Circuits for integrating learned and innate valences in the insect brain

Abstract

Animal behavior is shaped both by evolution and by individual experience. Parallel brain pathways encode innate and learned valences of cues, but the way in which they are integrated during action-selection is not well understood. We used electron microscopy to comprehensively map with synaptic resolution all neurons downstream of all mushroom body (MB) output neurons (encoding learned valences) and characterized their patterns of interaction with lateral horn (LH) neurons (encoding innate valences) in Drosophila larva. The connectome revealed multiple convergence neuron types that receive convergent MB and LH inputs. A subset of these receives excitatory input from positive-valence MB and LH pathways and inhibitory input from negative-valence MB pathways. We confirmed functional connectivity from LH and MB pathways and behavioral roles of two of these neurons. These neurons encode integrated odor value and bidirectionally regulate turning. Based on this, we speculate that learning could potentially skew the balance of excitation and inhibition onto these neurons and thereby modulate turning. Together, our study provides insights into the circuits that integrate learned and innate valences to modify behavior.

Different dopaminergic neurons signal absolute and relative aversive value in the Drosophila mushroom body

“…Learning relative aversive value requires an interplay between aversively reinforcing PPL1 DANs modulating KC-MBON connections which provide feedforward and recurrent feedback input that determines the activity of specific subtypes of rewarding PAM DANs. These results support long-held 85,86 and recent [44][45][46]54,87,88 models in both vertebrates and invertebrates suggesting that learning requires critical interactions between appetitive and aversive reinforcement systems. In the fly, and likely also mammals, this process relies on opposing populations of DANs providing predictive signals needed to compare current with previous experience to assign (and update) both absolute and relative value to stimuli during learning.…”

“…Our experiments here suggest that a similar interplay between opposing populations of DANs, and plasticity at different MBON junctions in the MB network, permits computation of relative aversive value (or difference) between a previous and a new aversive experience. Combined with previous work 44,45,54,55,97 and current computational models 70,98 , our data provide key features of how a heterogeneous DAN system can "pre-compute" a relative value during learning 5 that facilitates future value-based decisions.…”

“…Some MBONs are synaptically interconnected, providing cross excitation or inhibition between MB compartments. Lastly, many MBONs make synapses outside the MB onto DAN dendrites in a feedback or feedforward manner 31,44,46,[52][53][54][55] . During olfactory associative learning, specific DANs provide punishment or reward signals to individual MB compartments, and the released dopamine depresses synaptic strengths between sparse odor-activated KCs and the MBONs whose dendrites reside within the relevant 4 compartments 50,52,[56][57][58][59][60][61][62][63] .…”

Bisected graph matching improves automated pairing of bilaterally homologous neurons from connectomes

“…To ensure we could evaluate the performance of both algorithms, we restricted our analysis to connec-tomes for which pairings of individual neurons between sides of the nervous system were already known. We studied the (chemical) connectomes of both a hermaphrodite and a male Caenorhabditis elegans worm [37], the pharynges of two Pristionchus pacificus worms [36], and a subset of a larval Drosophila melanogaster [8–28]. For all three datasets, neuron pairings across sides of the nervous system are not complete - indeed, some neurons appear only on one side of the organism or exactly in the center [37].…”

“…In other words, they have only considered the ipsilateral connections which connect within a brain hemisphere, and ignored the contralateral connections which cross brain hemispheres. Contralateral connections are quite common in connectomes studied thus far: in subset of the larval Drosophila melanogaster (vinegar fly) brain connectome published thus far, an edge picked at random from the network has about a 35% chance of being a contralateral connection [8–28]. It is natural to wonder, then, whether these connections can be used successfully to improve automated neuron pairing.…”