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

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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Synaptic organization of the mushroom body calyx inDrosophila melanogaster

The Journal of Comparative Neurology ◽

10.1002/cne.10155 ◽

2002 ◽

Vol 445 (3) ◽

pp. 211-226 ◽

Cited By ~ 194

Author(s):

Kouji Yasuyama ◽

Ian A. Meinertzhagen ◽

Friedrich-Wilhelm Schürmann

Keyword(s):

Mushroom Body ◽

Synaptic Organization ◽

Mushroom Body Calyx

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Cumulative Effects of Foraging Behavior and Social Dominance on Brain Development in a Facultatively Social Bee (Ceratina australensis)

Brain Behavior and Evolution ◽

10.1159/000381414 ◽

2015 ◽

Vol 85 (2) ◽

pp. 117-124 ◽

Cited By ~ 11

Author(s):

Sandra M. Rehan ◽

Susan J. Bulova ◽

Sean O''Donnell

Keyword(s):

Brain Development ◽

Task Performance ◽

Mushroom Body ◽

Cumulative Effects ◽

Body Volume ◽

Total Brain Volume ◽

Carpenter Bee ◽

The Social ◽

Foraging Experience ◽

Mushroom Body Calyx

In social insects, both task performance (foraging) and dominance are associated with increased brain investment, particularly in the mushroom bodies. Whether and how these factors interact is unknown. Here we present data on a system where task performance and social behavior can be analyzed simultaneously: the small carpenter bee Ceratina australensis. We show that foraging and dominance have separate and combined cumulative effects on mushroom body calyx investment. Female C. australensis nest solitarily and socially in the same populations at the same time. Social colonies comprise two sisters: the social primary, which monopolizes foraging and reproduction, and the social secondary, which is neither a forager nor reproductive but rather remains at the nest as a guard. We compare the brains of solitary females that forage and reproduce but do not engage in social interactions with those of social individuals while controlling for age, reproductive status, and foraging experience. Mushroom body calyx volume was positively correlated with wing wear, a proxy for foraging experience. We also found that, although total brain volume did not vary among reproductive strategies (solitary vs. social nesters), socially dominant primaries had larger mushroom body calyx volumes (corrected for both brain and body size variation) than solitary females; socially subordinate secondaries (that are neither dominant nor foragers) had the least-developed mushroom body calyces. These data demonstrate that sociality itself does not explain mushroom body volume; however, achieving and maintaining dominance status in a group was associated with mushroom body calyx enlargement. Dominance and foraging effects were cumulative; dominant social primary foragers had larger mushroom body volumes than solitary foragers, and solitary foragers had larger mushroom body volumes than nonforaging social secondary guards. This is the first evidence for cumulative effects on brain development by dominance and task performance.

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3P-234 Conditioning-dependent calcium signals within the mushroom body calyx in the cricket(The 46th Annual Meeting of the Biophysical Society of Japan)

Seibutsu Butsuri ◽

10.2142/biophys.48.s163_6 ◽

2008 ◽

Vol 48 (supplement) ◽

pp. S163

Author(s):

Hiroto Ogawa ◽

Kotaro Oka

Keyword(s):

Annual Meeting ◽

Mushroom Body ◽

Calcium Signals ◽

Biophysical Society ◽

Mushroom Body Calyx

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Circuit reorganization in the Drosophila mushroom body calyx accompanies memory consolidation

10.1101/2020.08.20.259135 ◽

2020 ◽

Author(s):

Lothar Baltruschat ◽

Philipp Ranft ◽

Luigi Prisco ◽

J. Scott Lauritzen ◽

André Fiala ◽

...

Keyword(s):

Conditioned Stimulus ◽

Memory Consolidation ◽

Mushroom Body ◽

Structural Changes ◽

De Novo ◽

Projection Neurons ◽

Structural Modifications ◽

Behavioural Experiments ◽

The Individual ◽

Mushroom Body Calyx

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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