We identified the neurons comprising the Drosophila mushroom body (MB), an associative center in invertebrate brains, and provide a comprehensive map describing their potential connections. Each of the 21 MB output neuron (MBON) types elaborates segregated dendritic arbors along the parallel axons of ∼2000 Kenyon cells, forming 15 compartments that collectively tile the MB lobes. MBON axons project to five discrete neuropils outside of the MB and three MBON types form a feedforward network in the lobes. Each of the 20 dopaminergic neuron (DAN) types projects axons to one, or at most two, of the MBON compartments. Convergence of DAN axons on compartmentalized Kenyon cell-MBON synapses creates a highly ordered unit that can support learning to impose valence on sensory representations. The elucidation of the complement of neurons of the MB provides a comprehensive anatomical substrate from which one can infer a functional logic of associative olfactory learning and memory.

/pdf/the-neuronal-architecture-of-the-mushroom-body-provides-a-4jan707nqc.pdf

The neuronal architecture of the mushroom body provides a logic for associative learning

Food can be hazardous, either through toxicity or through bacterial infections that follow the ingestion of a tainted food source. Because learning about food quality enhances survival, one of the most robust forms of olfactory learning is conditioned avoidance of tastes associated with visceral malaise. The nematode Caenorhabditis elegans feeds on bacteria but is susceptible to infection by pathogenic bacteria in its natural environment. Here we show that C. elegans modifies its olfactory preferences after exposure to pathogenic bacteria, avoiding odours from the pathogen and increasing its attraction to odours from familiar nonpathogenic bacteria. Particular bacteria elicit specific changes in olfactory preferences that are suggestive of associative learning. Exposure to pathogenic bacteria increases serotonin in ADF chemosensory neurons by transcriptional and post-transcriptional mechanisms. Serotonin functions through MOD-1, a serotonin-gated chloride channel expressed in sensory interneurons, to promote aversive learning. An increase in serotonin may represent the negative reinforcing stimulus in pathogenic infection.

/pdf/pathogenic-bacteria-induce-aversive-olfactory-learning-in-10vdu1r0dd.pdf

Pathogenic bacteria induce aversive olfactory learning in Caenorhabditis elegans

Light-induced activation of distinct modulatory neurons triggers appetitive or aversive learning in Drosophila larvae.

Octopamine (OA) and tyramine (TA) are the invertebrate counterparts of the vertebrate adrenergic transmitters They are decarboxylation products of the amino acid tyrosine, with TA as the biological precursor of OA Nevertheless, both compounds are independent neurotransmitters that act through G protein-coupled receptors OA modulates a plethora of behaviors and peripheral and sense organs, enabling the insect to respond correctly to external stimuli Because these two phenolamines are the only biogenic amines whose physiological significance is presumably restricted to invertebrates, pharmacologists have focused their attention on the corresponding receptors, which are still believed to represent promising targets for new insecticides Recent progress made on all levels of OA and TA research has enabled researchers to understand better the molecular events underlying the control of complex behaviors

Tyramine and octopamine: ruling behavior and metabolism.

Remote Control of Behavior through Genetically Targeted Photostimulation of Neurons

The catecholamines play a major role in the regulation of behavior. Here we investigate, in the fly Drosophila melanogaster, the role of dopamine and octopamine (the presumed arthropod homolog of norepinephrine) during the formation of appetitive and aversive olfactory memories. We find that for the formation of both types of memories, cAMP signaling is necessary and sufficient within the same subpopulation of mushroom-body intrinsic neurons. On the other hand, memory formation can be distinguished by the requirement for different catecholamines, dopamine for aversive and octopamine for appetitive conditioning. Our results suggest that in associative conditioning, different memories are formed of the same odor under different circumstances, and that they are linked to the respective motivational systems by their specific modulatory pathways.

https://www.jneurosci.org/content/jneuro/23/33/10495.full.pdf

Dopamine and Octopamine Differentiate between Aversive and Appetitive Olfactory Memories in Drosophila

The ubiquitous cAMP-protein kinase A (PKA) signaling pathway exhibits complex temporal requirements during the time course of associative memory processing. This directly raises questions about the molecular mechanisms that provide signaling specificity to this pathway. Here, we use Drosophila olfactory conditioning to show that divergent cAMP signaling is mediated by functionally distinct pools of PKA. One particular pool is organized via the PKA regulatory type II subunit at the level of A-kinase anchoring proteins (AKAPs), a family of scaffolding proteins that provides focal points of spatiotemporal signal integration. This AKAP-bound pool of PKA is acting within neurons of the mushroom bodies to support a late phase of aversive memory. The requirement for AKAP-bound PKA signaling is limited to aversive memory, but dispensable during appetitive memory. This finding suggests the existence of additional mechanisms to support divergence within the cAMP-PKA signaling pathway during memory processing. Together, our results show that subcellular organization of signaling components plays a key role in memory processing.

https://www.jneurosci.org/content/jneuro/27/5/1229.full.pdf

Martin Schwaerzel

Papers

Dopamine and Octopamine Differentiate between Aversive and Appetitive Olfactory Memories in Drosophila

Signaling at A-Kinase Anchoring Proteins Organizes Anesthesia-Sensitive Memory in Drosophila