Memory block: A consequence of conflict resolution

Ito, Etsuro; Yamagishi, Miki; Hatakeyama, Dai; Watanabe, Takayuki; Fujito, Yutaka; Dyakonova, Varvara; Lukowiak, Ken

doi:10.1242/jeb.120329

Cited by 30 publications

(35 citation statements)

References 37 publications

(41 reference statements)

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“…Feeding suppressed appetitive memory, as it was shown by studies in Drosophila (29), but more interesting was that expression of aversive memory was enhanced in satiated crabs. This result is consistent with recent findings in crayfish showing that feeding modulates risk avoidance behaviors (36) and with studies in Lymnaea showing that hungry animals suppress the expression of taste aversion memory (37). We interpret the results in crabs as the consequence of an evaluation that the animal does in relation to costs, benefits and risks that it is willing to take.…”

Section: Mutual Interference Between Appetitive and Aversive Memoriessupporting

confidence: 92%

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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Section: Mutual Interference Between Appetitive and Aversive Memoriessupporting

confidence: 92%

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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“…That is, there is a conflict between the CTA memory and the desire/necessity to eat. As described in an earlier report (Ito et al, 2015b), the ‘necessity knows no law’ concept prevails in these snails. That is, snails do not express the memory phenotype if they are extremely hungry (for example, Day 5 snails), i.e.…”

Section: Discussionmentioning

confidence: 70%

“…This could be shown because the memory is context-dependent (Haney and Lukowiak, 2001; Lukowiak et al, 2007) and can only be observed when the snails are in a context similar to that in which the training occurred. Thus, if the Day 5 snails are fed after they received the training, the memory phenotype can be expressed (Ito et al, 2015b). Recently, dopamine was also shown to be involved in positive emotion states, even in invertebrates (Perry et al, 2016).…”

Section: Discussionmentioning

confidence: 99%

Relationship between the grades of a learned aversive-feeding response and the dopamine contents inLymnaea

et al. 2016

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The pond snail Lymnaea learns conditioned taste aversion (CTA) and remembers not to respond to food substances that initially cause a feeding response. The possible relationship between how well snails learn to follow taste-aversion training and brain dopamine contents is not known. We examined this relationship and found the following: first, snails in the act of eating just before the commencement of CTA training were poor learners and had the highest dopamine contents in the brain; second, snails which had an ad libitum access to food, but were not eating just before training, were average learners and had lower dopamine contents; third, snails food-deprived for one day before training were the best learners and had significantly lower contents of dopamine compared to the previous two cohorts. There was a negative correlation between the CTA grades and the brain dopamine contents in these three cohorts. Fourth, snails food-deprived for five days before training were poor learners and had higher dopamine contents. Thus, severe hunger increased the dopamine content in the brain. Because dopamine functions as a reward transmitter, CTA in the severely deprived snails (i.e. the fourth cohort) was thought to be mitigated by a high dopamine content.

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“…It should be noted that the Yerkes and Dodson (1908) paper did not present such an inverted-U curve. The inverted-U function is actually a figure adapted from Donald Hebb's 1955 presidential address to the American Psychological Association (Hebb, 1955; see also Diamond et al, 2007;Ito et al, 2015a;Kojima et al, 2015). It appears that Hebb was unaware of the earlier Yerkes and Dodson paper (Diamond et al, 2007).…”

Section: Discussionmentioning

confidence: 99%

A flavanoid component of chocolate quickly reverses an imposed memory deficit

Knezevic

Komatsuzaki

Freitas

et al. 2016

Journal of Experimental Biology

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The ability to remember is influenced by environmental and lifestyle factors, such as stress and diet. A flavanol contained in chocolate, epicatechin (Epi), has been shown to enhance long-term memory (LTM) formation in Lymnaea. Combining two stressors (low-calcium pond water and crowding) blocks learning and all forms of memory; that is, this combination of environmentally relevant stressors creates a memory-unfriendly state. We tested the hypothesis that Epi will immediately reverse the memory-unfriendly state, i.e. that snails in the memory-deficit state when trained in Epi will immediately become competent to learn and form memory. We found that Epi not only reverses the memory-deficit state but also further enhances LTM formation. Thus, a naturally occurring bioactive plant compound can overcome a memory-unfriendly state. This supports the idea that bioactive substances may mitigate memory-making deficits that, for example, occur with ageing.

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Memory block: A consequence of conflict resolution

Cited by 30 publications

References 37 publications

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

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

Relationship between the grades of a learned aversive-feeding response and the dopamine contents inLymnaea

A flavanoid component of chocolate quickly reverses an imposed memory deficit

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