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

2019 ◽  
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

AbstractIn 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.

scholarly journals Age and social experience induced plasticity across brain regions of the paper wasp Polistes fuscatus

2021 ◽  
Vol 17 (4) ◽  
Author(s):  
Christopher M. Jernigan ◽  
Natalie C. Zaba ◽  
Michael J. Sheehan
Keyword(s):  
Visual Processing ◽  
Mushroom Body ◽  
Developmental Plasticity ◽  
Brain Regions ◽  
Social Experience ◽  
Social Recognition ◽  
Paper Wasp ◽  
Paper Wasps ◽  
Polistes Fuscatus ◽  
Olfactory Processing

Developmental studies of brain volumes can reveal which portions of neural circuits are sensitive to environmental inputs. In social insects, differences in relative investment across brain regions emerge as behavioural repertoires change during ontogeny or as a result of experience. Here, we test the effects of maturation and social experience on morphological brain development in Polistes fuscatus paper wasps , focusing on brain regions involved in visual and olfactory processing. We find that mature wasps regardless of social experience have relatively larger brains than newly emerged wasps and this difference is driven by changes to mushroom body calyx and visual regions but not olfactory processing neuropils. Notably, social wasps invest more in the anterior optic tubercle (AOT), a visual glomerulus involved in colour and object processing in other taxa, relative to other visual integration centres the mushroom body calyces compared with aged socially naive wasps. Differences in developmental plasticity between visual and olfactory neuropil volumes are discussed in light of behavioural maturation in paper wasps, especially as it relates to social recognition. Previous research has shown that P. fuscatus need social experience to develop specialized visual processing of faces, which is used to individually recognize conspecifics. The present study suggests that the AOT is a candidate brain region that could mediate facial processing in this species.

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 Identification of FoxP circuits involved in locomotion and object fixation in Drosophila

2020 ◽  
Author(s):  
Ottavia Palazzo ◽  
Mathias Raß ◽  
Björn Brembs
Keyword(s):  
Transcription Factors ◽  
Mushroom Body ◽  
Mechanisms Of Action ◽  
Mushroom Bodies ◽  
Molecular Function ◽  
Genomic Locus ◽  
Kenyon Cells ◽  
Protocerebral Bridge ◽  
Object Fixation ◽  
Self Learning

AbstractThe FoxP family of transcription factors is necessary for operant self-learning, an evolutionary conserved form of motor learning. The expression pattern, molecular function and mechanisms of action of the Drosophila FoxP orthologue remain to be elucidated. By editing the genomic locus of FoxP with CRISPR/Cas9, we find that the three different FoxP isoforms are expressed in neurons, but not in glia and that not all neurons express all isoforms. Furthermore, we detect FoxP expression in, e.g., the protocerebral bridge, the fan shaped body and in motorneurons, but not in the mushroom bodies. Finally, we discover that FoxP expression during development, but not adulthood, is required for normal locomotion and landmark fixation in walking flies. While FoxP expression in the protocerebral bridge and motorneurons is involved in locomotion and landmark fixation, the FoxP gene can be excised from dorsal cluster neurons and mushroom-body Kenyon cells without affecting these behaviors.

scholarly journals Identification of FoxP circuits involved in locomotion and object fixation in Drosophila

Open Biology ◽  
2020 ◽  
Vol 10 (12) ◽  
pp. 200295
Author(s):  
Ottavia Palazzo ◽  
Mathias Rass ◽  
Björn Brembs
Keyword(s):  
Motor Neurons ◽  
Mushroom Body ◽  
Mechanisms Of Action ◽  
Mushroom Bodies ◽  
Molecular Function ◽  
Genomic Locus ◽  
Kenyon Cells ◽  
Protocerebral Bridge ◽  
Object Fixation ◽  
Self Learning

The FoxP family of transcription factors is necessary for operant self-learning, an evolutionary conserved form of motor learning. The expression pattern, molecular function and mechanisms of action of the Drosophila FoxP orthologue remain to be elucidated. By editing the genomic locus of FoxP with CRISPR/Cas9, we find that the three different FoxP isoforms are expressed in neurons, but not in glia and that not all neurons express all isoforms. Furthermore, we detect FoxP expression in, e.g. the protocerebral bridge, the fan-shaped body and in motor neurons, but not in the mushroom bodies. Finally, we discover that FoxP expression during development, but not adulthood, is required for normal locomotion and landmark fixation in walking flies. While FoxP expression in the protocerebral bridge and motor neurons is involved in locomotion and landmark fixation, the FoxP gene can be excised from dorsal cluster neurons and mushroom-body Kenyon cells without affecting these behaviours.

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.

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