A functional division of Drosophila sweet taste neurons that is value-based and task-specific

Sucrose is an attractive feeding substance and a positive reinforcer for Drosophila. But Drosophila females have been shown to robustly reject a sucrose-containing option for egg-laying when given a choice between a plain and a sucrose-containing option in specific contexts. How the sweet taste system of Drosophila promotes context-dependent devaluation of an egg-laying option that contains sucrose, an otherwise highly appetitive tastant, is unknown. Here, we report that devaluation of sweetness/sucrose for egg-laying is executed by a sensory pathway recruited specifically by the sweet neurons on the legs of Drosophila. First, silencing just the leg sweet neurons caused acceptance of the sucrose option in a sucrose versus plain decision, whereas expressing the channelrhodopsin CsChrimson in them caused rejection of a plain option that was “baited” with light over another that was not. Analogous bidirectional manipulations of other sweet neurons did not produce these effects. Second, circuit tracing revealed that the leg sweet neurons receive different presynaptic neuromodulations compared to some other sweet neurons and were the only ones with postsynaptic partners that projected prominently to the superior lateral protocerebrum (SLP) in the brain. Third, silencing one specific SLP-projecting postsynaptic partner of the leg sweet neurons reduced sucrose rejection, whereas expressing CsChrimson in it promoted rejection of a light-baited option during egg-laying. These results uncover that the Drosophila sweet taste system exhibits a functional division that is value-based and task-specific, challenging the conventional view that the system adheres to a simple labeled-line coding scheme.

Distinct protocerebral neuropils associated with attractive and aversive female-produced odorants in the male moth brain

The pheromone system of heliothine moths is an optimal model for studying principles underlying higher-order olfactory processing. In Helicoverpa armigera, three male-specific glomeruli receive input about three female-produced signals, the primary pheromone component, serving as an attractant, and two minor constituents, serving a dual function, i.e. attraction versus inhibition of attraction. From the antennal-lobe glomeruli, the information is conveyed to higher olfactory centers, including the lateral protocerebrum, via three main paths – of which the medial tract is the most prominent. In this study, we traced physiologically identified medial-tract projection neurons from each of the three male‑specific glomeruli with the aim of mapping their terminal branches in the lateral protocerebrum. Our data suggest that the neurons’ wide-spread projections are organized according to behavioral significance, including a spatial separation of signals representing attraction versus inhibition – however, with a unique capacity of switching behavioral consequence based on the amount of the minor components.

Shore crabs reveal novel evolutionary attributes of the mushroom body

Neural organization of mushroom bodies is largely consistent across insects, whereas the ancestral ground pattern diverges broadly across crustacean lineages resulting in successive loss of columns and the acquisition of domed centers retaining ancestral Hebbian-like networks and aminergic connections. We demonstrate here a major departure from this evolutionary trend in Brachyura, the most recent malacostracan lineage. In the shore crab Hemigrapsus nudus, instead of occupying the rostral surface of the lateral protocerebrum, mushroom body calyces are buried deep within it with their columns extending outwards to an expansive system of gyri on the brain’s surface. The organization amongst mushroom body neurons reaches extreme elaboration throughout its constituent neuropils. The calyces, columns, and especially the gyri show DC0 immunoreactivity, an indicator of extensive circuits involved in learning and memory.

Distinct protocerebral neuropils associated with attractive and aversive female-produced odorants in the male moth brain

The pheromone system of heliothine moths is an optimal model for studying principles underlying higher-order olfactory processing. In Helicoverpa armigera, three male-specific glomeruli receive input about three female-produced signals, the primary pheromone component, serving as an attractant, and two minor constituents, serving a dual function, i.e. attraction versus inhibition of attraction. From the antennal-lobe glomeruli, the information is conveyed to higher olfactory centers, including the lateral protocerebrum, via three main paths - of which the medial tract is the most prominent. In this study, we traced physiologically identified medial-tract projection neurons from each of the three male specific glomeruli with the aim of mapping their terminal branches in the lateral protocerebrum. Our data suggest that the neurons' wide-spread projections are organized according to behavioral significance, including a spatial separation of signals representing attraction versus inhibition - however, with a unique capacity of switching behavioral consequence based on the amount of the minor components.

Shore crabs reveal novel evolutionary attributes of the mushroom body

Neural organization of mushroom bodies is largely consistent across insects, whereas the ancestral ground pattern diverges broadly across crustacean lineages, resulting in successive loss of columns and the acquisition of domed centers retaining ancestral Hebbian-like networks and aminergic connections. We demonstrate here a major departure from this evolutionary trend in Brachyura, the most recent malacostracan lineage. Instead of occupying the rostral surface of the lateral protocerebrum, mushroom body calyces are buried deep within it, with their columns extending outwards to an expansive system of gyri on the brain’s surface. The organization amongst mushroom body neurons reaches extreme elaboration throughout its constituent neuropils. The calyces, columns, and especially the gyri show DC0 immunoreactivity, an indicator of extensive circuits involved in learning and memory.

Morphology and physiology of olfactory neurons in the lateral protocerebrum of the silkmoth Bombyx mori

Insect olfaction is a suitable model to investigate sensory processing in the brain. Olfactory information is first processed in the antennal lobe and is then conveyed to two second-order centres—the mushroom body calyx and the lateral protocerebrum. Projection neurons processing sex pheromones and plant odours supply the delta area of the inferior lateral protocerebrum (∆ILPC) and lateral horn (LH), respectively. Here, we investigated the neurons arising from these regions in the brain of the silkmoth, Bombyx mori, using mass staining and intracellular recording with a sharp glass microelectrode. The output neurons from the ∆ILPC projected to the superior medial protocerebrum, whereas those from the LH projected to the superior lateral protocerebrum. The dendritic innervations of output neurons from the ∆ILPC formed a subdivision in the ∆ILPC. We discuss pathways for odour processing in higher order centres.

Characterization of the olfactory system in Apis dorsata, an Asian honey bee

The European honeybee, Apis mellifera is the most common insect model system for studying learning and memory. We establish that the olfactory system of Apis dorsata, an Asian species of honeybee as an equivalent model to Apis mellifera to study physiology underlying learning and memory. We created an Atlas of the antennal lobe and counted the number of glomeruli in the antennal lobe of Apis dorsata to be around 165 which is similar to the number in the other honey bee species Apis mellifera and Apis florea. Apis dorsata was found to have five antenno-cerebral tracts namely mACT, lACT and 3 mlACTS which appear identical to Apis mellifera. Intracellular recording showed that the antennal lobe interneurons exhibit temporally patterned odor-cell specific responses. The neuritis of Kenyon cells with cell bodies located in a neighborhood in calyx retain their relative neighborhoods in the peduncle and alpha lobe forming a columnar organization in the mushroom body. Alpha lobe and the calyx of the mushroom body were innervated by extrinsic neurons with cell bodies in the lateral protocerebrum. A set of GABA positive cells in the lateral protocerebrum send their neurites towards alpha-lobe. Apis dorsata was amenable to olfactory conditioning and showed good learning and memory retention at 24 hours. They were amenable to massed and spaced conditioning and could distinguish trained odor from an untrained novel odor.

The Insect Visual System: Correspondence with Vertebrates and with Olfactory Processing

A 1915 monograph by the Nobel Prize–winning neuroanatomist Santiago Ramón y Cajal and Domingo Sánchez y Sánchez, describing neurons and their organization in the optic lobes of insects, is now standard fare for those studying the microcircuitry of the insect visual system. The work contains prescient assumptions about possible functional arrangements, such as lateral interactions, centrifugal pathways, and the convergence of neurons onto wider dendritic trees, to provide central integration of information processed at peripheral levels of the system. This chapter will consider further indications of correspondence between the insect-crustacean and the vertebrate visual systems, with particular reference to the deep organization of the optic lobe’s third optic neuropil, the lobula, and part of the lateral forebrain (protocerebrum) that receives inputs from it. Together, the lobula and lateral protocerebrum suggest valid comparison with the visual cortex and olfactory centers.

Long-range projection neurons in the taste circuit of Drosophila

Taste compounds elicit innate feeding behaviors and act as rewards or punishments to entrain other cues. The neural pathways by which taste compounds influence innate and learned behaviors have not been resolved. Here, we identify three classes of taste projection neurons (TPNs) in Drosophila melanogaster distinguished by their morphology and taste selectivity. TPNs receive input from gustatory receptor neurons and respond selectively to sweet or bitter stimuli, demonstrating segregated processing of different taste modalities. Activation of TPNs influences innate feeding behavior, whereas inhibition has little effect, suggesting parallel pathways. Moreover, two TPN classes are absolutely required for conditioned taste aversion, a learned behavior. The TPNs essential for conditioned aversion project to the superior lateral protocerebrum (SLP) and convey taste information to mushroom body learning centers. These studies identify taste pathways from sensory detection to higher brain that influence innate behavior and are essential for learned responses to taste compounds.