Abstract
Animals can form associations between temporally separated stimuli. To do so, the nervous system has to retain a neural representation of the first stimulus until the second stimulus appears. The neural substrate of such sensory stimulus memories is unknown. Here, we search for a sensory odor memory in the insect olfactory system and characterize odorant-evoked Ca2+ activity at three consecutive layers of the olfactory system in Drosophila: in olfactory receptor neurons (ORNs) and projection neurons (PNs) in the antennal lobe, and in Kenyon cells (KCs) in the mushroom body. We show that the post-stimulus responses in ORN axons, PN dendrites, PN somata, and KC dendrites are odor-specific, but they are not predictive of the chemical identity of past olfactory stimuli. However, the post-stimulus responses in KC somata carry information about the identity of previous olfactory stimuli. These findings show that the Ca2+ dynamics in KC somata could encode a sensory memory of odorant identity and thus might serve as a basis for associations between temporally separated stimuli.
Highlights
Odorants evoke odorant-specific spiking patterns across olfactory receptor neurons (ORNs), which drive odorant-specific neural activity patterns in different brain areas
We categorized Ca2+ responses according to their response dynamics, forming three threshold-based categories: on, off, or prolonged (Figure 2C, see methods for details on the construction of thresholds used for categorization)
The post-odor response pattern already developed during the odorant stimulation (Figure 6B, blue trace). This pattern remained correlated to the odor response pattern for at least 20 s after odorant offset, i.e., for a behaviorally relevant time scale (Galili et al, 2011). These results indicated that Ca2+ activity in Kenyon cells (KCs) dendrites and even more in KC somata had an elevated similarity between odor and post-odor response pattern
Summary
Odorants evoke odorant-specific spiking patterns across olfactory receptor neurons (ORNs), which drive odorant-specific neural activity patterns in different brain areas. Odorants evoke activity first across ORNs in the olfactory epithelium and in glomeruli in the olfactory bulb, followed by responses in the olfactory cortex, the amygdala, and other brain areas (Uchida et al, 2014). In insects, activity across ORNs first drives responses in olfactory glomeruli in the antennal lobe, and later in higher brain regions such as the mushroom bodies (Galizia, 2014). Activity (e.g., membrane potential or changes in cytosolic Ca2+ concentration) in the dendrite is often different from activity in axon terminals. Ca2+ has multiple functions: in presynaptic terminals Ca2+ triggers vesicle release (Stanley, 1997); at post-synaptic sites Ca2+ is involved in long-term synaptic
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