scholarly journals Compartment specific regulation of sleep by mushroom body requires GABA and dopaminergic signaling

2021 ◽  
Vol 11 (1) ◽  
Author(s):  
Margaret Driscoll ◽  
Steven N Buchert ◽  
Victoria Coleman ◽  
Morgan McLaughlin ◽  
Amanda Nguyen ◽  
...  

AbstractSleep is a fundamental behavioral state important for survival and is universal in animals with sufficiently complex nervous systems. As a highly conserved neurobehavioral state, sleep has been described in species ranging from jellyfish to humans. Biogenic amines like dopamine, serotonin and norepinephrine have been shown to be critical for sleep regulation across species but the precise circuit mechanisms underlying how amines control persistence of sleep, arousal and wakefulness remain unclear. The fruit fly, Drosophila melanogaster, provides a powerful model system for the study of sleep and circuit mechanisms underlying state transitions and persistence of states to meet the organisms motivational and cognitive needs. In Drosophila, two neuropils in the central brain, the mushroom body (MB) and the central complex (CX) have been shown to influence sleep homeostasis and receive aminergic neuromodulator input critical to sleep–wake switch. Dopamine neurons (DANs) are prevalent neuromodulator inputs to the MB but the mechanisms by which they interact with and regulate sleep- and wake-promoting neurons within MB are unknown. Here we investigate the role of subsets of PAM-DANs that signal wakefulness and project to wake-promoting compartments of the MB. We find that PAM-DANs are GABA responsive and require GABAA-Rdl receptor in regulating sleep. In mapping the pathways downstream of PAM neurons innervating γ5 and β′2 MB compartments we find that wakefulness is regulated by both DopR1 and DopR2 receptors in downstream Kenyon cells (KCs) and mushroom body output neurons (MBONs). Taken together, we have identified and characterized a dopamine modulated sleep microcircuit within the mushroom body that has previously been shown to convey information about positive and negative valence critical for memory formation. These studies will pave way for understanding how flies balance sleep, wakefulness and arousal.

Author(s):  
Margaret Driscoll ◽  
Steven Buchert ◽  
Victoria Coleman ◽  
Morgan McLaughlin ◽  
Amanda Nguyen ◽  
...  

AbstractNeural circuits involved in regulation of sleep play a critical role in sleep-wake transition and ability of an organism to engage in other behaviors critical for survival. The fruit fly, Drosophila melanogaster is a powerful system for the study of sleep and circuit mechanisms underlying sleep and co-regulation of sleep with other behaviors. In Drosophila, two neuropils in the central brain, mushroom body (MB) and central complex (CX) have been shown to influence sleep homeostasis and receive neuromodulator input critical to sleep-wake switch.Dopamine neurons (DANs) are the primary neuromodulator inputs to the MB but the mechanisms by which they regulate sleep- and wake-promoting neurons within MB are unknown. Here we investigate the role of subsets of DANs that signal wakefulness and project to wake-promoting compartments of the MB. We find that inhibition of specific subsets of PAM and PPL1 DANs projecting to the MB increase sleep in the presence of strong wake-inducing stimuli that reduces GABA transmission, although activity of these neurons is not directly modulated by GABA signaling. Of these subsets we find that DANs innervating the γ5 and β’2 MB compartments require both DopR1 and DopR2 receptors located in downstream Kenyon cells and mushroom body output neurons (MBONs). Further, we report that unlike the activity of wake-promoting MBONs and KCs, whose activity is modulated by sleep-need and PAM-DAN activity is independent of sleep-need. We have characterized a dopamine mediated sleep-circuit providing an inroad into understanding how common circuits within MB regulate sleep, wakefulness and behavioral arousal.


SLEEP ◽  
2021 ◽  
Author(s):  
Jelena Skorucak ◽  
Nathan Weber ◽  
Mary A Carskadon ◽  
Chelsea Reynolds ◽  
Scott Coussens ◽  
...  

Abstract The high prevalence of chronic sleep restriction in adolescents underscores the importance of understanding how adolescent sleep is regulated under such conditions. One component of sleep regulation is a homeostatic process: if sleep is restricted, then sleep intensity increases. Our knowledge of this process is primarily informed by total sleep deprivation studies and has been incorporated in mathematical models of human sleep regulation. Several animal studies, however, suggest that adaptation occurs in chronic sleep restriction conditions, showing an attenuated or even decreased homeostatic response. We investigated the homeostatic response of adolescents to different sleep opportunities. Thirty-four participants were allocated to one of three groups with 5, 7.5 or 10 h of sleep opportunity per night for 5 nights. Each group underwent a protocol of 9 nights designed to mimic a school week between 2 weekends: 2 baseline nights (10 h sleep opportunity), 5 condition nights (5, 7.5 or 10 h), and two recovery nights (10 h). Measures of sleep homeostasis (slow-wave activity and slow-wave energy) were calculated from frontal and central EEG derivations and compared to predictions derived from simulations of the homeostatic process of the two-process model of sleep regulation. Only minor differences were found between empirical data and model predictions, indicating that sleep homeostasis is preserved under chronic sleep restriction in adolescents. These findings improve our understanding of effects of repetitive short sleep in adolescents.


2021 ◽  
pp. 174702182110215
Author(s):  
Erick G. Chuquichambi Apaza ◽  
Guido B. Corradi ◽  
Enric Munar ◽  
Jaume Rosselló-Mir

Symmetry and contour take part in shaping visual preference. However, less is known about their combined contribution to preference. We examined the hedonic tone and preference triggered by the interaction of symmetry and contour. Symmetric/curved, symmetric/sharp-angled, asymmetric/curved, and asymmetric/sharp-angled stimuli were presented in an implicit and explicit task. The implicit task consisted of an affective stimulus-response compatibility task where participants matched the stimuli with positive and negative valence response cues. The explicit task recorded liking ratings from the same stimuli. We used instructed mindset to induce participants to focus on symmetry or contour in different parts of the experimental session. We found an implicit compatibility of symmetry and curvature with positive hedonic tone. Explicit results showed preference for symmetry and curvature. In both tasks, symmetry and curvature showed a cumulative interaction, with a larger contribution of symmetry to the overall effect. While symmetric and asymmetric stimuli contributed to the implicit positive valence of symmetry, the effect of curvature was mainly caused by inclination toward curved contours rather than rejection of sharp-angled contours. We did not find any correlation between implicit and explicit measures, suggesting that they may involve different cognitive processing.


2021 ◽  
Vol 11 (1) ◽  
Author(s):  
Chang Zhao ◽  
Yves F. Widmer ◽  
Sören Diegelmann ◽  
Mihai A. Petrovici ◽  
Simon G. Sprecher ◽  
...  

AbstractOlfactory learning and conditioning in the fruit fly is typically modelled by correlation-based associative synaptic plasticity. It was shown that the conditioning of an odor-evoked response by a shock depends on the connections from Kenyon cells (KC) to mushroom body output neurons (MBONs). Although on the behavioral level conditioning is recognized to be predictive, it remains unclear how MBONs form predictions of aversive or appetitive values (valences) of odors on the circuit level. We present behavioral experiments that are not well explained by associative plasticity between conditioned and unconditioned stimuli, and we suggest two alternative models for how predictions can be formed. In error-driven predictive plasticity, dopaminergic neurons (DANs) represent the error between the predictive odor value and the shock strength. In target-driven predictive plasticity, the DANs represent the target for the predictive MBON activity. Predictive plasticity in KC-to-MBON synapses can also explain trace-conditioning, the valence-dependent sign switch in plasticity, and the observed novelty-familiarity representation. The model offers a framework to dissect MBON circuits and interpret DAN activity during olfactory learning.


2021 ◽  
Vol 49 (12) ◽  
pp. 1-11
Author(s):  
Cheng Kang ◽  
Nan Ye ◽  
Fangwen Zhang ◽  
Yanwen Wu ◽  
Guichun Jin ◽  
...  

Although studies have investigated the influence of the emotionality of primes on the cross-modal affective priming effect, it is unclear whether this effect is due to the contribution of the arousal or the valence of primes. We explored how the valence and arousal of primes influenced the cross-modal affective priming effect. In Experiment 1 we manipulated the valence of primes (positive and negative) that were matched by arousal. In Experiments 2 and 3 we manipulated the arousal of primes under the conditions of positive and negative valence, respectively. Affective words were used as auditory primes and affective faces were used as visual targets in a priming task. The results suggest that the valence of primes modulated the cross-modal affective priming effect but that the arousal of primes did not influence the priming effect. Only when the priming stimuli were positive did the cross-modal affective priming effect occur, but negative primes did not produce a priming effect. In addition, for positive but not negative primes, the arousal of primes facilitated the processing of subsequent targets. Our findings have great significance for understanding the interaction of different modal affective information.


2021 ◽  
Author(s):  
Erick Gustavo Chuquichambi ◽  
Guido Corradi ◽  
Jaume Rossello ◽  
Enric Munar

Symmetry and contour take part in shaping visual preference. However, less is known about their combined contribution to preference. We examined the hedonic tone and preference triggered by the interaction of symmetry and contour. Symmetric/curved, symmetric/sharp-angled, asymmetric/curved, and asymmetric/sharp-angled stimuli were presented in an implicit and explicit task. The implicit task consisted of an affective stimulus-response compatibility task where participants matched the stimuli with positive and negative valence response cues. The explicit task recorded liking ratings from the same stimuli. We used instructed mindset to induce participants to focus on symmetry or contour in different parts of the experimental session. We found an implicit compatibility of symmetry and curvature with positive hedonic tone. Explicit results showed preference for symmetry and curvature. In both tasks, symmetry and curvature showed a cumulative interaction, with a larger contribution of symmetry to the overall effect. While symmetric and asymmetric stimuli contributed to the implicit positive valence of symmetry, the effect of curvature was mainly caused by inclination toward curved contours rather than rejection of sharp-angled contours. We did not find any correlation between implicit and explicit measures, suggesting that they may involve different cognitive processing.


2020 ◽  
Author(s):  
Jun Tomita ◽  
Gosuke Ban ◽  
Yoshiaki S. Kato ◽  
Kazuhiko Kume

AbstractThe central complex is one of the major brain regions that control sleep in Drosophila, but the circuitry details of sleep regulation have yet to be elucidated. Here, we show a novel sleep-regulating neuronal circuit in the protocerebral bridge (PB) of the central complex. Activation of the PB interneurons labeled by the R59E08-Gal4 and the PB columnar neurons in the R52B10-Gal4 promoted sleep and wakefulness, respectively. A targeted GFP reconstitution across synaptic partners (t-GRASP) analysis demonstrated synaptic contacts between these two groups of sleep-regulating PB neurons. Furthermore, we found that activation of a pair of dopaminergic (DA) neurons projecting to the PB (T1 DA neurons) decreased sleep. The wake-promoting T1 DA neurons and the sleep-promoting PB interneurons formed close associations. Dopamine 2-like receptor (Dop2R) knockdown in the sleep-promoting PB interneurons increased sleep. These results indicated that the neuronal circuit in the PB regulated by dopamine signaling mediates sleep-wakefulness.


Author(s):  
Cassie J. Hilditch ◽  
Erin E. Flynn-Evans

This chapter examines circadian rhythms and homeostatic mechanisms for sleep regulation. It reviews the current evidence describing the two-process model of sleep regulation and how to assess disruption to either of these sleep drives. This chapter also reviews the role of the photic and non-photic resetting of the circadian rhythm and describes how some aspects of modern society can cause sleep and circadian disruption. Further, this chapter describes how misalignment between the circadian rhythm and sleep homeostasis, such as occurs during jet lag and shift-work, can lead to sleep disruption. The short- and long-term consequences of circadian misalignment are also reviewed.


Sign in / Sign up

Export Citation Format

Share Document