Sweet taste and nutrient value subdivide rewarding dopaminergic neurons in Drosophila.
Dopaminergic neurons provide reward learning signals in mammals and insects [1-4]. Recent work in Drosophila has demonstrated that water-reinforcing dopaminergic neurons are different to those for nutritious sugars [5]. Here, we tested whether the sweet taste and nutrient properties of sugar reinforcement further subdivide the fly reward system. We found that dopaminergic neurons expressing the OAMB octopamine receptor [6] specifically convey the short-term reinforcing effects of sweet taste [4]. These dopaminergic neurons project to the β'2 and γ4 regions of the mushroom body lobes. In contrast, nutrient-dependent long-term memory requires different dopaminergic neurons that project to the γ5b regions, and it can be artificially reinforced by those projecting to the β lobe and adjacent α1 region. Surprisingly, whereas artificial implantation and expression of short-term memory occur in satiated flies, formation and expression of artificial long-term memory require flies to be hungry. These studies suggest that short-term and long-term sugar memories have different physiological constraints. They also demonstrate further functional heterogeneity within the rewarding dopaminergic neuron population.
Centre for Neural Circuits and Behaviour, The University of Oxford, Tinsley Building, Mansfield Road, Oxford OX1 3SR, UK; Zukunftskolleg, University of Konstanz, Universitätsstraße 10, 78457 Konstanz, Germany.
Wolf
W
Huetteroth
Centre for Neural Circuits and Behaviour, The University of Oxford, Tinsley Building, Mansfield Road, Oxford OX1 3SR, UK.
Emmanuel
E
Perisse
Centre for Neural Circuits and Behaviour, The University of Oxford, Tinsley Building, Mansfield Road, Oxford OX1 3SR, UK.
Suewei
S
Lin
Centre for Neural Circuits and Behaviour, The University of Oxford, Tinsley Building, Mansfield Road, Oxford OX1 3SR, UK; Laboratorio de Neurobiología de la Memoria, Departamento de Fisiología y Biología Molecular y Celular, IFIBYNE-CONICET, Pabellón II, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires C1428EGA, Argentina.
Martín
M
Klappenbach
Centre for Neural Circuits and Behaviour, The University of Oxford, Tinsley Building, Mansfield Road, Oxford OX1 3SR, UK.
Christopher
C
Burke
Centre for Neural Circuits and Behaviour, The University of Oxford, Tinsley Building, Mansfield Road, Oxford OX1 3SR, UK. Electronic address: scott.waddell@cncb.ox.ac.uk.
Scott
S
Waddell
D000818:Animals; D030801:Animals, Genetically Modified; D001070:Appetitive Behavior / Q000502:physiology; D059290:Dopaminergic Neurons / Q000502:physiology*; D029721:Drosophila Proteins / Q000235:genetics / Q000502:physiology; D004331:Drosophila melanogaster / Q000166:cytology / Q000235:genetics / Q000502:physiology*; D005260:Female; D008297:Male; D057567:Memory, Long-Term / Q000502:physiology; D008570:Memory, Short-Term / Q000502:physiology; D024521:Mushroom Bodies / Q000166:cytology / Q000502:physiology; D009154:Mutation; D009753:Nutritive Value; D017981:Receptors, Neurotransmitter / Q000235:genetics / Q000502:physiology; D012054:Reinforcement, Psychology; D012201:Reward; D013649:Taste / Q000502:physiology*
D029721:Drosophila Proteins; C480734:OAMB protein, Drosophila; D017981:Receptors, Neurotransmitter