Toward elucidating diversity of neural mechanisms underlying insect learning (original) (raw)
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BMC Biology, 2009
Background: In insect classical conditioning, octopamine (the invertebrate counterpart of noradrenaline) or dopamine has been suggested to mediate reinforcing properties of appetitive or aversive unconditioned stimulus, respectively. However, the roles of octopaminergic and dopaminergic neurons in memory recall have remained unclear. Results: We studied the roles of octopaminergic and dopaminergic neurons in appetitive and aversive memory recall in olfactory and visual conditioning in crickets. We found that pharmacological blockade of octopamine and dopamine receptors impaired aversive memory recall and appetitive memory recall, respectively, thereby suggesting that activation of octopaminergic and dopaminergic neurons and the resulting release of octopamine and dopamine are needed for appetitive and aversive memory recall, respectively. On the basis of this finding, we propose a new model in which it is assumed that two types of synaptic connections are formed by conditioning and are activated during memory recall, one type being connections from neurons representing conditioned stimulus to neurons inducing conditioned response and the other being connections from neurons representing conditioned stimulus to octopaminergic or dopaminergic neurons representing appetitive or aversive unconditioned stimulus, respectively. The former is called 'stimulus-response connection' and the latter is called 'stimulus-stimulus connection' by theorists studying classical conditioning in higher vertebrates. Our model predicts that pharmacological blockade of octopamine or dopamine receptors during the first stage of second-order conditioning does not impair second-order conditioning, because it impairs the formation of the stimulusresponse connection but not the stimulus-stimulus connection. The results of our study with a cross-modal second-order conditioning were in full accordance with this prediction. Conclusion: We suggest that insect classical conditioning involves the formation of two kinds of memory traces, which match to stimulus-stimulus connection and stimulus-response connection. This is the first study to suggest that classical conditioning in insects involves, as does classical conditioning in higher vertebrates, the formation of stimulus-stimulus connection and its activation for memory recall, which are often called cognitive processes.
Roles of aminergic neurons in formation and recall of associative memory in crickets
Frontiers in behavioral neuroscience, 2010
We review recent progress in the study of roles of octopaminergic (OA-ergic) and dopaminergic (DA-ergic) signaling in insect classical conditioning, focusing on our studies on crickets. Studies on olfactory learning in honey bees and fruit-flies have suggested that OA-ergic and DA-ergic neurons convey reinforcing signals of appetitive unconditioned stimulus (US) and aversive US, respectively. Our work suggested that this is applicable to olfactory, visual pattern, and color learning in crickets, indicating that this feature is ubiquitous in learning of various sensory stimuli. We also showed that aversive memory decayed much faster than did appetitive memory, and we proposed that this feature is common in insects and humans. Our study also suggested that activation of OA- or DA-ergic neurons is needed for appetitive or aversive memory recall, respectively. To account for this finding, we proposed a model in which it is assumed that two types of synaptic connections are strengthened ...
Scientific reports, 2015
Elucidation of reinforcement mechanisms in associative learning is an important subject in neuroscience. In mammals, dopamine neurons are thought to play critical roles in mediating both appetitive and aversive reinforcement. Our pharmacological studies suggested that octopamine and dopamine neurons mediate reward and punishment, respectively, in crickets, but recent studies in fruit-flies concluded that dopamine neurons mediates both reward and punishment, via the type 1 dopamine receptor Dop1. To resolve the discrepancy between studies in different insect species, we produced Dop1 knockout crickets using the CRISPR/Cas9 system and found that they are defective in aversive learning with sodium chloride punishment but not appetitive learning with water or sucrose reward. The results suggest that dopamine and octopamine neurons mediate aversive and appetitive reinforcement, respectively, in crickets. We suggest unexpected diversity in neurotransmitters mediating appetitive reinforcem...
Frontiers in behavioral neuroscience, 2015
Elucidation of reinforcing mechanisms for associative learning is an important subject in neuroscience. Based on results of our previous pharmacological studies in crickets, we suggested that octopamine and dopamine mediate reward and punishment signals, respectively, in associative learning. In fruit-flies, however, it was concluded that dopamine mediates both appetitive and aversive reinforcement, which differs from our suggestion in crickets. In our previous studies, the effect of conditioning was tested at 30 min after training or later, due to limitations of our experimental procedures, and thus the possibility that octopamine and dopamine were not needed for initial acquisition of learning was not ruled out. In this study we first established a conditioning procedure to enable us to evaluate acquisition performance in crickets. Crickets extended their maxillary palpi and vigorously swung them when they perceived some odors, and we found that crickets that received pairing of a...
Roles of dopamine neurons in mediating the prediction error in aversive learning in insects
Scientific Reports, 2017
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. We recently reported blocking in classical conditioning of an odor with water reward in crickets. We also reported an "autoblocking" phenomenon in appetitive learning, which supported the prediction error theory and rejected alternative theories. The presence of auto-blocking also suggested that octopamine neurons mediate reward prediction error signals. Here we show that blocking and auto-blocking occur in aversive learning to associate an odor with salt water (US) in crickets, and our results suggest that dopamine neurons mediate aversive prediction error signals. We conclude that the prediction error theory is applicable to both appetitive learning and aversive learning in insects. Associative learning allows animals to adapt to various environments by acquiring knowledge on events in their environments. Based on the knowledge, animals find suitable food, avoid toxic food and escape from predators. Thus, both appetitive learning and aversive learning are essential for survival of animals. Many efforts have been made to elucidate learning rules governing associative learning in mammals 1,2 , but whether appetitive learning and aversive learning are ruled by the same general principles remains unclear. In associative learning in mammals, it is widely accepted that the discrepancy, or error, between the actual unconditioned stimulus (US) and predicted US determines whether learning occurs when a stimulus is paired with the US 1,2. This theory stems from the finding of a "blocking" phenomenon by Kamin 3. He observed in rats that a stimulus X that had been paired previously with a 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 (XY + training, see Table 1). Kamin 3 argued that no learning of stimulus Y occurs since the US was fully predicted by stimulus X and argued that surprise is needed for learning. This proposition was formulated into the prediction error theory by Rescorla and Wagner 4 , and subsequent electrophysiological studies suggested that dopamine (DA) neurons in the midbrain convey reward prediction error signals 1. Evidence for the prediction error theory, however, has been imperfect since blocking can also be accounted for by theories other than the prediction error theory such as attentional theory and retrieval theory 5-7 , which account for blocking by competition between X and Y stimuli, and evidence to convincingly refute alternative theories has been lacking 8-10. We previously reported blocking in appetitive associative learning in crickets 11. Moreover, we obtained evidence that octopamine (OA) neurons play critical roles in appetitive learning in crickets 12-19 , and we demonstrated that when a stimulus X was paired with water (appetitive US) under the condition of administration of an OA receptor antagonist, in which no learning of X occurs, subsequent learning of X was blocked in training to associate the stimulus X with the US given after recovery from the effect of the antagonist 11. This "auto-blocking" can be accounted for by the prediction error theory since if blockade of OA-ergic transmission impairs learning but not formation of the prediction of the US by stimulus X, no learning of stimulus X should occur in subsequent training. This "auto-blocking" phenomenon cannot be accounted for by any of the competitive theories
Pharmacology Biochemistry and Behavior, 1992
We followed the titer of free amino acids in nervous ganglia and hemolimph of the cricket Pteronemobius sp. at different times during and after a shock avoidance training that included one experimental group and three controls. The results showed that Tau, urea, Thr, His, GABA, and an unidentified compound (Q) increased their titer in ganglia and hemolimph during training, whereas Ala, Arg, Val, Glu, Ser, and one or all of the group formed by Cys, Phe, Ile, Leu, and Trp decreased theirs concomitantly to memory consolidation. The difference in the rate of experimental insects and their yoked slaves to consolidate the learned task was reflected in the changes of the titers of the amino acids mentioned above. The data add to the evidence for a direct involvement of these amino acids in modulating the memory consolidation process. Amino acids Insects Memory consolidation Long-term memory Memory Crickets Neuromodulation Aversive conditioning Learning Amino acid changes
Learning and Memory in Honeybees: From Behavior to Neural Substrates
Annual Review of Neuroscience, 1996
Learning and memory in honeybees is analyzed on five levels, using a top-down approach, (a) Observatory learning is applied during navigation and dance communication. (b) Local cues at the feeding site are learned associatively. (c) Classical conditioning of the proboscis extension response to olfactory stimuli provides insight into behavioral, neural, and neuropharmacological mechanisms of associative learning, (d) At the neural level, the pathways coding the conditioned and the unconditioned stimulus are identified. The reinforcing function of the unconditioned stimulus is traced to a particular neuron, (e) At the cellular level, the cAMP pathway is found to be critically involved. Nitric oxide is an essential mediator for the transfer from short-to long-term memory.
Neuroscience Research, 2007
Associative strength between conditioned stimulus (CS) and unconditioned stimulus (US) is thought to determine learning efficacy in classical conditioning. Elucidation of the neuronal mechanism that underlies the association between CS and US in the brain is thus critical to understand the principle of memory formation. With a simple brain organization, the Drosophila larva provides an attractive model system to investigate learning at the neurocircuitry level. Previously, we described a single-odor paradigm for larval associative learning using sucrose as a reward, and showed that larval appetitive memory lasts longer than 2 h. In this work, we describe behavioral and genetic characterization of larval aversive olfactory memory formed in our paradigm, and compare its stability and neurocircuitry with those of appetitive memory. Despite identical training paradigms, larval olfactory memory formed with quinine or NaCl is shortlived to be lost in 20 min. As with appetitive memory, larval aversive memory produced in this paradigm depends on intact cAMP signaling, but neither mutation of amnesiac nor suppression of CREB activity affects its kinetics. Neurocircuitry analyses suggest that aversive memory is stored before the presynaptic termini of the larval mushroom body neurons as is the case with appetitive memory. However, synaptic output of octopaminergic and dopaminergic neurons, which exhibit distinctive innervation patterns on the larval mushroom body and antennal lobe, is differentially required for the acquisition of appetitive and aversive memory, respectively. These results as a whole suggest that the genetically programmed memory circuitries might provide predisposition in the efficacy of inducing longer-lived memory components in associative learning.