Specific octopaminergic neurons arbitrate between perseverance and reward in hungry Drosophila
In pursuit of palatable food, hungry animals mobilize significant energy resources and overcome obstacles, exhaustion and fear. Their perseverance depends on metabolic state, internal motivation and the expected benefit. Sustained commitment to a trying task is crucial, however, disengagement from one behavior to engage into another can be essential for optimal adaptation and survival. How neural circuits allow prioritizing perseverance over withdrawal based on the animals need is not understood. Using a single fly spherical treadmill, we show that hungry flies display increasing perseverance to track a food odor in the repeated absence of the predicted food reward. While this perseverance is mediated by a group of dopaminergic neurons, a subset of neurons expressing octopamine, the invertebrate counterpart of noradrenaline, provide reward feedback and counteract dopamine-motivated food seeking. Our data and modeling suggest that two important neuromodulators tally internal and external signals to coordinate motivation-dependent antagonistic behavioral drives: perseverance vs. change of behavior.\n\n\n\nO_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=87 SRC=\"FIGDIR/small/259119_ufig1.gif\" ALT=\"Figure 1\">\nView larger version (21K):\norg.highwire.dtl.DTLVardef@9833e1org.highwire.dtl.DTLVardef@7616d4org.highwire.dtl.DTLVardef@d4e8bforg.highwire.dtl.DTLVardef@1fc615c_HPS_FORMAT_FIGEXP M_FIG C_FIG HighlightsO_LILack of reward stimulates perseverance, and not quitting.\nC_LIO_LIDopaminergic neurons previously implicated in aversive learning promote perseverance.\nC_LIO_LISugar responsive octopaminergic neurons directly counteract perseverant odor tracking through a downstream inhibitory neuron.\nC_LIO_LIComputational modeling supports a simple neural circuit featuring antagonistic functions for dopamine and octopamine as tallies of expense and gain.\nC_LI