Two Different Forms of Arousal in Drosophila Are Oppositely Regulated by the Dopamine D1 Receptor Ortholog DopR via Distinct Neural Circuits

Lebestky, Tim; Chang, Jung Sook C; Dankert, H.; Zelnik, Lihi; Kim, Young-Cho; Han, Kuo; Wolf, Fred W.; Perona, Pietro; Anderson, David J.

doi:10.1016/j.neuron.2009.09.031

Cited by 243 publications

(322 citation statements)

References 83 publications

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“…Direct evidence for sleep/wake changes in the brain levels of any of these neurotransmitters is missing in flies. However, both dopamine (42,43) and octopamine (44,45) promote arousal, although they do so by affecting brain regions other than the MBs (43)(44)(45). Moreover, both dopamine and octopamine modulate calcium and cAMP levels (46) in response to cholinergic inputs and play an important role in modulating MB neuronal activity during associative olfactory learning (47)(48)(49)(50), suggesting that they could affect the excitability of Kenyon cells.…”

Section: Discussionmentioning

confidence: 99%

Sleep- and wake-dependent changes in neuronal activity and reactivity demonstrated in fly neurons using in vivo calcium imaging

Bushey

Tononi

Cirelli

2015

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

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Sleep in Drosophila shares many features with mammalian sleep, but it remains unknown whether spontaneous and evoked activity of individual neurons change with the sleep/wake cycle in flies as they do in mammals. Here we used calcium imaging to assess how the Kenyon cells in the fly mushroom bodies change their activity and reactivity to stimuli during sleep, wake, and after short or long sleep deprivation. As before, sleep was defined as a period of immobility of >5 min associated with a reduced behavioral response to a stimulus. We found that calcium levels in Kenyon cells decline when flies fall asleep and increase when they wake up. Moreover, calcium transients in response to two different stimuli are larger in awake flies than in sleeping flies. The activity of Kenyon cells is also affected by sleep/wake history: in awake flies, more cells are spontaneously active and responding to stimuli if the last several hours (5-8 h) before imaging were spent awake rather than asleep. By contrast, long wake (≥29 h) reduces both baseline and evoked neural activity and decreases the ability of neurons to respond consistently to the same repeated stimulus. The latter finding may underlie some of the negative effects of sleep deprivation on cognitive performance and is consistent with the occurrence of local sleep during wake as described in behaving rats. Thus, calcium imaging uncovers new similarities between fly and mammalian sleep: fly neurons are more active and reactive in wake than in sleep, and their activity tracks sleep/wake history.T he fundamental features that characterize mammalian sleep also define Drosophila melanogaster sleep (1-3). Most crucially, in both flies and mammals, sleep is distinguished from simple rest (quiet wake) by an increased arousal threshold, i.e., a reduced ability to respond to external stimuli. Moreover, in flies and mammals sleep is controlled homeostatically by the duration as well by the intensity of prior wake, suggesting basic similarities in the mechanisms of sleep regulation across species. Thus, in flies both sleep deprivation and a rich learning experience lead to a sleep rebound characterized by overall increased sleep time, increased arousal threshold, and longer sleep episodes (4-6). As in mammals, overall neuronal activity in flies is also high during wake and low during sleep (6-8). Specifically, a seminal study using local field potential (LFP) recordings from the Drosophila medial protocerebrum found high spike-like potentials that disappeared after the block of synaptic transmission in the mushroom bodies (MBs) (7). This high spike activity was present when flies were moving or had been quiescent for only a few seconds, but disappeared with sleep (i.e., after periods of immobility >5 min), when the overall LFP power in all frequencies also decreased by ∼60% (7). The study concluded that neural activity in the sleeping fly brain, or at least in a central region spanning the MBs, resembles that seen in mammals in several brainstem cell groups including noradrenergic ne...

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Section: Discussionmentioning

confidence: 99%

Sleep- and wake-dependent changes in neuronal activity and reactivity demonstrated in fly neurons using in vivo calcium imaging

Bushey

Tononi

Cirelli

2015

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

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“…Each air puff (35 psi) lasted 200 msec with a 5-sec interpuff interval. Movies were analyzed using custom locomotor tracking software (described in Lebestky et al 2009). …”

Section: Negative Geotaxismentioning

confidence: 99%

“…The dVMAT mutant has altered startle-induced activity Dopamine has been previously implicated in arousal and startle responsiveness in Drosophila (Kume et al 2005;Lebestky et al 2009). Although there are no reports on the role of other amines in the Drosophila startle response per se, OA has been suggested to increase arousal and mediate the fight-or-flight response in other insects (Adamo et al 1995;Bacon et al 1995;Stern 1999;Rind et al 2008).…”

Section: Dopamine and Octopamine Play Complementary Or Redundant Rolementioning

confidence: 99%

“…To further assess the role of OA and other amines in startle-induced locomotion, we utilized a previously described repetitive startle assay (the puff-o-mat), which allows quantification of parameters and phases within the startle response (Lebestky et al 2009). In response to air puffs, WT controls increase locomotor speed within seconds and then gradually return to a less active state in a response profile that can be characterized by a single exponential (Lebestky et al 2009).…”

Section: Dopamine and Octopamine Play Complementary Or Redundant Rolementioning

confidence: 99%

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Dispensable, Redundant, Complementary, and Cooperative Roles of Dopamine, Octopamine, and Serotonin inDrosophila melanogaster

Chen

Lebestky

et al. 2013

Genetics

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To investigate the regulation of Drosophila melanogaster behavior by biogenic amines, we have exploited the broad requirement of the vesicular monoamine transporter (VMAT) for the vesicular storage and exocytotic release of all monoamine neurotransmitters. We used the Drosophila VMAT (dVMAT) null mutant to globally ablate exocytotic amine release and then restored DVMAT activity in either individual or multiple aminergic systems, using transgenic rescue techniques. We find that larval survival, larval locomotion, and female fertility rely predominantly on octopaminergic circuits with little apparent input from the vesicular release of serotonin or dopamine. In contrast, male courtship and fertility can be rescued by expressing DVMAT in octopaminergic or dopaminergic neurons, suggesting potentially redundant circuits. Rescue of major aspects of adult locomotion and startle behavior required octopamine, but a complementary role was observed for serotonin. Interestingly, adult circadian behavior could not be rescued by expression of DVMAT in a single subtype of aminergic neurons, but required at least two systems, suggesting the possibility of unexpected cooperative interactions. Further experiments using this model will help determine how multiple aminergic systems may contribute to the regulation of other behaviors. Our data also highlight potential differences between behaviors regulated by standard exocytotic release and those regulated by other mechanisms. BOTH invertebrate and mammalian behaviors undergo extensive regulation by monoamine neurotransmitters (reviewed in Joshua et al.

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“…These data suggest that DTK FruM neurons promote a state of arousal or motivation that is apparently aggression-specific. Our previous work has provided evidence of other behaviorspecific forms of arousal in Drosophila (Lebestky et al 2009). …”

Section: A Neuron and A Neuropeptide That Control Aggressive Arousalmentioning

confidence: 98%

Internal States and Behavioral Decision-Making: Toward an Integration of Emotion and Cognition

Kennedy

Asahina²,

Hoopfer

et al. 2014

Cold Spring Harb Symp Quant Biol

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Social interactions, such as an aggressive encounter between two conspecific males or a mating encounter between a male and a female, typically progress from an initial appetitive or motivational phase, to a final consummatory phase. This progression involves both changes in the intensity of the animals' internal state of arousal or motivation and sequential changes in their behavior. How are these internal states, and their escalating intensity, encoded in the brain? Does this escalation drive the progression from the appetitive/motivational to the consummatory phase of a social interaction and, if so, how are appropriate behaviors chosen during this progression? Recent work on social behaviors in flies and mice suggests possible ways in which changes in internal state intensity during a social encounter may be encoded and coupled to appropriate behavioral decisions at appropriate phases of the interaction. These studies may have relevance to understanding how emotion states influence cognitive behavioral decisions at higher levels of brain function.

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Two Different Forms of Arousal in Drosophila Are Oppositely Regulated by the Dopamine D1 Receptor Ortholog DopR via Distinct Neural Circuits

Cited by 243 publications

References 83 publications

Sleep- and wake-dependent changes in neuronal activity and reactivity demonstrated in fly neurons using in vivo calcium imaging

Sleep- and wake-dependent changes in neuronal activity and reactivity demonstrated in fly neurons using in vivo calcium imaging

Dispensable, Redundant, Complementary, and Cooperative Roles of Dopamine, Octopamine, and Serotonin inDrosophila melanogaster

Internal States and Behavioral Decision-Making: Toward an Integration of Emotion and Cognition

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