scholarly journals Reward signaling in a recurrent circuit of dopaminergic neurons and Kenyon cells

2018 ◽  
Author(s):  
Radostina Lyutova ◽  
Maximilian Pfeuffer ◽  
Dennis Segebarth ◽  
Jens Habenstein ◽  
Mareike Selcho ◽  
...  
Keyword(s):  
Learning And Memory ◽  
Dopaminergic Neurons ◽  
Mushroom Body ◽  
Olfactory Learning ◽  
Mushroom Bodies ◽  
Neuronal Circuitry ◽  
Sustained Activity ◽  
Kenyon Cells ◽  
Reward Information ◽  
The Brain

1.AbstractDopaminergic neurons in the brain of theDrosophilalarva play a key role in mediating reward information to the mushroom bodies during appetitive olfactory learning and memory. Using optogenetic activation of Kenyon cells we provide evidence that a functional recurrent signaling loop exists between Kenyon cells and dopaminergic neurons of the primary protocerebral anterior (pPAM) cluster. An optogenetic activation of Kenyon cells paired with an odor is sufficient to induce appetitive memory, while a simultaneous impairment of the dopaminergic pPAM neurons abolishes memory expression. Thus, dopaminergic pPAM neurons mediate reward information to the Kenyon cells, but in turn receive feedback from Kenyon cells. We further show that the activation of recurrent signaling routes within mushroom body circuitry increases the persistence of an odor-sugar memory. Our results suggest that sustained activity in a neuronal circuitry is a conserved mechanism in insects and vertebrates to consolidate memories.

scholarly journals Olfactory Learning in Drosophila

Physiology ◽  
2010 ◽  
Vol 25 (6) ◽  
pp. 338-346 ◽  
Author(s):  
Germain U. Busto ◽  
Isaac Cervantes-Sandoval ◽  
Ronald L. Davis
Keyword(s):  
Dopaminergic Neurons ◽  
Mushroom Body ◽  
Sensory Information ◽  
Brain Regions ◽  
Olfactory Learning ◽  
Mushroom Bodies ◽  
Neural Pathways ◽  
Olfactory Information ◽  
Appetitive Stimuli ◽  
The Brain

Studies of olfactory learning in Drosophila have provided key insights into the brain mechanisms underlying learning and memory. One type of olfactory learning, olfactory classical conditioning, consists of learning the contingency between an odor with an aversive or appetitive stimulus. This conditioning requires the activity of molecules that can integrate the two types of sensory information, the odorant as the conditioned stimulus and the aversive or appetitive stimulus as the unconditioned stimulus, in brain regions where the neural pathways for the two stimuli intersect. Compelling data indicate that a particular form of adenylyl cyclase functions as a molecular integrator of the sensory information in the mushroom body neurons. The neuronal pathway carrying the olfactory information from the antennal lobes to the mushroom body is well described. Accumulating data now show that some dopaminergic neurons provide information about aversive stimuli and octopaminergic neurons about appetitive stimuli to the mushroom body neurons. Inhibitory inputs from the GABAergic system appear to gate olfactory information to the mushroom bodies and thus control the ability to learn about odors. Emerging data obtained by functional imaging procedures indicate that distinct memory traces form in different brain regions and correlate with different phases of memory. The results from these and other experiments also indicate that cross talk between mushroom bodies and several other brain regions is critical for memory formation.

scholarly journals Predictive olfactory learning in Drosophila

2021 ◽  
Vol 11 (1) ◽  
Author(s):  
Chang Zhao ◽  
Yves F. Widmer ◽  
Sören Diegelmann ◽  
Mihai A. Petrovici ◽  
Simon G. Sprecher ◽  
...  
Keyword(s):  
Synaptic Plasticity ◽  
Dopaminergic Neurons ◽  
Mushroom Body ◽  
Trace Conditioning ◽  
Fruit Fly ◽  
Olfactory Learning ◽  
Shock Strength ◽  
Behavioral Experiments ◽  
Kenyon Cells ◽  
Output Neurons

AbstractOlfactory learning and conditioning in the fruit fly is typically modelled by correlation-based associative synaptic plasticity. It was shown that the conditioning of an odor-evoked response by a shock depends on the connections from Kenyon cells (KC) to mushroom body output neurons (MBONs). Although on the behavioral level conditioning is recognized to be predictive, it remains unclear how MBONs form predictions of aversive or appetitive values (valences) of odors on the circuit level. We present behavioral experiments that are not well explained by associative plasticity between conditioned and unconditioned stimuli, and we suggest two alternative models for how predictions can be formed. In error-driven predictive plasticity, dopaminergic neurons (DANs) represent the error between the predictive odor value and the shock strength. In target-driven predictive plasticity, the DANs represent the target for the predictive MBON activity. Predictive plasticity in KC-to-MBON synapses can also explain trace-conditioning, the valence-dependent sign switch in plasticity, and the observed novelty-familiarity representation. The model offers a framework to dissect MBON circuits and interpret DAN activity during olfactory learning.

scholarly journals Predictive olfactory learning in Drosophila

2019 ◽  
Author(s):  
Chang Zhao ◽  
Yves F Widmer ◽  
Soeren Diegelmann ◽  
Mihai Petrovici ◽  
Simon G Sprecher ◽  
...  
Keyword(s):  
Synaptic Plasticity ◽  
Dopaminergic Neurons ◽  
Mushroom Body ◽  
Trace Conditioning ◽  
Fruit Fly ◽  
Olfactory Learning ◽  
Shock Strength ◽  
Behavioral Experiments ◽  
Kenyon Cells ◽  
Output Neurons

AbstractOlfactory learning and conditioning in the fruit fly is typically modelled by correlation-based associative synaptic plasticity. It was shown that the conditioning of an odor-evoked response by a shock depends on the connections from Kenyon cells (KC) to mushroom body output neurons (MBONs). Although on the behavioral level conditioning is recognized to be predictive, it remains unclear how MBONs form predictions of aversive or appetitive values (valences) of odors on the circuit level. We present behavioral experiments that are not well explained by associative plasticity between conditioned and unconditioned stimuli, and we suggest two alternative models for how predictions can be formed. In error-driven predictive plasticity, dopaminergic neurons (DANs) represent the error between the predictive odor value and the shock strength. In target-driven predictive plasticity, the DANs represent the target for the predictive MBON activity. Predictive plasticity in KC-to-MBON synapses can also explain trace-conditioning, the valence-dependent sign switch in plasticity, and the observed novelty-familiarity representation. The model offer a framework to dissect MBON circuits and interpret DAN activity during olfactory learning.

scholarly journals Drosophila mushroom bodies integrate hunger and satiety signals to control innate food-seeking behavior

eLife ◽  
2018 ◽  
Vol 7 ◽  
Author(s):  
Chang-Hui Tsao ◽  
Chien-Chun Chen ◽  
Chen-Han Lin ◽  
Hao-Yu Yang ◽  
Suewei Lin
Keyword(s):  
Dopaminergic Neurons ◽  
Mushroom Body ◽  
Energy State ◽  
Fruit Fly ◽  
Mushroom Bodies ◽  
Kenyon Cells ◽  
Control Food ◽  
Seeking Behavior ◽  
Output Neurons ◽  
Food Seeking

The fruit fly can evaluate its energy state and decide whether to pursue food-related cues. Here, we reveal that the mushroom body (MB) integrates hunger and satiety signals to control food-seeking behavior. We have discovered five pathways in the MB essential for hungry flies to locate and approach food. Blocking the MB-intrinsic Kenyon cells (KCs) and the MB output neurons (MBONs) in these pathways impairs food-seeking behavior. Starvation bi-directionally modulates MBON responses to a food odor, suggesting that hunger and satiety controls occur at the KC-to-MBON synapses. These controls are mediated by six types of dopaminergic neurons (DANs). By manipulating these DANs, we could inhibit food-seeking behavior in hungry flies or promote food seeking in fed flies. Finally, we show that the DANs potentially receive multiple inputs of hunger and satiety signals. This work demonstrates an information-rich central circuit in the fly brain that controls hunger-driven food-seeking behavior.

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

eLife ◽  
2014 ◽  
Vol 3 ◽  
Author(s):  
Yoshinori Aso ◽  
Daisuke Hattori ◽  
Yang Yu ◽  
Rebecca M Johnston ◽  
Nirmala A Iyer ◽  
...  
Keyword(s):  
Associative Learning ◽  
Learning And Memory ◽  
Mushroom Body ◽  
Dopaminergic Neuron ◽  
Olfactory Learning ◽  
Kenyon Cell ◽  
Feedforward Network ◽  
Kenyon Cells ◽  
Functional Logic ◽  
Dendritic Arbors

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.

scholarly journals Drosophila mef2 is essential for normal mushroom body and wing development

2018 ◽  
Author(s):  
Jill R. Crittenden ◽  
Efthimios M. C. Skoulakis ◽  
Elliott. S. Goldstein ◽  
Ronald L. Davis
Keyword(s):  
Nuclear Localization ◽  
Mushroom Body ◽  
Normal Development ◽  
Cell Types ◽  
Mushroom Bodies ◽  
Wing Development ◽  
Myocyte Enhancer Factor 2 ◽  
Multiple Cell ◽  
The Brain ◽  
Enhancer Factor

ABSTRACTMEF2 (myocyte enhancer factor 2) transcription factors are found in the brain and muscle of insects and vertebrates and are essential for the differentiation of multiple cell types. We show that in the fruitfly Drosophila, MEF2 is essential for normal development of wing veins, and for mushroom body formation in the brain. In embryos mutant for D-mef2, there was a striking reduction in the number of mushroom body neurons and their axon bundles were not detectable. D-MEF2 expression coincided with the formation of embryonic mushroom bodies and, in larvae, expression onset was confirmed to be in post-mitotic neurons. With a D-mef2 point mutation that disrupts nuclear localization, we find that D-MEF2 is restricted to a subset of Kenyon cells that project to the α/β, and γ axonal lobes of the mushroom bodies, but not to those forming the α’/β’ lobes. Our findings that ancestral mef2 is specifically important in dopamine-receptive neurons has broad implications for its function in mammalian neurocircuits.

scholarly journals Presynaptic developmental plasticity allows robust sparse wiring of the Drosophila mushroom body

eLife ◽  
2020 ◽  
Vol 9 ◽  
Author(s):  
Najia A Elkahlah ◽  
Jackson A Rogow ◽  
Maria Ahmed ◽  
E Josephine Clowney
Keyword(s):  
Mushroom Body ◽  
Developmental Plasticity ◽  
Brain Regions ◽  
Mushroom Bodies ◽  
Set Convergence ◽  
Limited Size ◽  
Sensory Inputs ◽  
Kenyon Cells ◽  
Complex Stimuli ◽  
Developmental Patterning

In order to represent complex stimuli, principle neurons of associative learning regions receive combinatorial sensory inputs. Density of combinatorial innervation is theorized to determine the number of distinct stimuli that can be represented and distinguished from one another, with sparse innervation thought to optimize the complexity of representations in networks of limited size. How the convergence of combinatorial inputs to principle neurons of associative brain regions is established during development is unknown. Here, we explore the developmental patterning of sparse olfactory inputs to Kenyon cells of the Drosophila melanogaster mushroom body. By manipulating the ratio between pre- and post-synaptic cells, we find that postsynaptic Kenyon cells set convergence ratio: Kenyon cells produce fixed distributions of dendritic claws while presynaptic processes are plastic. Moreover, we show that sparse odor responses are preserved in mushroom bodies with reduced cellular repertoires, suggesting that developmental specification of convergence ratio allows functional robustness.

scholarly journals Brain composition in Heliconius butterflies, post-eclosion growth and experience dependent neuropil plasticity

2015 ◽  
Author(s):  
Stephen H Montgomery ◽  
Richard M Merrill ◽  
Swidbert R Ott
Keyword(s):  
Behavioral Ecology ◽  
Neural Development ◽  
Mushroom Body ◽  
Brain Regions ◽  
Mushroom Bodies ◽  
Heliconius Butterflies ◽  
Sensory Adaptations ◽  
Differential Expansion ◽  
The Brain

Behavioral and sensory adaptations are often based in the differential expansion of brain components. These volumetric differences represent changes in investment, processing capacity and/or connectivity, and can be used to investigate functional and evolutionary relationships between different brain regions, and between brain composition and behavioral ecology. Here, we describe the brain composition of two species of Heliconius butterflies, a long-standing study system for investigating ecological adaptation and speciation. We confirm a previous report of striking mushroom body expansion, and explore patterns of post-eclosion growth and experience-dependent plasticity in neural development. This analysis uncovers age- and experience-dependent post-emergence mushroom body growth comparable to that in foraging hymenoptera, but also identifies plasticity in several other neuropil. An interspecific analysis indicates that Heliconius display remarkable levels of investment in mushroom bodies for a lepidopteran, and indeed rank highly compared to other insects. Our analyses lay the foundation for future comparative and experimental analyses that will establish Heliconius as a useful case study in evolutionary neurobiology.

Octopamine-like immunoreactivity in the brain and suboesophageal ganglion of two parasitic wasps, Cotesia glomerata and Cotesia rubecula

2006 ◽  
Vol 56 (2) ◽  
pp. 247-257 ◽  
Author(s):  
Hans Smid ◽  
Brenda van der Zee ◽  
Maartje Bleeker
Keyword(s):  
Learning And Memory ◽  
Parasitoid Wasp ◽  
Staining Intensity ◽  
Cotesia Glomerata ◽  
Mushroom Bodies ◽  
Suboesophageal Ganglion ◽  
Wasp Species ◽  
Labelling Intensity ◽  
Protocerebral Bridge ◽  
The Brain

AbstractTwo closely related parasitoid wasp species, Cotesia glomerata L. and C. rubecula Marshall (Hymenoptera: Braconidae), differ in their display of associative learning and memory during host searching. As octopamine is involved in learning and memory in insects we investigated octopaminergic pathways in the brain and suboesophageal ganglion (SOG) of the two wasps. We used an anti-octopamine antibody and subsequent whole mount analysis using a confocal laserscanning microscope and pertinent software. Three groups of octopaminergic cells were located in the brain and suboesophageal ganglion. One group was located near the antennal lobes and consisted of six to eight cell bodies. A second group was located ventrally in the SOG and was most likely formed by ventral unpaired median (VUM) and VCBN (ventral cell body neurite) neurons. A third group was located in the pars intercerebralis and consisted of four to six cells. Octopamine-like immunoreactivity was furthermore present in the central body, protocerebral bridge, the SOG, antennal lobe, near the alpha and beta lobes of the mushroom bodies and in the mushroom body calyces. Due to the used methods and a high variability in staining intensity it was not possible to detect if there were any differences in the number of neurons, in arborisation patterns or in labelling intensity between the two wasp species.

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