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Review
. 2022 Nov 10:16:1008818.
doi: 10.3389/fnbeh.2022.1008818. eCollection 2022.

Fear conditioning in invertebrates

Amy K Pribadi  1   2 , Sreekanth H Chalasani  1   2
Affiliations
Review

Fear conditioning in invertebrates

Amy K Pribadi et al. Front Behav Neurosci. .

Abstract

Learning to identify and predict threats is a basic skill that allows animals to avoid harm. Studies in invertebrates like Aplysia californica, Drosophila melanogaster, and Caenorhabditis elegans have revealed that the basic mechanisms of learning and memory are conserved. We will summarize these studies and highlight the common pathways and mechanisms in invertebrate fear-associated behavioral changes. Fear conditioning studies utilizing electric shock in Aplysia and Drosophila have demonstrated that serotonin or dopamine are typically involved in relaying aversive stimuli, leading to changes in intracellular calcium levels and increased presynaptic neurotransmitter release and short-term changes in behavior. Long-term changes in behavior typically require multiple, spaced trials, and involve changes in gene expression. C. elegans studies have demonstrated these basic aversive learning principles as well; however, fear conditioning has yet to be explicitly demonstrated in this model due to stimulus choice. Because predator-prey relationships can be used to study learned fear in a naturalistic context, this review also summarizes what is known about predator-induced behaviors in these three organisms, and their potential applications for future investigations into fear conditioning.

Keywords: A. californica; C. elegans; D. melanogaster; fear conditioning; invertebrates; learning; memory; predator-prey.

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Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

FIGURE 1
FIGURE 1
Associative conditioning schemes in Aplysia (top), Drosophila (middle), and Caenorhabditis elegans (bottom). Classical conditioning in Aplysia: training is performed by pairing electric shock with siphon touch. After training, siphon touch elicits the longer whole-body withdrawal response normally seen only with electric shock. Olfactory fear conditioning in Drosophila melanogaster: pairing electric shock with odor can alter olfactory preference. Aversive olfactory conditioning in C. elegans: pairing acid with odor results in avoidance of the paired odor.
FIGURE 2
FIGURE 2
Conserved molecules in associative learning, as identified in invertebrate models. An unconditioned stimulus, like electric shock, causes release of dopamine/serotonin. The presence of a conditioned stimulus causes postsynaptic calcium levels to rise through closing of K+ channels. High intracellular calcium results in increased release of neurotransmitter. Long-term behavioral changes can be effected through altered transcription via nuclear translocation of CREB.
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