Eight Different Types of Dopaminergic Neurons Innervate the Drosophila Mushroom Body Neuropil: Anatomical and Physiological Heterogeneity

By Zhengmei Mao, Ronald L. Davis. 2009

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We examined tyrosine hydroxylase (TH-GAL4) expression and anti-TH immunoreactivity in the Drosophila protocerebrum and characterized single cell clones of the TH-GAL4 neurons. Eight clusters of putative dopaminergic neurons were characterized. Neurons in three of the clusters project to the mushroom body neuropil: PAM neurons project to the medial portion of the horizontal lobes; PPL1 neurons project to the vertical lobes, the junction area, the heel and distal peduncle; and PPL2ab neurons project to the calyx. Five types of PPL1 neurons were discovered that innervate different zones of the mushroom body lobes. Functional imaging experiments showed that the dopaminergic processes in four of the zones differ in response properties to odor, electric shock, or following the pairing of odor and electric shock. These results indicate that distinct dopaminergic neurons define separate zones of the mushroom body lobes and are probably involved in different functions. Differences in functional response properties of these neurons suggest that they are involved in different behavioral processes.

Subfields: Cellular and Molecular Neuroscience, Ecology, Genetics

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Citations in the corpus

Dopaminergic neurons write and update memories with cell-type-specific rules (2016, background): “Punitive or rewarding stimuli such as electric shock, heat, cold, bitter taste and sugar generally activate a complex pattern of DANs (Riemensperger et al., 2005; Mao and Davis, 2009; ; Liu et al., 2012; Tomchik, 2013; Galili et al., 2014; Das et al., 2014; Kirkhart and Scott, 2015).”
Coordinated and Compartmentalized Neuromodulation Shapes Sensory Processing in Drosophila (2015, positive): “The mushroom body lobes are also richly innervated by dopaminergic neurons (DANs) thought to convey the contextual signals that impart meaning to an odor (Aso et al., 2012; Burke et al., 2012; Claridge-Chang et al., 2009; Liu et al., 2012; Mao and Davis, 2009; Waddell, 2013; Yamagata et al., 2015).”
The neuronal architecture of the mushroom body provides a logic for associative learning (2014, background): “These convergence zones are major sites of arborization for the dendrites of the DANs and axons of the MBONs.”
Layered reward signaling through octopamine and dopamine in Drosophila (2012, unknown): “Importantly, neither line labels DA neurons in the Paired Posterior Lateral 1 (PPL1) cluster that convey negative value 18,19,20 (Supplementary Fig.”
Different classes of input and output neurons reveal new features in microglomeruli of the adult Drosophila mushroom body calyx (2012, background): “…input also arises from octopamine-positive cells (Sinakevitch and Strausfeld, 2006; Busch et al., 2009) and possibly also from neurons that express other neurotransmitter systems, such as dopamine and serotonin (Roy et al., 2007; Johard et al., 2008; Tanaka et al., 2008; Mao and Davis, 2009).”
A Complete Electron Microscopy Volume of the Brain of Adult Drosophila melanogaster (2017, background): “Of the 15 cell types 337 known to arborize within the MB calyx (Aso et al., 2014; Burke et al., 2012; Busch et al., 2009; 338 Chen et al., 2012; de Haro et al., 2010; Mao and Davis, 2009; Roy et al., 2007; Tanaka et al., 339 2008), we found that a small subset contributes most of the postsynaptic ne”
A Higher Brain Circuit for Immediate Integration of Conflicting Sensory Information in Drosophila. (2015, background): “The MB lobes receive extensive modulatory inputs, especially by dopaminergic neurons of the protocerebral posterior lateral (PPL1) and the protocerebral anterior medial (PAM) cluster [16–19].”
The Drosophila Mushroom Body: From Architecture to Algorithm in a Learning Circuit. (2020, background): “The dopamine receptor as well as many signaling pathway components involved in learning have the KCs as their site of action (Davis 2005, Kim et al. 2007, Margulies et al. 2005, Qin et al. 2012).”
A genetically-encoded fluorescent sensor enables rapid and specific detection of dopamine in flies, fish, and mice (2018, background): “Thus, GRABDA sensors create new opportunities for exploring how specific compartments in the MB of the fly may exhibit distinct DA dynamics, which has been suggested by previous reports (Aso et al., 2014; Cognigni et al., 2018; Cohn et al., 2015; Mao and Davis, 2009).”
cAMP signalling in mushroom bodies modulates temperature preference behaviour in Drosophila (2008, background): “innervation profile in MB [27], we suspected that the dopamine system can modulate TPB in Drosophila.”
Episodic-like memory trace in awake replay of hippocampal place cell activity sequences (2015, methodology): “After spike sorting as previously described (Takahashi et al., 2003; Takahashi and Sakurai, 2009; Takahashi, 2013), putative principal cells were distinguished from putative fast-spiking cells based on spike width (0.”
Bruchpilot, A Synaptic Active Zone Protein for Anesthesia-Resistant Memory (2011, background): “This hypothesis may be tested in future by the identification of extrinsic neurons that are specifically required for ARM and corresponding functional imaging of memory traces (Yu et al., 2005; Mao and Davis, 2009; Tomchik and Davis, 2009; Gervasi et al., 2010).”
A neural circuit mechanism integrating motivational state with memory expression in Drosophila (2009, background): “Structural and Functional Subdivision of DA Neurons There are eight different morphological classes of DA neurons that innervate the MB (Mao and Davis, 2009), and our data imply functional subdivision.”