A Late-Phase, Long-Term Memory Trace Forms in the γ Neurons of Drosophila Mushroom Bodies after Olfactory Classical Conditioning

By D. Akalal, Dinghui Yu, Ronald L. Davis. 2010

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Using functional optical imaging in vivo, we demonstrate that the γ mushroom body (MB) neurons of Drosophila melanogaster respond with axonal calcium influx when odors or electric shock stimuli are presented to the fly. Pairing of odor and electric shock stimuli in a single training trial or multiple, massed training trials failed to modify the odor-evoked calcium signal when flies were tested at several different times after training. In contrast, animals that received multiple but spaced odor–shock pairings exhibited a robust increase in calcium influx into the MB axons when tested between 18 and 48 h after training. This time window for the γ neuron memory trace is displaced relative to the modifications that occur between 9 and 24 h after training in the α branch of the α/β MB neurons. The α/β and the γ neuron long-term memory traces were both blocked by expressing a repressor of the transcription factor cAMP response element-binding protein or a calcium/calmodulin-dependent kinase II hairpin RNA. These results demonstrate that behavioral long-term olfactory memory is encoded as modifications of calcium influx into distinct MB neurons during overlapping but different windows of time after training.

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): “…from those responsible for memories with shorter retention times (Yin et al., 1994; Pascual and Preat, 2001; Dubnau et al., 2003; Comas et al., 2004; Isabel et al., 2004; Yu et al., 2006; Blum et al., 2009; Akalal et al., 2010, 2011; Trannoy et al., 2011; Huang et al., 2012; Placais et al., 2012).”
Different Kenyon Cell Populations Drive Learned Approach and Avoidance in Drosophila (2013, background): “…the ab, a0b0, and g classes of MB neuron has been reported (Crittenden et al., 1998; Zars et al., 2000; Yu et al., 2006; Krashes et al., 2007; Wang et al., 2008; Akalal et al., 2010; Trannoy et al., 2011; Qin et al., 2012; Tanaka et al., 2008), until now a valence-restricted role has been elusive.”
Are mushroom bodies cerebellum-like structures? (2011, background): “…bodies through rutabaga adenylyl cyclase activation potentiates Ca2þ influx in Kenyon cells in response to stimulation (Yu et al., 2006; Tomchik and Davis, 2009; Akalal et al., 2010), although a causal link to LTP-like synaptic plasticity in Kenyon cells remains to be demonstrated.”
Drosophila ORB protein in two mushroom body output neurons is necessary for long-term memory formation (2013, background): “LTM formation requires the transcription factor, CREB, and the N-methyl-D-aspartate (NMDA) receptor in many animals, includingDrosophila (12, 14, 26).”
Heterosynaptic plasticity underlies aversive olfactory learning in Drosophila (2015, unknown): “While odor-evoked calcium signals increase in KC axons (Akalal et al., 2010, 2011; Boto et al., 2014; Tomchik and Davis, 2009; Wang et al., 2008; Yu et al., 2006, but see Zhang and Roman, 2013), signals in MBONs decrease in some cases (Owald et al., 2015; Séjourné et al., 2011) and increase in…”
Spaced Training Forms Complementary Long-Term Memories of Opposite Valence in Drosophila (2019, unknown): “However, γ and α′β′ KCs have also been implicated in LTM, either directly or by virtue of a requirement for downstream MBONs, such as MBON-γ3, MBON-γ3β′1 and MBON-M4β′2mp (Akalal et al., 2010; Wu et al., 2017).”
The Long-Term Memory Trace Formed in the Drosophilaα/β Mushroom Body Neurons is abolished in Long-Term Memory Mutants (2011, background): “(5) The LTM trace requires the normal activity of calcium/calmodulin-dependent protein kinase II (CaMKII) (disrupted by an RNA hairpin to CaMKII mRNA), like long-term behavioral memory (Akalal et al., 2010).”