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

Abstract

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 ...

Proactive and retroactive interference with associative memory consolidation in the snail Lymnaea is time and circuit dependent

“…When the interference is due to another type of associative learning that is fundamentally different in nature from the first one, both memories are capable of consolidating in parallel. In Neohelice crabs, an appetitive and aversive paradigm utilized in a single training session induces separate appetitive and aversive memories that compete during retrieval but not during acquisition 36 . The results indicated that both memories consolidated in parallel, similar to our results using consecutive appetitive and aversive training during a non-lapse period.…”

Aversive Training of Honey Bees in an Automated Y-Maze

“…Animals have to make choices between different environments to escape dangers in many situations, and learn about which environments are dangerous based on previous experience. Choice behaviors can be exploited to study the mechanisms of sensory coding, learning and memory, and decision making (Guerrieri et al, 2005; Hadar and Menzel, 2010; Devaud et al, 2015; Klappenbach et al, 2017). Recent technological developments allow for increasingly automated systems (e.g., Yang et al, 2011; Itskov et al, 2014; Alisch et al, 2018), affording for large-scale screening and standardized conditions.…”

“…For example, we could see how trained honeybees would react to ambiguous or contradictory compounds. The mushroom bodies are thought to be responsible for the formation of both appetitive and aversive memory, and studies in Drosophila indicate that these two circuits are mostly independent, and act by shifting the balance of common output neurons (Klappenbach et al, 2017; Cognigni et al, 2018). It would be interesting to verify if multi-sensory stimuli are similarly compartmentalized such that the different elements are only integrated at a late stage in the circuitry.…”

Food-derived volatiles enhance consumption inDrosophila melanogaster

“…(e.g. Klappenbach et al, 2017;Lewis et al, 2015). In particular, natural food sources are mixtures that might contain substances which are not appetitive by themselves, including bitter compounds, such as alkaloids in nectar from some flowers (Adler, 2000) and glucosinolates in Brassica (Cartea and Velasco, 2008).…”