Abstract
The olfactory system encodes odor stimuli as combinatorial activity of populations of neurons whose response depends on stimulus history. How and on which timescales previous stimuli affect these combinatorial representations remains unclear. We use in vivo optical imaging in Drosophila to analyze sensory adaptation at the first synaptic step along the olfactory pathway. We show that calcium signals in the axon terminals of olfactory receptor neurons (ORNs) do not follow the same adaptive properties as the firing activity measured at the antenna. While ORNs calcium responses are sustained on long timescales, calcium signals in the postsynaptic projection neurons (PNs) adapt within tens of seconds. We propose that this slow component of the postsynaptic response is mediated by a slow presynaptic depression of vesicle release and enables the combinatorial population activity of PNs to adjust to the mean and variance of fluctuating odor stimuli.
Highlights
Internal sensory representations can carry information about both the identity of an object and its location in space
From previous analysis of olfactory receptor neurons (ORNs) spiking activity, we expected that calcium signals measured at the ORN axon terminals would decrease over time when a sustained flickering stimulus is applied (Martelli et al, 2013)
Calcium onset is faster in projection neurons (PNs) than ORNs, as previously shown in measurements of the firing rate (Bhandawat et al, 2007), and LNs show even more transient dynamics with a larger decrease in activity during a single odor pulse (Nagel and Wilson, 2016)
Summary
Internal sensory representations can carry information about both the identity of an object and its location in space. To demonstrate that this property of the calcium dynamics cannot be explained by the sensor kinetics, we have convolved the firing rate with a linear filter modeling the kinetics of the sensors (Schnell et al, 2014)(Figure 3F) For both GCaMP3 and GCaMP6f, the model predicts a decrease in activity during background presentation and a lower response to the odor pulse. We could conclude that calcium in axonal terminals encodes the actual stimulus concentration rather than the change in concentration This is not the case when the test pulse is lower than the background: in this case the calcium response becomes lower than in the non-adapted condition (Figure 3G, orange). We conclude that glomerular calcium responses do not reflect adaptation observed in firing rate and encode increases and decreases in concentration differently
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