Brain Modularity in Arthropods: Individual Neurons That Support “What” But Not “Where” Memories

Sztarker, Julieta; Tomsic, Daniel

doi:10.1523/jneurosci.6029-10.2011

Cited by 40 publications

(38 citation statements)

References 32 publications

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“…Despite clear evidence that some forms of habituation are context specific and therefore associative (Shalter, 1978;Tomsic et al, 1998;Rose and Rankin, 2001;Sztarker and Tomsic, 2011) (present study), most textbooks still classify habituation as a simple, nonassociative form of learning (Kandel et al, 2000;Bear et al, 2007;Bouton, 2007). This classification has been unaltered since the earliest studies on habituation, even though there are, as far as we know, no studies providing clear evidence to this effect.…”

Section: The Classification Of Habituationmentioning

confidence: 59%

“…Thus, the response decline to the habituation dummy could not be a result of retinotopic habituation. Similarly, in the laboratory the brachyuran crab Chasmagnathus granulatus can recognize a learned stimulus independently of its retinal position (Sztarker and Tomsic, 2011). Because the crabs in the present study constantly change orientation, they would not have been able to reference the dummy with respect to their own body direction, but as an absolute compass direction.…”

Section: Stimulus Identification Under Natural Conditionsmentioning

confidence: 77%

“…In a field study on pied flycatchers, the initial mobbing response strength was evoked by changing the location of a model predator, to which the birds had habituated (Shalter, 1978). Furthermore, habituation has clearly been shown to be context specific in laboratory studies using the worm Caenorhabditis elegans (Rose and Rankin, 2001) as well as in C. granulatus (Tomsic et al, 1998;Sztarker and Tomsic, 2011). These studies suggest that habituation can be facilitated by associative processes.…”

Section: Is Habituation Associative?mentioning

confidence: 96%

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Habituation under natural conditions: model predators are distinguished by approach direction

Raderschall

Magrath

Hemmi

2011

Journal of Experimental Biology

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SUMMARYHabituation is an active process that allows animals to learn to identify repeated, harmless events, and so could help individuals deal with the trade-off between reducing the risk of predation and minimizing escape costs. Safe habituation requires an accurate distinction between dangerous and harmless events, but in natural environments such an assessment is challenging because sensory information is often noisy and limited. What, then, comprises the information animals use to recognize objects that they have previously learned to be harmless? We tested whether the fiddler crab Uca vomeris distinguishes objects purely by their sensory signature or whether identification also involves more complex attributes such as the direction from which an object approaches. We found that crabs habituated their escape responses after repeated presentations of a dummy predator consistently approaching from the same compass direction. Females habituated both movement towards the burrow and descent into the burrow, whereas males only habituated descent into the burrow. The crabs were more likely to respond again when a physically identical dummy approached them from a new compass direction. The crabs distinguished between the two dummies even though both dummies were visible for the entire duration of the experiment and there was no difference in the timing of the dummiesʼ movements. Thus, the position or approach direction of a dummy encodes important information that allows animals to identify an event and habituate to it. These results argue against the traditional notion that habituation is a simple, nonassociative learning process, and instead suggest that habituation is very selective and uses information to distinguish between objects that is not available from the sensory signature of the object itself.

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Section: The Classification Of Habituationmentioning

confidence: 59%

Section: Stimulus Identification Under Natural Conditionsmentioning

confidence: 77%

Section: Is Habituation Associative?mentioning

confidence: 96%

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Habituation under natural conditions: model predators are distinguished by approach direction

Raderschall

Magrath

Hemmi

2011

Journal of Experimental Biology

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“…The brain areas and circuits involved in contextual aversive memory in crabs have just recently started to be elucidated (27,33). Areas in the crab brain that are structurally homologous to the mushroom bodies of insects receive dopaminergic innervations and undergo plasticity related with the contextual aversive memory (7).…”

Section: Mutual Interference Between Appetitive and Aversive Memoriesmentioning

confidence: 99%

Parallel memory traces are built after an experience containing aversive and appetitive components in the crab Neohelice

Klappenbach

Nally

Locatelli

2017

Proc. Natl. Acad. Sci. U.S.A.

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The neurobiology of learning and memory has been mainly studied by focusing on pure aversive or appetitive experiences. Here, we challenged this approach considering that real-life stimuli come normally associated with competing aversive and appetitive consequences and that interaction between conflicting information must be intrinsic part of the memory processes. We used Neohelice crabs, taking advantage of two well-described appetitive and aversive learning paradigms and combining them in a single training session to evaluate how this affects memory. We found that crabs build separate appetitive and aversive memories that compete during retrieval but not during acquisition. Which memory prevails depends on the balance between the strength of the unconditioned stimuli and on the motivational state of the animals. The results indicate that after a mix experience with appetitive and aversive consequences, parallel memories are established in a way that appetitive and aversive information is stored to be retrieved in an opportunistic manner.long-term memory | consolidation | retrieval | appetitive | aversive I n the wild, it is crucial for animals to learn and remember which places represent a danger and which ones are associated with appetitive rewards such as food, shelter, or mate. Understanding how these associations are acquired, retained, and retrieved are major goals in neurobiology. A successful strategy suited to laboratory conditions has been simplifying learning episodes to appetitive or aversive experiences, because in those ideal cases, learning and memory can be unequivocally measured as attraction or avoidance. The present study is framed on the view that those pure appetitive or aversive experiences do not fully represent real-life situations. In nature, animals are exposed to stimuli that predict positive and negative consequences at the same time, and the conflicting information must be weighed and organized to allow expression of the most beneficial behavior. Invertebrates are convenient models to study the interaction between appetitive and aversive memory processes because neurochemical pathways and circuits involved in both types of memory have begun to be elucidated (1-5). The hypothesis that appetitive and aversive information interact during memory processes gets support from pharmacological studies in crabs (6, 7) and bees (8,9), which show that the neurotransmitter necessary for appetitive memory formation does, in turn, impair aversive memory, whereas the transmitter necessary for aversive memory impairs appetitive memory. In addition, studies in Drosophila, in which memory mechanisms can be dissected at the neuron level, provide evidence that the interaction between appetitive and aversive information occurs from the circuits that encode reward and punishment to circuits that regulate memory expression (10)(11)(12)(13)(14).In contrast to the knowledge about the interaction at the circuit level, the description about the consequence of competing experiences in regards to the content of ...

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“…Electrophysiological techniques have been applied to the study of learning mechanisms in some invertebrates [39][40][41][42][43][44][45][46][47]. However, neurophysiological mechanisms responsible for their brain functions remain to be clarified at the level of identifiable nerve cells in the future chiefly because of experimental difficulties in recording their activities from freely behaving animals.…”

Section: Introductionmentioning

confidence: 99%

Discrimination learning with light stimuli in restrained American lobster

Tomina

Takahata

2012

Behavioural Brain Research

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Operant discrimination learning has been extensively utilized in the study on the perceptual ability of animals and their higher-order brain functions. We tested in this study whether American lobster Homarus americanus, which was previously found to possess ability of operant learning with claw gripping, could be trained to discriminate light stimuli of different intensities. For the current purpose, we newly developed a PC-controlled operant chamber that allowed the animal under a body-fixed condition to perform operant reward learning with claw gripping. Lobsters were first reinforced when they gripped the sensor bar upon presentation of a light cue. Then they were trained to grip the bar only when the light stimulus of a specific intensity was presented to obtain food reward while the stimuli of three different intensities including the reinforced one were presented in a random order. Finally, they were re-trained to grip the bar only when the light stimulus of another intensity that was not rewarded in the preceding training to obtain food while other intensities including the one that was rewarded previously were not rewarded any more. In these training procedures, the operant behavior occurred more frequently in response to the rewarded cue than to the non-rewarded one. The action latency for the reinforced stimuli showed a significant decrease in the course of training.These data demonstrate that lobsters can be trained with the light cues of different intensity as discriminative stimuli under a restrained condition that would allow application of electrophysiological techniques to the behaving subjects.-3-

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Brain Modularity in Arthropods: Individual Neurons That Support “What” But Not “Where” Memories

Cited by 40 publications

References 32 publications

Habituation under natural conditions: model predators are distinguished by approach direction

Habituation under natural conditions: model predators are distinguished by approach direction

Parallel memory traces are built after an experience containing aversive and appetitive components in the crab Neohelice

Discrimination learning with light stimuli in restrained American lobster

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