Dissociation between sensitization and learning-related neuromodulation in an aplysiid species

Abstract

Mosquitoes can learn to change their host-feeding behaviors, such as shifting activity times to avoid bednets or switching from biting animals to biting humans, leading to the transfer of zoonotic diseases. Dopamine is critical for insect learning, but its role in the antennal lobe remains unclear, and it is unknown whether different mosquito species learn the same odor cues. We assayed aversive olfactory learning and dopaminergic brain innervation in four mosquito species with different host preferences and report here that they differentially learn odors salient to their preferred host and innervation patterns vary across species. Using genetically-encoded GCaMP6s Aedes aegypti, we mapped odor-evoked antennal lobe activity and report that glomeruli tuned to "learnable" odors have significantly higher dopaminergic innervation. Changes in dopamine expression in the antennal lobes of diverse invertebrate species may be an evolutionary mechanism to adapt olfactory learning circuitry without changing brain structure and for mosquitoes an ability to adapt to other hosts when their preferred are no longer present.

Neural mechanisms underlying the evolvability of behaviour

“…In the stomatogastric nervous systems of crustaceans, there are species differences in the presence of neurotransmitters and in the effects of neuromodulatory substances [99][100][101]. In aplysiid molluscs, the effect of serotonin on sensory neuron excitability and synaptic strength varies in a phylogenetic manner and may underlie species differences in behavioural sensitization [102][103][104]. Species differences in neuromodulatory actions also underlie differences in the swimming behaviours of frog embryos [105,106].…”

Evolution of Learning in Three Aplysiid Species: Differences in Heterosynaptic Plasticity Contrast with Conservation in Serotonergic Pathways

“…1999). Furthermore, these species can adapt their behaviour to their past experience through simple forms of learning such as sensitization, a generalized increase in responsiveness after a novel or noxious stimulus (Wright, 1998; Erixon et al . 1999).…”

mtDNA Ribosomal Gene Phylogeny of Sea Hares in the Genus Aplysia (Gastropoda, Opisthobranchia, Anaspidea): Implications for Comparative Neurobiology

“…The neural circuit for these two re exes is known to involve >100 neurons in the abdominal ganglion (Frost and Kandel, 1995). Most of the studies have been performed on A. californica, although recent studies have been published that compare different species and different genera (Wright et al, 1996;Wright, 1998;Kurokawa et al, 1998;Erixon et al, 1999). Kurokawa et al (1998) studied siphon and gill withdrawal in three species (A. californica, A kurodai, and A. juliana), two from the subgenus Varria and one from the subgenus Aplysia, respectively.…”

“…Wright et al (1996) utilized a morphology-based phylogeny of the Anaspidea to demonstrate that the genus Dolabrifera has lost two well-studied neuromodulatory learning mechanisms: serotonin-induced increase in spike duration, and excitability of tail sensory neurons. On the basis of molecular evidence suggesting that Dolabrifera and Phyllaplysia are sister taxa (Medina, 1998;Medina and Walsh, 2000), Erixon et al (1999) tested several evolutionary hypotheses at both cellular and behavioral levels. In Aplysia, the presence of both neuromodulatory traits is associated with the presence of the sensitization phenotype.…”

“…This correlation between neural and behavioral phenotypes appears to break down in Phyllaplysia, however, which shows the neuromodulatory traits but no sensitization. Erixon et al (1999) concluded that at the neuromodulatory level Phyllaplysia resembles ancestral sea hares (i.e., Aplysia), whereas at the behavioral level they resemble their sister taxon Dolabrifera. These studies addressed evolution at the level of families within the order.…”