scholarly journals Structured sampling of olfactory input by the fly mushroom body

2020 ◽  
Author(s):  
Zhihao Zheng ◽  
Feng Li ◽  
Corey Fisher ◽  
Iqbal J. Ali ◽  
Nadiya Sharifi ◽  
...  
Keyword(s):  
Network Structure ◽  
Mushroom Body ◽  
Sensory Information ◽  
Fruit Fly ◽  
Projection Neurons ◽  
Large Numbers ◽  
Unified View ◽  
Olfactory Input ◽  
To Receive ◽  
Random Connectivity

AbstractAssociative memory formation and recall in the adult fruit fly Drosophila melanogaster is subserved by the mushroom body (MB). Upon arrival in the MB, sensory information undergoes a profound transformation. Olfactory projection neurons (PNs), the main MB input, exhibit broadly tuned, sustained, and stereotyped responses to odorants; in contrast, their postsynaptic targets in the MB, the Kenyon cells (KCs), are nonstereotyped, narrowly tuned, and only briefly responsive to odorants. Theory and experiment have suggested that this transformation is implemented by random connectivity between KCs and PNs. However, this hypothesis has been challenging to test, given the difficulty of mapping synaptic connections between large numbers of neurons to achieve a unified view of neuronal network structure. Here we used a recent whole-brain electron microscopy (EM) volume of the adult fruit fly to map large numbers of PN- to-KC connections at synaptic resolution. Comparison of the observed connectome to precisely defined null models revealed unexpected network structure, in which a subset of food-responsive PN types converge on individual downstream KCs more frequently than expected. The connectivity bias is consistent with the neurogeometry: axons of the overconvergent PNs tend to arborize near one another in the MB main calyx, making local KC dendrites more likely to receive input from those types. Computational modeling of the observed PN-to-KC network showed that input from the overconvergent PN types is better discriminated than input from other types. These results suggest an ‘associative fovea’ for olfaction, in that the MB is wired to better discriminate more frequently occurring and ethologically relevant combinations of food-related odors.

scholarly journals The anterior paired lateral neuron normalizes odour-evoked activity at the mushroom body calyx

2021 ◽  
Author(s):  
Luigi Prisco ◽  
Stephan Hubertus Deimel ◽  
Hanna Yeliseyeva ◽  
Andre Fiala ◽  
Gaia Tavosanis
Keyword(s):  
Mushroom Body ◽  
Activity Patterns ◽  
Sensory Information ◽  
Input Circuit ◽  
Projection Neurons ◽  
Neuronal Populations ◽  
Kenyon Cells ◽  
Presynaptic Boutons ◽  
Evoked Activity

To identify and memorize discrete but similar environmental inputs, the brain needs to distinguish between subtle differences of activity patterns in defined neuronal populations. The Kenyon cells of the Drosophila adult mushroom body (MB) respond sparsely to complex olfactory input, a property that is thought to support stimuli discrimination in the MB. To understand how this property emerges, we investigated the role of the inhibitory anterior paired lateral neuron (APL) in the input circuit of the MB, the calyx. Within the calyx, presynaptic boutons of projection neurons (PNs) form large synaptic microglomeruli (MGs) with dendrites of postsynaptic Kenyon cells (KCs). Combining EM data analysis and in vivo calcium imaging, we show that APL, via inhibitory and reciprocal synapses targeting both PN boutons and KC dendrites, normalizes odour-evoked representations in MGs of the calyx. APL response scales with the PN input strength and is regionalized around PN input distribution. Our data indicate that the formation of a sparse code by the Kenyon cells requires APL-driven normalization of their MG postsynaptic responses. This work provides experimental insights on how inhibition shapes sensory information representation in a higher brain centre, thereby supporting stimuli discrimination and allowing for efficient associative memory formation.

scholarly journals The anterior paired lateral neuron normalizes odour-evoked activity in the Drosophila mushroom body calyx

eLife ◽  
2021 ◽  
Vol 10 ◽  
Author(s):  
Luigi Prisco ◽  
Stephan Hubertus Deimel ◽  
Hanna Yeliseyeva ◽  
André Fiala ◽  
Gaia Tavosanis
Keyword(s):  
Mushroom Body ◽  
Activity Patterns ◽  
Sensory Information ◽  
Input Circuit ◽  
Projection Neurons ◽  
Neuronal Populations ◽  
Kenyon Cells ◽  
Presynaptic Boutons ◽  
Evoked Activity

To identify and memorize discrete but similar environmental inputs, the brain needs to distinguish between subtle differences of activity patterns in defined neuronal populations. The Kenyon cells of the Drosophila adult mushroom body (MB) respond sparsely to complex olfactory input, a property that is thought to support stimuli discrimination in the MB. To understand how this property emerges, we investigated the role of the inhibitory anterior paired lateral neuron (APL) in the input circuit of the MB, the calyx. Within the calyx, presynaptic boutons of projection neurons (PNs) form large synaptic microglomeruli (MGs) with dendrites of postsynaptic Kenyon cells (KCs). Combining EM data analysis and in vivo calcium imaging, we show that APL, via inhibitory and reciprocal synapses targeting both PN boutons and KC dendrites, normalizes odour-evoked representations in MGs of the calyx. APL response scales with the PN input strength and is regionalized around PN input distribution. Our data indicate that the formation of a sparse code by the Kenyon cells requires APL-driven normalization of their MG postsynaptic responses. This work provides experimental insights on how inhibition shapes sensory information representation in a higher brain centre, thereby supporting stimuli discrimination and allowing for efficient associative memory formation.

scholarly journals Direct neural pathways convey distinct visual information to Drosophila mushroom bodies

eLife ◽  
2016 ◽  
Vol 5 ◽  
Author(s):  
Katrin Vogt ◽  
Yoshinori Aso ◽  
Toshihide Hige ◽  
Stephan Knapek ◽  
Toshiharu Ichinose ◽  
...  
Keyword(s):  
Visual Information ◽  
Mushroom Body ◽  
Mushroom Bodies ◽  
Small Subset ◽  
Projection Neurons ◽  
Neural Pathways ◽  
Associative Memories ◽  
Visual Projection ◽  
Olfactory Input ◽  
Odor Representation

Previously, we demonstrated that visual and olfactory associative memories of Drosophila share mushroom body (MB) circuits (<xref ref-type="bibr" rid="bib46">Vogt et al., 2014</xref>). Unlike for odor representation, the MB circuit for visual information has not been characterized. Here, we show that a small subset of MB Kenyon cells (KCs) selectively responds to visual but not olfactory stimulation. The dendrites of these atypical KCs form a ventral accessory calyx (vAC), distinct from the main calyx that receives olfactory input. We identified two types of visual projection neurons (VPNs) directly connecting the optic lobes and the vAC. Strikingly, these VPNs are differentially required for visual memories of color and brightness. The segregation of visual and olfactory domains in the MB allows independent processing of distinct sensory memories and may be a conserved form of sensory representations among insects.

scholarly journals Mushroom body input connections form independently of sensory activity in Drosophila melanogaster

2021 ◽  
Author(s):  
Tatsuya Hayashi ◽  
Alexander John MacKenzie ◽  
Ishani Ganguly ◽  
Hayley Smihula ◽  
Miles Solomon Jacob ◽  
...  
Keyword(s):  
Drosophila Melanogaster ◽  
Mushroom Body ◽  
Activity Patterns ◽  
Sensory Information ◽  
Population Level ◽  
Connectivity Pattern ◽  
Projection Neurons ◽  
Efficient Manner ◽  
Kenyon Cells ◽  
Sensory Activity

Associative brain centers, such as the insect mushroom body, need to represent sensory information in an efficient manner. In Drosophila melanogaster, the Kenyon cells of the mushroom body integrate inputs from a random set of olfactory projection neurons, but some projection neurons, namely those activated by a few ethologically meaningful odors, connect to Kenyon cells more frequently than others. This biased and random connectivity pattern is conceivably advantageous, as it enables the mushroom body to represent a large number of odors as unique activity patterns while prioritizing the representation of a few specific odors. How this connectivity pattern is established remains largely unknown. Here, we test whether the mechanisms patterning the connections between Kenyon cells and projection neurons depend on sensory activity or whether they are hardwired. We mapped a large number of mushroom body input connections in anosmic flies, flies lacking the obligate odorant co-receptor Orco, and in wildtype flies. Statistical analyses of these datasets reveal that the random and biased connectivity pattern observed between Kenyon cells and projection neurons forms normally in the absence of most olfactory sensory activity. This finding supports the idea that even comparatively subtle, population-level patterns of neuronal connectivity can be encoded by fixed genetic programs and are likely to be the result of evolved prioritization of ecologically and ethologically salient stimuli.

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 Multimodal integration and stimulus categorization in putative mushroom body output neurons of the honeybee

2018 ◽  
Vol 5 (2) ◽  
pp. 171785 ◽  
Author(s):  
Martin F. Strube-Bloss ◽  
Wolfgang Rössler
Keyword(s):  
Visual Information ◽  
Mushroom Body ◽  
Visual Cues ◽  
Sensory Modality ◽  
Sensory Information ◽  
Insect Brain ◽  
Pollinating Insects ◽  
Output Neurons ◽  
Electrophysiological Characterization ◽  
Nonlinear Integration

Flowers attract pollinating insects like honeybees by sophisticated compositions of olfactory and visual cues. Using honeybees as a model to study olfactory–visual integration at the neuronal level, we focused on mushroom body (MB) output neurons (MBON). From a neuronal circuit perspective, MBONs represent a prominent level of sensory-modality convergence in the insect brain. We established an experimental design allowing electrophysiological characterization of olfactory, visual, as well as olfactory–visual induced activation of individual MBONs. Despite the obvious convergence of olfactory and visual pathways in the MB, we found numerous unimodal MBONs. However, a substantial proportion of MBONs (32%) responded to both modalities and thus integrated olfactory–visual information across MB input layers. In these neurons, representation of the olfactory–visual compound was significantly increased compared with that of single components, suggesting an additive, but nonlinear integration. Population analyses of olfactory–visual MBONs revealed three categories: (i) olfactory, (ii) visual and (iii) olfactory–visual compound stimuli. Interestingly, no significant differentiation was apparent regarding different stimulus qualities within these categories. We conclude that encoding of stimulus quality within a modality is largely completed at the level of MB input, and information at the MB output is integrated across modalities to efficiently categorize sensory information for downstream behavioural decision processing.

Materials and methods.

2022 ◽  
pp. 5-5
Author(s):  
Richard A. I. Drew ◽  
Meredith C. Romig
Keyword(s):  
Papua New Guinea ◽  
New Guinea ◽  
Fruit Fly ◽  
Methyl Eugenol ◽  
Microscopic Identification ◽  
Host Fruit ◽  
Large Numbers ◽  
Wide Range

Abstract Large numbers of dacine specimens were collected throughout Papua New Guinea by trapping and host fruit sampling. Steinertype fruit fly traps, baited with cue lure, methyl eugenol or vanillylacetone (zingerone), were set in many localities over a wide range of ecosystems. In most cases, the traps were serviced on 2-week cycles for at least 1 year. Samples of rainforest and cultivated fruits were collected in some provinces. All specimens collected were preserved in a dry state and sent to R.A.I. Drew at Griffith University, Brisbane, Australia, for microscopic identification and curation. Data and photographs of Bactrocera longicornis were received from the Museum Nationale d'Histoire Naturelle, Paris, France. The subgeneric classification used herein follows Drew and Hancock (2016) and Hancock and Drew (2006, 2015, 2016, 2017a,b,c,d,e, 2018a,b,c, 2019).

scholarly journals Increased Callosal Connectivity in Reeler Mice Revealed by Brain-Wide Input Mapping of VIP Neurons in Barrel Cortex

2020 ◽  
Author(s):  
Georg Hafner ◽  
Julien Guy ◽  
Mirko Witte ◽  
Pavel Truschow ◽  
Alina Rüppel ◽  
...  
Keyword(s):  
Long Range ◽  
Cortical Neurons ◽  
Barrel Cortex ◽  
Projection Neurons ◽  
Subcortical Structures ◽  
Virus Tracing ◽  
Cortical Inputs ◽  
Callosal Projection ◽  
To Receive ◽  
The Brain

Abstract The neocortex is composed of layers. Whether layers constitute an essential framework for the formation of functional circuits is not well understood. We investigated the brain-wide input connectivity of vasoactive intestinal polypeptide (VIP) expressing neurons in the reeler mouse. This mutant is characterized by a migration deficit of cortical neurons so that no layers are formed. Still, neurons retain their properties and reeler mice show little cognitive impairment. We focused on VIP neurons because they are known to receive strong long-range inputs and have a typical laminar bias toward upper layers. In reeler, these neurons are more dispersed across the cortex. We mapped the brain-wide inputs of VIP neurons in barrel cortex of wild-type and reeler mice with rabies virus tracing. Innervation by subcortical inputs was not altered in reeler, in contrast to the cortical circuitry. Numbers of long-range ipsilateral cortical inputs were reduced in reeler, while contralateral inputs were strongly increased. Reeler mice had more callosal projection neurons. Hence, the corpus callosum was larger in reeler as shown by structural imaging. We argue that, in the absence of cortical layers, circuits with subcortical structures are maintained but cortical neurons establish a different network that largely preserves cognitive functions.

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 Connectivity patterns shape sensory representation in a cerebellum-like network

2021 ◽  
Author(s):  
Daniel Zavitz ◽  
Elom A. Amematsro ◽  
Alla Borisyuk ◽  
Sophie J.C. Caron
Keyword(s):  
Learning Outcomes ◽  
Network Architecture ◽  
Mushroom Body ◽  
Structural Features ◽  
Projection Neurons ◽  
Sensory Representation ◽  
Learning Function ◽  
Kenyon Cells ◽  
Connectivity Patterns ◽  
Function Relationship

SUMMARYCerebellum-like structures are found in many brains and share a basic fan-out–fan-in network architecture. How the specific structural features of these networks give rise to their learning function remains largely unknown. To investigate this structure–function relationship, we developed a realistic computational model of an empirically very well-characterized cerebellum-like structure, the Drosophila melanogaster mushroom body. We show how well-defined connectivity patterns between the Kenyon cells, the constituent neurons of the mushroom body, and their input projection neurons enable different functions. First, biases in the likelihoods at which individual projection neurons connect to Kenyon cells allow the mushroom body to prioritize the learning of particular, ethologically meaningful odors. Second, groups of projection neurons connecting preferentially to the same Kenyon cells facilitate the mushroom body generalizing across similar odors. Altogether, our results demonstrate how different connectivity patterns shape the representation space of a cerebellum-like network and impact its learning outcomes.

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