibit unique behaviors such as camouflage and tactile learning. The brain functions correlated to these behaviors have long been analyzed through behavioral observations of animals subject to surgical manipulation or electrical stimulation of brain lobes. However, physiological methods have rarely been introduced to investigate the functions of each individual lobe, though physiological work on giant axons and slices of the vertical lobe system of the cephalopods have provided deep insights into ion conductance of nerves and long-term synaptic plasticity.

Roles of dopamine neurons in mediating the prediction error in aversive learning in insects.

In associative learning in mammals, it is widely accepted that the discrepancy, or error, between actual and predicted reward determines whether learning occurs. The prediction error theory has been proposed to account for the finding of a blocking phenomenon, in which pairing of a stimulus X with an unconditioned stimulus (US) could block subsequent association of a second stimulus Y to the US when the two stimuli were paired in compound with the same US. Evidence for this theory, however, has been imperfect since blocking can also be accounted for by competitive theories.

Two Parallel Olfactory Pathways for Processing General Odors in a Cockroach.

In animals, sensory processing via parallel pathways, including the olfactory system, is a common design. However, the mechanisms that parallel pathways use to encode highly complex and dynamic odor signals remain unclear. In the current study, we examined the anatomical and physiological features of parallel olfactory pathways in an evolutionally basal insect, the cockroach .