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Mushroom body output neurons MBON-a1/a2 define an odor intensity channel that regulates behavioral odor discrimination learning in larval Drosophila.

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Mohamed, Abdulkadir 
Malekou, Iro 
Sim, Timothy 
O'Kane, Cahir J 
Maait, Yousef 


The sensitivity of animals to sensory input must be regulated to ensure that signals are detected and also discriminable. However, how circuits regulate the dynamic range of sensitivity to sensory stimuli is not well understood. A given odor is represented in the insect mushroom bodies (MBs) by sparse combinatorial coding by Kenyon cells (KCs), forming an odor quality representation. To address how intensity of sensory stimuli is processed at the level of the MB input region, the calyx, we characterized a set of novel mushroom body output neurons that respond preferentially to high odor concentrations. We show that a pair of MB calyx output neurons, MBON-a1/2, are postsynaptic in the MB calyx, where they receive extensive synaptic inputs from KC dendrites, the inhibitory feedback neuron APL, and octopaminergic sVUM1 neurons, but relatively few inputs from projection neurons. This pattern is broadly consistent in the third-instar larva as well as in the first instar connectome. MBON-a1/a2 presynaptic terminals innervate a region immediately surrounding the MB medial lobe output region in the ipsilateral and contralateral brain hemispheres. By monitoring calcium activity using jRCamP1b, we find that MBON-a1/a2 responses are odor-concentration dependent, responding only to ethyl acetate (EA) concentrations higher than a 200-fold dilution, in contrast to MB neurons which are more concentration-invariant and respond to EA dilutions as low as 10-4. Optogenetic activation of the calyx-innervating sVUM1 modulatory neurons originating in the SEZ (Subesophageal zone), did not show a detectable effect on MBON-a1/a2 odor responses. Optogenetic activation of MBON-a1/a2 using CsChrimson impaired odor discrimination learning compared to controls. We propose that MBON-a1/a2 form an output channel of the calyx, summing convergent sensory and modulatory input, firing preferentially to high odor concentration, and might affect the activity of downstream MB targets.


Peer reviewed: True

Acknowledgements: We thank M. Morgan for help in building the optogenetic behavioural apparatus, and Alex McLachlan for technical support. We thank Scott Waddell, Tzumin Lee, Andrew Lin, Kristin Scott and especially the Bloomington Drosophila Stock Center for fly stocks, and the Developmental Studies Hybridoma Bank for antibodies. YM and BS were supported by summer research bursaries from Magdalene College of the University of Cambridge. The work was partly supported by BBSRC grant BB/N007948/1 to LMM-N and CJO′K. We thank the Department of Genetics, University of Cambridge, for infrastructural support for LMM-N.


MBONs, calyx, intensity coding, mushroom bodies, odor discrimination learning

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Front Physiol

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Frontiers Media SA
Biotechnology and Biological Sciences Research Council (BB/N007948/1)
BBSRC grant BB/N007948/1 to LMM-N and CJO'K. YM and BS were supported by summer research bursaries from Magdalene College of the University of Cambridge.