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 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 Sparsening and Temporal Sharpening of Olfactory Representations in the Honeybee Mushroom Bodies

2005 ◽  
Vol 94 (5) ◽  
pp. 3303-3313 ◽  
Author(s):  
Paul Szyszka ◽  
Mathias Ditzen ◽  
Alexander Galkin ◽  
C. Giovanni Galizia ◽  
Randolf Menzel
Keyword(s):  
Mushroom Body ◽  
Antennal Lobe ◽  
Activity Patterns ◽  
Projection Neuron ◽  
Insect Brain ◽  
Projection Neurons ◽  
Similar Response ◽  
Kenyon Cell ◽  
Cell Responses ◽  
Kenyon Cells

We explored the transformations accompanying the transmission of odor information from the first-order processing area, the antennal lobe, to the mushroom body, a higher-order integration center in the insect brain. Using Ca2+ imaging, we recorded activity in the dendrites of the projection neurons that connect the antennal lobe with the mushroom body. Next, we recorded the presynaptic terminals of these projection neurons. Finally, we characterized their postsynaptic partners, the intrinsic neurons of the mushroom body, the clawed Kenyon cells. We found fundamental differences in odor coding between the antennal lobe and the mushroom body. Odors evoked combinatorial activity patterns at all three processing stages, but the spatial patterns became progressively sparser along this path. Projection neuron dendrites and boutons showed similar response profiles, but the boutons were more narrowly tuned to odors. The transmission from projection neuron boutons to Kenyon cells was accompanied by a further sparsening of the population code. Activated Kenyon cells were highly odor specific. Furthermore, the onset of Kenyon cell responses to projection neurons occurred within the first 200 ms and complex temporal patterns were transformed into brief phasic responses. Thus two types of transformations occurred within the MB: sparsening of a combinatorial code, mediated by pre- and postsynaptic processing within the mushroom body microcircuits, and temporal sharpening of postsynaptic Kenyon cell responses, probably involving a broader loop of inhibitory recurrent neurons.

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.

Olfactory Microcircuits in Drosophila Melanogaster

2017 ◽  
pp. 361-368
Author(s):  
Jürgen Rybak ◽  
Bill S. Hansson
Keyword(s):  
Drosophila Melanogaster ◽  
Sensory Neurons ◽  
Mushroom Body ◽  
Antennal Lobe ◽  
Odorant Receptor ◽  
Second Order ◽  
Projection Neurons ◽  
Order Processing ◽  
Vinegar Fly ◽  
Maxillary Palps

In the vinegar fly (Drosophila melanogaster), the neuronal pathway that processes olfactory information is organized into multiple layers: a peripheral set of olfactory sensory neurons (OSNs); the primary olfactory center, or antennal lobe (AL); and two second-order neuropils, the mushroom body (MB) and lateral horn (LH). Odorants are detected by the dendrites of OSNs housed in sensilla on the maxillary palps and antennae. The OSN axons converge onto spherical synaptic neuropil within the AL termed glomeruli. OSNs that express the same odorant receptor project to the same glomerulus in a one-to-one fashion, forming discrete olfactory pathways. In the AL, a network of local interneurons (LNs) and projection neurons (PNs) contribute to the first-order processing within the glomeruli. Two types of PNs constitute the principal, parallel output pathways made by PN axons that end in the second-order neuropils of the MB and LH: uniglomerular PNs (uPNs) and multiglomerular PNs (mPNs).

Mushroom Body of the Honeybee

2017 ◽  
pp. 353-360
Author(s):  
Jürgen Rybak ◽  
Randolf Menzel
Keyword(s):  
Mushroom Body ◽  
Higher Order ◽  
Insect Species ◽  
Insect Brain ◽  
Projection Neurons ◽  
Kenyon Cells ◽  
Output Neurons ◽  
The Brain

The mushroom body (MB) in the insect brain is composed of a large number of densely packed neurons called Kenyon cells (KCs) (Drosophila, 2200; honeybee, 170,000). In most insect species, the MB consists of two caplike dorsal structures, the calyces, which contain the dendrites of KCs, and two to four lobes formed by collaterals of branching KC axons. Although the MB receives input and provides output throughout its whole structure, the neuropil part of the calyx receives predominantly multimodal input from sensory projection neurons (PNs) of second or a higher order, and the lobes send output neurons to many other parts of the brain, including recurrent neurons to the MB calyx. Widely branching, supposedly modulatory neurons (serotonergic, octopaminergic) innervate the MB at all levels (calyx, peduncle, and lobes), including the somata of KCs in the calyx (dopamine).

Olfactory Representations by Drosophila Mushroom Body Neurons

2008 ◽  
Vol 99 (2) ◽  
pp. 734-746 ◽  
Author(s):  
Glenn C. Turner ◽  
Maxim Bazhenov ◽  
Gilles Laurent
Keyword(s):  
Olfactory Receptor ◽  
Mushroom Body ◽  
Temporal Integration ◽  
Activity Patterns ◽  
Olfactory Receptor Neurons ◽  
Projection Neurons ◽  
Contributing Factors ◽  
Receptor Neurons ◽  
Whole Cell Recordings

Learning and memory has been studied extensively in Drosophila using behavioral, molecular, and genetic approaches. These studies have identified the mushroom body as essential for the formation and retrieval of olfactory memories. We investigated odor responses of the principal neurons of the mushroom body, the Kenyon cells (KCs), in Drosophila using whole cell recordings in vivo. KC responses to odors were highly selective and, thus sparse, compared with those of their direct inputs, the antennal lobe projection neurons (PNs). We examined the mechanisms that might underlie this transformation and identified at least three contributing factors: excitatory synaptic potentials (from PNs) decay rapidly, curtailing temporal integration, PN convergence onto individual KCs is low (∼10 PNs per KC on average), and KC firing thresholds are high. Sparse activity is thought to be useful in structures involved in memory in part because sparseness tends to reduce representation overlaps. By comparing activity patterns evoked by the same odors across olfactory receptor neurons and across KCs, we show that representations of different odors do indeed become less correlated as they progress through the olfactory system.

scholarly journals Visual input into the Drosophila melanogaster mushroom body

2020 ◽  
Author(s):  
Jinzhi Li ◽  
Brennan Dale Mahoney ◽  
Miles Solomon Jacob ◽  
Sophie Jeanne Cécile Caron
Keyword(s):  
Drosophila Melanogaster ◽  
Multisensory Integration ◽  
Visual Processing ◽  
Visual Information ◽  
Mushroom Body ◽  
Fundamental Property ◽  
Sensory Systems ◽  
Connectivity Pattern ◽  
Ideal System ◽  
Genetic Techniques

ABSTRACTThe ability to integrate input from different sensory systems is a fundamental property of many brains. Yet, the patterns of neuronal connectivity that underlie such multisensory integration remain poorly characterized. The Drosophila melanogaster mushroom body — an associative center required for the formation of olfactory and visual memories — is an ideal system to investigate how different sensory channels converge in higher-order brain centers. The neurons connecting the mushroom body to the olfactory system have been described in great detail, but input from other sensory systems remains poorly defined. Here, we use a range of anatomical and genetic techniques to identify two novel types of mushroom body input neuron that connect visual processing centers — namely the lobula and the posterior lateral protocerebrum — to the dorsal accessory calyx of the mushroom body. Together with previous work that described a pathway conveying visual information from the medulla to the ventral accessory calyx of the mushroom body (Vogt et al., 2016), our study defines a second, parallel pathway that is anatomically poised to convey information from the visual system to the dorsal accessory calyx. This connectivity pattern — the segregation of the visual information into two separate pathways — could be a fundamental feature of the neuronal architecture underlying multisensory integration in associative brain centers.

scholarly journals Inhibitory muscarinic acetylcholine receptors enhance aversive olfactory learning in adult Drosophila

eLife ◽  
2019 ◽  
Vol 8 ◽  
Author(s):  
Noa Bielopolski ◽  
Hoger Amin ◽  
Anthi A Apostolopoulou ◽  
Eyal Rozenfeld ◽  
Hadas Lerner ◽  
...  
Keyword(s):  
Synaptic Plasticity ◽  
Mushroom Body ◽  
Acetylcholine Receptors ◽  
Olfactory Learning ◽  
Muscarinic Acetylcholine Receptors ◽  
Projection Neurons ◽  
Kenyon Cell ◽  
Muscarinic Acetylcholine ◽  
Kenyon Cells ◽  
Output Neurons

Olfactory associative learning in Drosophila is mediated by synaptic plasticity between the Kenyon cells of the mushroom body and their output neurons. Both Kenyon cells and their inputs from projection neurons are cholinergic, yet little is known about the physiological function of muscarinic acetylcholine receptors in learning in adult flies. Here, we show that aversive olfactory learning in adult flies requires type A muscarinic acetylcholine receptors (mAChR-A), particularly in the gamma subtype of Kenyon cells. mAChR-A inhibits odor responses and is localized in Kenyon cell dendrites. Moreover, mAChR-A knockdown impairs the learning-associated depression of odor responses in a mushroom body output neuron. Our results suggest that mAChR-A function in Kenyon cell dendrites is required for synaptic plasticity between Kenyon cells and their output neurons.

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.

Sign in / Sign up

Export Citation Format

Share Document