Distribution of metabotropic receptors of serotonin, dopamine, GABA, glutamate, and short neuropeptide F in the central complex of Drosophila

Kahsai, Lily; Carlsson, Mikael A.; Winther, Åsa M.E.; Nässel, Dick R.

doi:10.1016/j.neuroscience.2012.02.007

Cited by 66 publications

(69 citation statements)

References 105 publications

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“…Drosophila DopR receptors reportedly correspond to the postsynaptic D1-receptor type in mammals (30) and mediate responses to environmental stressors (24) and ethanol-induced hyperactivity (22). These receptors are abundant on neuronal processes within the fan-shaped body, noduli, and ellipsoid body of the central complex, where they appear to be in close contact with TH-positive neurons (31). Our results also show close proximity between DopR immunostaining and the sites of presynaptic arbors of targeted PPM3 within the fan-shaped body and the noduli (Fig.…”

Section: Discussionmentioning

confidence: 99%

Single dopaminergic neurons that modulate aggression in Drosophila

Alekseyenko

Chan

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

152

150

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Monoamines, including dopamine (DA), have been linked to aggression in various species. However, the precise role or roles served by the amine in aggression have been difficult to define because dopaminergic systems influence many behaviors, and all can be altered by changing the function of dopaminergic neurons. In the fruit fly, with the powerful genetic tools available, small subsets of brain cells can be reliably manipulated, offering enormous advantages for exploration of how and where amine neurons fit into the circuits involved with aggression. By combining the GAL4/upstream activating sequence (UAS) binary system with the Flippase (FLP) recombination technique, we were able to restrict the numbers of targeted DA neurons down to a single-cell level. To explore the function of these individual dopaminergic neurons, we inactivated them with the tetanus toxin light chain, a genetically encoded inhibitor of neurotransmitter release, or activated them with dTrpA1, a temperature-sensitive cation channel. We found two sets of dopaminergic neurons that modulate aggression, one from the T1 cluster and another from the PPM3 cluster. Both activation and inactivation of these neurons resulted in an increase in aggression. We demonstrate that the presynaptic terminals of the identified T1 and PPM3 dopaminergic neurons project to different parts of the central complex, overlapping with the receptor fields of DD2R and DopR DA receptor subtypes, respectively. These data suggest that the two types of dopaminergic neurons may influence aggression through interactions in the central complex region of the brain involving two different DA receptor subtypes.A ggression is an innate behavior commonly used to obtain resources such as territories, mates, or food. Although some features of aggression are species-specific, broad similarities exist across species in the behavioral patterns and neurochemical systems involved (1, 2). Monoamines such as dopamine (DA) and serotonin have been linked to aggression in many species (3). Elaboration of the neural pathways that control aggression, however, has proven difficult because monoaminergic neurons also regulate other behaviors (1, 2). The pharmacological and genetic manipulations usually used for altering amine neuron function influence most of the neurons within a given monoaminergic population and thereby cause many behavioral changes. This makes it difficult to pinpoint the relationship between any particular amine-induced behavioral phenotype and an associated neuronal pathway.The fruit fly offers enormous advantages in these regards because existing powerful genetic methods permit manipulation of small subsets of brain cells for exploration of the neural mechanisms of behavior (4-6). In the Drosophila model of aggression (7,8), males fight and form stable hierarchical relationships. Using this model, we have shown that acute shutdown of serotonergic neurons yielded flies that could initiate fights but showed a reduced ability to escalate aggression. Activation of serotonergic ne...

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Section: Discussionmentioning

confidence: 99%

Single dopaminergic neurons that modulate aggression in Drosophila

Alekseyenko

Chan

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

152

150

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“…The following transgenic strains of Drosophila melanogaster were used for crosses: OK107-GAL4 (IV) (Connolly et al, 1996), MB247-GAL4 (III) (Zars et al, 2000), UAS-dicer2 (II) (Dietzl et al, 2007), UAS-sNPF-RNAi (X;II) (Lee et al, 2004), UAS-sNPF-RNAi (X), MB247-GAL80 (II) (Krashes et al, 2007), elav-GAL4 (X) (Lin and Goodman, 1994), UAS-sNPF (II;III) (Lee et al, 2004), UAS-sNPFR1-RNAi (III) (Hong et al, 2012), UAS-TrpA1 (II) (Hamada et al, 2008), NP3061-GAL4 (III) (Aso et al, 2009), andwhite (w 1118 ). UAS-dicer2 was used together with MB247-GAL4 in all knockdown experiments and respective control experiments.…”

Section: Methodsmentioning

confidence: 99%

“…Despite the importance of the MB, a functional neurotransmitter or neuromodulator produced by the Kenyon cells has not been conclusively identified in any insect. An immunohistochemical screen for candidate neuroactive substances identified the precursor for short neuropeptides F (sNPF) and its processed peptides in a majority of the Kenyon cells, both in larval and adult Drosophila Nässel et al, 2008). In most cases, neuropeptides act as neuromodulators (Nässel and Winther, 2010), but rarely as neurotransmitters in the strict sense.…”

Section: Introductionmentioning

confidence: 99%

Short Neuropeptide F Acts as a Functional Neuromodulator for Olfactory Memory in Kenyon Cells ofDrosophilaMushroom Bodies

et al. 2013

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In insects, many complex behaviors, including olfactory memory, are controlled by a paired brain structure, the so-called mushroom bodies (MB). In Drosophila, the development, neuroanatomy, and function of intrinsic neurons of the MB, the Kenyon cells, have been well characterized. Until now, several potential neurotransmitters or neuromodulators of Kenyon cells have been anatomically identified. However, whether these neuroactive substances of the Kenyon cells are functional has not been clarified yet. Here we show that a neuropeptide precursor gene encoding four types of short neuropeptide F (sNPF) is required in the Kenyon cells for appetitive olfactory memory. We found that activation of Kenyon cells by expressing a thermosensitive cation channel (dTrpA1) leads to a decrease in sNPF immunoreactivity in the MB lobes. Targeted expression of RNA interference against the sNPF precursor in Kenyon cells results in a highly significant knockdown of sNPF levels. This knockdown of sNPF in the Kenyon cells impairs sugar-rewarded olfactory memory. This impairment is not due to a defect in the reflexive sugar preference or odor response. Consistently, knockdown of sNPF receptors outside the MB causes deficits in appetitive memory. Altogether, these results suggest that sNPF is a functional neuromodulator released by Kenyon cells.

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“…Interestingly, a recent metaanalysis strongly suggests that the CX is deeply homologous to the mammalian basal ganglia (Strausfeld and Hirth, 2013). Moreover, the CX is heavily invested in GABAergic (inhibitory) receptors as well as receptors for numerous neuromodulators, including dopamine (Homberg et al, 1999;Kahsai and Winther, 2011;Kunst et al, 2011;Kahsai et al, 2012).…”

Section: Research Articlementioning

confidence: 99%

Encoding wide-field motion and direction in the central complex of the cockroach, Blaberous discoidalis

Kathman

Kesavan

Ritzmann

2014

Journal of Experimental Biology

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In the arthropod brain, the central complex (CX) receives various forms of sensory signals and is associated with motor functions, but its precise role in behavior is controversial. The optomotor response is a highly conserved turning behavior directed by visual motion. In tethered cockroaches, 20% procaine injected into the CX reversibly blocked this behavior. We then used multichannel extracellular recording to sample unit activity in the CX in response to wide-field visual motion stimuli, moving either horizontally or vertically at various temporal frequencies. For the 401 units we sampled, we identified five stereotyped response patterns: tonically inhibited or excited responses during motion, phasically inhibited or excited responses at the initiation of motion, and phasically excited responses at the termination of motion. Sixty-seven percent of the units responded to horizontal motion, while only 19% responded to vertical motion. Thirty-eight percent of responding units were directionally selective to horizontal motion. Response type and directional selectivity were sometimes conditional with other stimulus parameters, such as temporal frequency. For instance, 16% of the units that responded tonically to low temporal frequencies responded phasically to high temporal frequencies. In addition, we found that 26% of wide-field motion responding units showed a periodic response that was entrained to the temporal frequency of the stimulus. Our results show a diverse population of neurons within the CX that are variably tuned to wide-field motion parameters. Our behavioral data further suggest that such CX activity is required for effective optomotor responses.

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Distribution of metabotropic receptors of serotonin, dopamine, GABA, glutamate, and short neuropeptide F in the central complex of Drosophila

Cited by 66 publications

References 105 publications

Single dopaminergic neurons that modulate aggression in Drosophila

Single dopaminergic neurons that modulate aggression in Drosophila

Short Neuropeptide F Acts as a Functional Neuromodulator for Olfactory Memory in Kenyon Cells ofDrosophilaMushroom Bodies

Encoding wide-field motion and direction in the central complex of the cockroach, Blaberous discoidalis

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