System-like consolidation of olfactory memories in Drosophila

By Isaac Cervantes-Sandoval, A. Martín-Peña, Jacob A. Berry, Ronald L. Davis. 2013

79 citations recorded by the source corpus.

System consolidation, as opposed to cellular consolidation, is defined as the relatively slow process of reorganizing the brain circuits that maintain long-term memory. This concept is founded in part on observations made in mammals that recently formed memories become progressively independent of brain regions initially involved in their acquisition and retrieval and dependent on other brain regions for their long-term storage. Here we present evidence that olfactory appetitive and aversive memories in Drosophila evolve using a system-like consolidation process. We show that all three classes of mushroom body neurons (MBNs) are involved in the retrieval of short- and intermediate-term memory. With the passage of time, memory retrieval becomes independent of α′/β′ and γ MBNs, and long-term memory becomes completely dependent on α/β MBNs. This shift in neuronal dependency for behavioral performance is paralleled by shifts in the activity of the relevant neurons during the retrieval of short-term versus long-term memories. Moreover, transient neuron inactivation experiments using flies trained to have both early and remote memories showed that the α′/β′ MBNs have a time-limited role in memory processing. These results argue that system consolidation is not a unique feature of the mammalian brain and memory systems, but rather a general and conserved feature of how different temporal memories are encoded from relatively simple to complex brains.

Subfields: Cellular and Molecular Neuroscience, Ecology, Genetics

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Citations in the corpus

Mushroom body output neurons encode valence and guide memory-based action selection in Drosophila (2014, background): “…our results indicate that circuits in the α lobe play key roles in long-term aversive and appetitive memory (Figure 10) (Pascual and Preat, 2001; Isabel et al., 2004; Yu et al., 2006; Blum et al., 2009; Sejourne et al., 2011; Cervantes-Sandoval et al., 2013; Pai et al., 2013; Placais et al., 2013).”
Origins of Cell-Type-Specific Olfactory Processing in the Drosophila Mushroom Body Circuit. (2017, unknown): “Moreover, genetic manipulations of KCs have suggested that olfactory memory is engraved in multiple lobes and specific sets of them are necessary for retrieving recent and remote memories (Blum et al., 2009; Cervantes-Sandoval et al., 2013; Krashes et al., 2007; Krashes and Waddell, 2008; Trannoy et”
A single pair of neurons links sleep to memory consolidation in Drosophila melanogaster (2015, background): “Elegant studies using conditional inhibition of transmitter release have provided a temporal ordering of transfer (Keene and Waddell, 2007; Cervantes-Sandoval et al., 2013; Dubnau and Chiang, 2013) leading to the idea that the role of DPM neurons is to facilitate the movement of memory from α’/β’ lo”
Activity of Defined Mushroom Body Output Neurons Underlies Learned Olfactory Behavior in Drosophila (2015, background): “Others have shown a role for a0b0 neuron output to retrieve earlier forms of memory (Wang et al., 2008; Cervantes-Sandoval et al., 2013).”
Shared mushroom body circuits underlie visual and olfactory memories in Drosophila (2014, unknown): “Interestingly, the contribution of the α′/β′ lobes is selective for olfactory memories (Figure 6; Krashes et al., 2007; Cervantes-Sandoval et al., 2013).”
Two pairs of mushroom body efferent neurons are required for appetitive long-term memory retrieval in Drosophila. (2013, result): “These data contradict the conclusion from a recent study claiming that appetitive training induces an increase in the CS+ response in the MB a lobes 24 hr after training (Cervantes-Sandoval et al., 2013).”
Two independent mushroom body output circuits retrieve the six discrete components of Drosophila aversive memory. (2015, methodology): “, 2008), and g (Cervantes-Sandoval et al., 2013) KCs.”
Reward signal in a recurrent circuit drives appetitive long-term memory formation (2015, unknown): “presumed to be modified in the course of memory formation by the reinforcing dopamine neurons (Tomchik and Davis, 2009; Gervasi et al., 2010; Sejourne et al., 2011; Cervantes-Sandoval et al., 2013; Placais et al., 2013; Boto et al., 2014).”