Targeting expression to projection neurons that innervate specific mushroom body calyx and antennal lobe glomeruli in larval Drosophila

SummaryThe capacity of utilizing past experience to guide future action is a fundamental and conserved function of the nervous system. Associative memory formation initiated by the coincident detection of a conditioned stimulus (CS, e.g. odour) and an unconditioned stimulus (US, e.g. sugar reward) can lead to a short-lived memory trace (STM) within distinct circuits [1-5]. Memories can be consolidated into long-term memories (LTM) through processes that are not fully understood, but depend on de-novo protein synthesis [6, 7], require structural modifications within the involved neuronal circuits and might lead to the recruitment of additional ones [8-17]. Compared to modulation of existing connections, the reorganization of circuits affords the unique possibility of sampling for potential new partners [18-20]. Nonetheless, only few examples of rewiring associated with learning have been established thus far [14, 21-24]. Here, we report that memory consolidation is associated with the structural and functional reorganization of an identified circuit in the adult fly brain. The formation and retrieval of olfactory associative memories in Drosophila requires the mushroom body (MB) [25]. We identified the individual synapses of olfactory projection neurons (PNs) that deliver a conditioned odour to the MB and reconstructed the complexity of the microcircuit they form. Combining behavioural experiments with high-resolution microscopy and functional imaging, we demonstrated that the consolidation of appetitive olfactory memories closely correlates with an increase in the number of synaptic complexes formed by the PNs that deliver the conditioned stimulus and their postsynaptic partners. These structural changes result in additional functional synaptic connections.

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Olfactory Microcircuits in Drosophila Melanogaster

Handbook of Brain Microcircuits ◽

10.1093/med/9780190636111.003.0030 ◽

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).

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

Journal of Neurophysiology ◽

10.1152/jn.00397.2005 ◽

2005 ◽

Vol 94 (5) ◽

pp. 3303-3313 ◽

Cited By ~ 107

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.

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Connectomics analysis reveals first, second, and third order thermosensory and hygrosensory neurons in the adult Drosophila brain

10.1101/2020.01.20.912709 ◽

2020 ◽

Cited By ~ 4

Author(s):

Elizabeth C. Marin ◽

Ruairí J.V. Roberts ◽

Laurin Büld ◽

Maria Theiss ◽

Markus W. Pleijzier ◽

...

Keyword(s):

Circadian Clock ◽

Motor Neurons ◽

Mushroom Body ◽

Antennal Lobe ◽

Adult Brain ◽

Local Network ◽

Projection Neurons ◽

List Type ◽

Third Order ◽

Accessory Medulla

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

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Octopaminergic neurons have multiple targets in Drosophila larval mushroom body calyx and regulate behavioral odor discrimination

10.1101/295659 ◽

2018 ◽

Author(s):

J Y Hilary Wong ◽

Bo Angela Wan ◽

Tom Bland ◽

Marcella Montagnese ◽

Alex McLachlan ◽

...

Keyword(s):

Mushroom Body ◽

Inhibitory Neuron ◽

Odor Discrimination ◽

Learning Ability ◽

Projection Neurons ◽

Input Region ◽

Output Neurons ◽

Mushroom Body Calyx ◽

Intrinsic Neurons ◽

Selection Of

AbstractDiscrimination of sensory signals is essential for an organism to form and retrieve memories of relevance in a given behavioural context. Sensory representations are modified dynamically by changes in behavioral state, facilitating context-dependent selection of behavior, through signals carried by noradrenergic input in mammals, or octopamine (OA) in insects. To understand the circuit mechanisms of this signaling, we characterized the function of two OA neurons, sVUM1 neurons, that originate in the subesophageal zone (SEZ) and target the input region of the memory center, the mushroom body (MB) calyx, in larval Drosophila. We find that sVUM1 neurons target multiple neurons, including olfactory projection neurons (PNs), the inhibitory neuron APL, and a pair of extrinsic output neurons, but relatively few mushroom body intrinsic neurons, Kenyon cells. PN terminals carried the OA receptor Oamb, a Drosophila α1-adrenergic receptor ortholog. Using an odor discrimination learning paradigm, we showed that optogenetic activation of OA neurons compromised discrimination of similar odors but not learning ability. Our results suggest that sVUM1 neurons modify odor representations via multiple extrinsic inputs at the sensory input area to the MB olfactory learning circuit.

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