Olfactory Microcircuits in Drosophila Melanogaster

Author(s):  
Jürgen Rybak ◽  
Bill S. Hansson

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).

2020 ◽  
Vol 11 ◽  
Author(s):  
Gerd Bicker ◽  
Michael Stern

Regeneration after injury is accompanied by transient and lasting changes in the neuroarchitecture of the nervous system and, thus, a form of structural plasticity. In this review, we introduce the olfactory pathway of a particular insect as a convenient model to visualize neural regeneration at an anatomical level and study functional recovery at an electrophysiological level. The olfactory pathway of the locust (Locusta migratoria) is characterized by a multiglomerular innervation of the antennal lobe by olfactory receptor neurons. These olfactory afferents were axotomized by crushing the base of the antenna. The resulting degeneration and regeneration in the antennal lobe could be quantified by size measurements, dye labeling, and immunofluorescence staining of cell surface proteins implicated in axonal guidance during development. Within 3 days post lesion, the antennal lobe volume was reduced by 30% and from then onward regained size back to normal by 2 weeks post injury. The majority of regenerating olfactory receptor axons reinnervated the glomeruli of the antennal lobe. A few regenerating axons project erroneously into the mushroom body on a pathway that is normally chosen by second-order projection neurons. Based on intracellular responses of antennal lobe output neurons to odor stimulation, regenerated fibers establish functional synapses again. Following complete absence after nerve crush, responses to odor stimuli return to control level within 10–14 days. On average, regeneration of afferents, and re-established synaptic connections appear faster in younger fifth instar nymphs than in adults. The initial degeneration of olfactory receptor axons has a trans-synaptic effect on a second order brain center, leading to a transient size reduction of the mushroom body calyx. Odor-evoked oscillating field potentials, absent after nerve crush, were restored in the calyx, indicative of regenerative processes in the network architecture. We conclude that axonal regeneration in the locust olfactory system appears to be possible, precise, and fast, opening an avenue for future mechanistic studies. As a perspective of biomedical importance, the current evidence for nitric oxide/cGMP signaling as positive regulator of axon regeneration in connectives of the ventral nerve cord is considered in light of particular regeneration studies in vertebrate central nervous systems.


2010 ◽  
Vol 10 (7-8) ◽  
pp. 328-337 ◽  
Author(s):  
Liria M. Masuda-Nakagawa ◽  
Takeshi Awasaki ◽  
Kei Ito ◽  
Cahir J. O’Kane

2005 ◽  
Vol 94 (5) ◽  
pp. 3303-3313 ◽  
Author(s):  
Paul Szyszka ◽  
Mathias Ditzen ◽  
Alexander Galkin ◽  
C. Giovanni Galizia ◽  
Randolf Menzel

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.


e-Neuroforum ◽  
2011 ◽  
Vol 17 (3) ◽  
Author(s):  
Silke Sachse ◽  
Jürgen Krieger

SummaryOdorants provide insects with crucial information about their environment and trigger various insect behaviors. A remarkably sensitive and selective sense of smell allows the animals to detect extremely low amounts of relevant odorants and thereby recognize, e.g., food, conspecifics, and predators. In recent years, significant progress has been made to­wards understanding the molecular elements and cellular mechanisms of odorant detection in the antenna and the principles under­lying the primary processing of olfactory signals in the brain. These findings show that olfactory hairs on the antenna are specifically equipped with chemosensory detector units. They contain several binding proteins, which transfer odorants to specific receptors resid­ing in the dendritic membrane of olfacto­ry sensory neurons (OSN). Binding of odor­ant to the receptor initiates ionotropic and/or metabotropic mechanisms, translating the chemical signal into potential changes, which alter the spontaneous action potential frequency in the axon of the sensory neurons. The odor-dependent action potentials propagate from the antennae along the axon to the brain leading to an input signal with­in the antennal lobe. In the antennal lobe, the first relay station for olfactory information, the input signals are extensively processed by a complex network of local interneurons be­fore being relayed by projection neurons to higher brain centers, where olfactory perception takes place.


Author(s):  
Elizabeth C. Marin ◽  
Ruairí J.V. Roberts ◽  
Laurin Büld ◽  
Maria Theiss ◽  
Markus W. Pleijzier ◽  
...  

SUMMARYAnimals exhibit innate and learned preferences for temperature and humidity – conditions critical for their survival and reproduction. Here, we leveraged a whole adult brain electron microscopy volume to study the circuitry associated with antennal thermosensory and hygrosensory neurons, which target specific ventroposterior (VP) glomeruli in the Drosophila melanogaster antennal lobe. We have identified two new VP glomeruli, in addition to the five known ones, and the projection neurons (VP PNs) that relay VP information to higher brain centres, including the mushroom body and lateral horn, seats of learned and innate olfactory behaviours, respectively. Focussing on the mushroom body lateral accessory calyx (lACA), a known thermosensory neuropil, we present a comprehensive connectome by reconstructing neurons downstream of heating- and cooling-responsive VP PNs. We find that a few lACA-associated mushroom body intrinsic neurons (Kenyon cells) solely receive thermosensory inputs, while most receive additional olfactory and thermo- or hygrosensory PN inputs in the main calyx. Unexpectedly, we find several classes of lACA-associated neurons that form a local network with outputs to other brain neuropils, suggesting that the lACA serves as a general hub for thermosensory circuitry. For example, we find DN1 pacemaker neurons that link the lACA to the accessory medulla, likely mediating temperature-based entrainment of the circadian clock. Finally, we survey strongly connected downstream partners of VP PNs across the protocerebrum; these include a descending neuron that receives input mainly from dry-responsive VP PNs, meaning that just two synapses might separate hygrosensory inputs from motor neurons in the nerve cord. (249)HIGHLIGHTSTwo novel thermo/hygrosensory glomeruli in the fly antennal lobeFirst complete set of thermosensory and hygrosensory projection neuronsFirst connectome for a thermosensory centre, the lateral accessory calyxNovel third order neurons, including a link to the circadian clock


2020 ◽  
Author(s):  
Tim Frey ◽  
Charles A. Kwadha ◽  
Erika A. Wallin ◽  
Elsa Holgersson ◽  
Erik Hedenström ◽  
...  

AbstractBackgroundAll living things speak chemical. The challenge is to discover the vocabulary, the volatile odorant chemicals that enable communication across phylogenies and to translate them to physiological, behavioural and ecological function. Olfactory receptors (ORs) interface animals with airborne odorants. Expression of single ORs in human embryonic kidney cells (HEK-293) makes it possible to interrogate ORs with synthetic chemicals and to identify cognate ligands that convey olfactory information.ResultsThe cosmopolitan strain of the vinegar fly Drosophila melanogaster has accompanied the human expansion out of Africa, more than ten thousand years ago. These flies are strictly anthropophilic and depend on human resources and housing for survival, particularly in colder climate zones. Curiously, humans sense the scent of a single fly, and more precisely the female pheromone (Z)-4 undecenal (Z4-11Al), at 10 ng/mL (0.06 µmol/L). A screening of all functional human ORs in a HEK-293 assay provides an explanation for this astounding sensitivity, as it shows that OR10A6, one of the most highly expressed human ORs, is specifically tuned to Z4-11Al. Chemical analysis of fly effluvia confirms that cosmopolitan D. melanogaster females release Z4-11Al, while females of an African fly strain from Zimbabwe release a 1:3-blend of Z4-11Al and (Z)-4 nonenal (Z4-9Al). Interestingly, a blend of Z4-9Al and Z4-11Al produces a different aroma than the the single compounds, which is why we readily differentiate cosmopolitan and Zimbabwe flies by nose.ConclusionThat we sensitively and specifically perceive the fly pheromone Z4-11Al suggests that it is a component of human odour scenes. This may have afforded a sensory drive during adaptation of commensal flies to human habitats and selected for a role of Z4-11Al in fly aggregation and premating communication. Screening ORs for key ligands leads to the discovery of messenger chemicals that enable chemical communication among and betwen vertebrate and invertebrate animals.


eLife ◽  
2018 ◽  
Vol 7 ◽  
Author(s):  
Jane Anne Horne ◽  
Carlie Langille ◽  
Sari McLin ◽  
Meagan Wiederman ◽  
Zhiyuan Lu ◽  
...  

Using FIB-SEM we report the entire synaptic connectome of glomerulus VA1v of the right antennal lobe in Drosophila melanogaster. Within the glomerulus we densely reconstructed all neurons, including hitherto elusive local interneurons. The fruitless-positive, sexually dimorphic VA1v included >11,140 presynaptic sites with ~38,050 postsynaptic dendrites. These connected input olfactory receptor neurons (ORNs, 51 ipsilateral, 56 contralateral), output projection neurons (18 PNs), and local interneurons (56 of >150 previously reported LNs). ORNs are predominantly presynaptic and PNs predominantly postsynaptic; newly reported LN circuits are largely an equal mixture and confer extensive synaptic reciprocity, except the newly reported LN2V with input from ORNs and outputs mostly to monoglomerular PNs, however. PNs were more numerous than previously reported from genetic screens, suggesting that the latter failed to reach saturation. We report a matrix of 192 bodies each having >50 connections; these form 88% of the glomerulus’ pre/postsynaptic sites.


2021 ◽  
Author(s):  
Tatsuya Hayashi ◽  
Alexander John MacKenzie ◽  
Ishani Ganguly ◽  
Hayley Smihula ◽  
Miles Solomon Jacob ◽  
...  

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.


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