Models of heterogeneous dopamine signaling in an insect learning and memory center

The Drosophila mushroom body exhibits dopamine dependent synaptic plasticity that underlies the acquisition of associative memories. Recordings of dopamine neurons in this system have identified signals related to external reinforcement such as reward and punishment. However, other factors including locomotion, novelty, reward expectation, and internal state have also recently been shown to modulate dopamine neurons. This heterogeneity is at odds with typical modeling approaches in which these neurons are assumed to encode a global, scalar error signal. How is dopamine dependent plasticity coordinated in the presence of such heterogeneity? We develop a modeling approach that infers a pattern of dopamine activity sufficient to solve defined behavioral tasks, given architectural constraints informed by knowledge of mushroom body circuitry. Model dopamine neurons exhibit diverse tuning to task parameters while nonetheless producing coherent learned behaviors. Notably, reward prediction error emerges as a mode of population activity distributed across these neurons. Our results provide a mechanistic framework that accounts for the heterogeneity of dopamine activity during learning and behavior.

Neuromodulation and Differential Learning Across Mosquito Species

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.

Models of heterogeneous dopamine signaling in an insect learning and memory center

The Drosophila mushroom body exhibits dopamine dependent synaptic plasticity that underlies the acquisition of associative memories. Recordings of dopamine neurons in this system have identified signals related to external reinforcement such as reward and punishment. However, other factors including locomotion, novelty, reward expectation, and internal state have also recently been shown to modulate dopamine neurons. This heterogeneity is at odds with typical modeling approaches in which these neurons are assumed to encode a global, scalar error signal. How is dopamine dependent plasticity coordinated in the presence of such heterogeneity? We develop a modeling approach that infers a pattern of dopamine activity sufficient to solve defined behavioral tasks, given architectural constraints informed by knowledge of mushroom body circuitry. Model dopamine neurons exhibit diverse tuning to task parameters while nonetheless producing coherent learned behaviors. Our results provide a mechanistic framework that accounts for the heterogeneity of dopamine activity during learning and behavior.

Considerations for Insect Learning in Integrated Pest Management

The past 100 yr have seen dramatic philosophical shifts in our approach to controlling or managing pest species. The introduction of integrated pest management in the 1970s resulted in the incorporation of biological and behavioral approaches to preserve ecosystems and reduce reliance on synthetic chemical pesticides. Increased understanding of the local ecosystem, including its structure and the biology of its species, can improve efficacy of integrated pest management strategies. Pest management strategies incorporating insect learning paradigms to control insect pests or to use insects to control other pests can mediate risk to nontarget insects, including pollinators. Although our understanding of insect learning is in its early stages, efforts to integrate insect learning into pest management strategies have been promising. Due to considerable differences in cognitive abilities among insect species, a case-by-case assessment is needed for each potential application of insect learning within a pest management strategy.

What Associative Learning in Insects Tells Us about the Evolution of Learned and Fixed Behavior

Contemporary models for the evolution of learning suggest that environmental predictability plays a critical role in whether learning is expected to evolve in a particular species, a claim originally made over 50 years ago. However, amongst many behavioral scientists who study insect learning, as well as amongst neuroscientists who study the brain architecture of insects, a very different view is emerging, namely that all animals possessing a nervous system should be able to learn. More specifically, the capacity for associative learning may be an emergent property of nervous systems such that, whenever selection pressures favor the evolution of nervous systems, for whatever reason, the capacity for associative learning follows ipso facto. One way to reconcile these disparate views of learning is to suggest that the assumed default in these evolutionary models, namely the non-learning phenotype, is incorrect: The ability to learn is, in fact, the default but, under certain conditions, selection pressures can override that ability, resulting in hard-wired, or considerably less plastic, responses. Thus, models for the evolution of learning actually may be models for the conditions under which inherent plasticity is overridden. Moreover, what have been revealed as the costs of learning in insects may, instead, be costs associated with far more complex cognitive feats than simple associative learning – cognitive skills that researchers are just now beginning to reveal.

Olfactory conditioning in mate searching by the parasitoidAphidius ervi(Hymenoptera: Braconidae)

Despite the fact that insect learning capacity has been broadly demonstrated, the role that this process plays during mate searching has been scarcely explored. We studied whether the sexual behaviour of a male parasitic wasp can be conditioned to the odours from two alternative host plant complexes (HPCs) present during its first copulation. The experimental subjects were newly emerged males of the aphid parasitoid,Aphidius ervi, and two alternative HPCs (alfalfa or wheat). In the training protocol, copulation experience corresponded to an unconditioning stimulus and HPC odours to the conditioning stimuli. The initial (just after eclosion) and trained responses were assessed in a glass Y-olfactometer. The results showed that neither alfalfa HPC nor wheat HPC stimuli elicited sexual-related behaviours in initial male responses. Conversely, both HPCs triggered strong attraction and wing fanning courtship behaviour in trained responses when the male was exposed to a female plus HPC during training. In males trained with females plus a given HPC but tested with the alternative HPC in the olfactometer, trained response showed a similar trend to the non-associative treatments. Hence, through learning, the olfactory stimulus context present during copulation could become a predictive cue for further mate searching. These results are discussed in terms of parasitic wasp ecology and host fidelity.