A neural circuit mechanism integrating motivational state with memory expression in Drosophila

By M. Krashes, Shamik DasGupta, Andrew P. Vreede, Ben White, J. Armstrong, S. Waddell. 2009

570 citations recorded by the source corpus.

Motivational states are important determinants of behavior. In fruit flies appetitive memory expression is constrained by satiety and promoted by hunger. Here we identify a neural mechanism that integrates the motivational state of hunger and memory. We show that stimulation of neurons that express Neuropeptide F (dNPF), an ortholog of mammalian NPY, mimicks food-deprivation and promotes memory performance in satiated flies. Robust appetitive memory performance requires the dNPF receptor in six dopaminergic neurons that innervate a distinct region of the mushroom bodies. Blocking these dopaminergic neurons releases memory performance in satiated flies whereas stimulation suppresses memory performance in hungry flies. Therefore dNPF and dopamine provide a motivational switch in the mushroom body that controls the output of appetitive memory.

Subfields: Cellular and Molecular Neuroscience, Genetics, Insect Science

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Citations in the corpus

Dopaminergic neurons write and update memories with cell-type-specific rules (2016, background): “DOI: 10.7554/eLife.16135.001”
Mushroom body output neurons encode valence and guide memory-based action selection in Drosophila (2014, background): “Other internal states, in addition to sleep, are likely to affect the decision to carry out a particular memory-guided behavior; for example, the state of satiety has been shown to regulate memory expression (Krashes et al., 2009).”
The neuronal architecture of the mushroom body provides a logic for associative learning (2014, background): “This bias is likely to reflect the combined effects of external experiences and the internal state of the fly (see accompanying paper) (Aso et al., 2014, Krashes et al., 2009; Bracker et al., 2013).”
Dopamine Is Required for Learning and Forgetting in Drosophila (2012, neutral): “, 2009), motivation (Wise, 2004; Krashes et al., 2009), decision making (Doya, 2008; Zhang et al.”
γ neurons mediate dopaminergic input during aversive olfactory memory formation in Drosophila (2012, unknown): “It is worth noting that DA inputs to MBs also have been implicated in hunger/satiety modulation of appetitive memory retrieval [7, 33], and DopR signaling also has been implicated in several forms of arousal [47] that in principle could represent a component of the reinforcement signal that could be”
Cell Type-Specific Transcriptome Analysis in the Drosophila Mushroom Body Reveals Memory-Related Changes in Gene Expression (2016, unknown): “Thus, these data suggest a mechanism for the established relationships between memory formation and circadian or feeding rhythms (Joiner et al., 2006; Krashes et al., 2009).”
Insects have the capacity for subjective experience (2016, background): “These specialized circuits modify how the insect responds to events according to its subjective internal state such as arousal, sleep, satiation, hunger, and reward (Andretic et al., 2005; Burke et al., 2012; Krashes et al., 2009; Liu, Liu, Kodama, Driscoll, & Wu, 2012; Søvik et al., 2015).”
Short neuropeptide F is a sleep-promoting inhibitory modulator (2013, background): “Dopaminergic neu- rons have also been shown to be a critical part of NPF-regulated changes in satiety and response to food (Inagaki et al., 2012; Krashes et al., 2009), and activation of these neurons indeed led to an immediate onset of food dwelling, which reversed rapidly upon dTRPA1 inactivation…”
Drosophila Learn Opposing Components of a Compound Food Stimulus (2014, methodology): “To test whether either of these neurons were required for DEET learning, we expressed the dominant temperature-sensitive UAS-shibirets1 transgene [22] in MP1, MV1, and M3 neurons using the c061; MBGAL80, R73F07, and NP5272 and NP1528 GAL4 drivers [7, 23, 24], respectively.”
Do the right thing: neural network mechanisms of memory formation, expression and update in Drosophila (2018, background): “By re-routing information throughout the MBON network, the mushroom body can therefore integrate context and internal state with sensory stimuli to direct the most appropriate behavior [21,56].”
Heterosynaptic plasticity underlies aversive olfactory learning in Drosophila (2015, unknown): “This matches well with the picture developed from recent behavioral studies indicating the different compartments are related to distinct motivational drives (Burke et al., 2012; Huetteroth et al., 2015; Krashes et al., 2009; Lin et al., 2014b; Liu et al., 2012; Musso et al., 2015; Yamagata et al., ”
The Biology of Forgetting – A Perspective (2017, background): “However, the designation of at least a subset of DAn as forgetting cells should not be construed to mean that spurring the process of forgetting is their sole function, just as engram cells and other neurons in the central nervous system have multiple functions (Muller et al., 1987; Krashes et al., ”
cAMP signalling in mushroom bodies modulates temperature preference behaviour in Drosophila (2008, background): “For example, protocerebral posterior lateral 1 cluster which innervates MB is reported as routes for reinforcement and retrieval in memory formation [28,29].”
Three Dopamine Pathways Induce Aversive Odor Memories with Different Stability (2012, background): “ory, some of which are mapped in the MB [17,21,24,26,27,28,29].”
Drosophila ORB protein in two mushroom body output neurons is necessary for long-term memory formation (2013, background): “During olfactory conditioning, an odor CS signal is encoded in sparse subsets of MB neurons (31), whereas the aversive US signal is delivered to most, if not all, Kenyon cells via dopaminergic neurons (29, 32, 33).”
A Higher Brain Circuit for Immediate Integration of Conflicting Sensory Information in Drosophila. (2015, background): “Receiving input from multiple sensory modalities and behavioral state [38, 41, 44–48], the MB could be this higher processing center in insects.”
A single pair of neurons links sleep to memory consolidation in Drosophila melanogaster (2015, background): “, 2002; Sakai and Kitamoto, 2006), or more generally during the integration of internal and external cues and decision making (Zhang et al., 2007; Neckameyer and Matsuo, 2008; Krashes et al., 2009; Donlea et al., 2012; Bracker et al., 2013).”