Immediate perception of a reward is distinct from the reward’s long-term salience

  1. John P McGinnis
  2. Huoqing Jiang
  3. Moutaz Ali Agha
  4. Consuelo Perez Sanchez
  5. Jeff Lange
  6. Zulin Yu
  7. Frederic Marion-Poll
  8. Kausik Si  Is a corresponding author
  1. Stowers Institute for Medical Research, United States
  2. University of Kansas Medical Center, United States
  3. Université Paris-Sud, Université Paris-Saclay, France
  4. AgroParisTech, France
  5. University of Kansas School of Medicine, United States
6 figures

Figures

Figure 1 with 1 supplement
Flies’ immediate preference for a sugar is not predictive of their long-term memory: various sugars from fruits.

(A) Schematic of behavioral assays. In the appetitive associative memory paradigm, hungry flies are trained for 2 min with the sugar-odor pair and memory is assayed by subsequently giving a choice …

https://doi.org/10.7554/eLife.22283.003
Figure 1—figure supplement 1
The CS-US association occurs during the two-minute training.

(A) Flies trained with sucrose, which produces robust 24 hr memory, were immediately provided either rich nutritious food or water. If sucrose’s nutritional value is assessed beyond the 2-min …

https://doi.org/10.7554/eLife.22283.004
Figure 2 with 4 supplements
Flies’ immediate preference for a sugar is not predictive of their long-term memory: L- vs D-arabinose.

(A) Structures of D- and L-arabinose. (B) Survival percentages for flies given solely 1 M sugar solutions. n = 10 (50 flies per n) for each time point. (C) Short- and long-term memory of sucrose and …

https://doi.org/10.7554/eLife.22283.005
Figure 2—figure supplement 1
Palatability of D- and L-arabinose over a concentration range.

Fifty male flies per trial were given water alone for 24–36 hr, then put on a microtiter plate checkered with food-dye-labeled water and either D-arabinose or L-arabinose at various concentrations. …

https://doi.org/10.7554/eLife.22283.006
Figure 2—figure supplement 2
Specificity of L-arabinose memory.

(A) L-arabinose from different sources (USB and Sigma) generated equivalent long-term memory, controlling for other contaminating sugars. (B) Canton-S flies obtained from two different labs show …

https://doi.org/10.7554/eLife.22283.007
Figure 2—figure supplement 3
Although both are sweet, D-arabinose is preferred over L-arabinose.

(A) At equal concentrations, flies overwhelmingly prefer D-arabinose to L-arabinose; the preference begins to shift when L-arabinose is ≥3 times more concentrated than D-arabinose. (B) CAFÉ assay …

https://doi.org/10.7554/eLife.22283.008
Figure 2—figure supplement 4
Detection and memory.

(A) Proboscis extension reflex response to D- and L-arabinose. Flies were given a drop of water, then 10 mM D-ara, then 100 mM D-ara, then 1 M D-ara, water, followed by 10 mM L-ara, 100 mM L-ara, …

https://doi.org/10.7554/eLife.22283.009
Figure 3 with 2 supplements
Gr43a- and Gr61a-expressing neurons are involved in D vs L preference and in L-arabinose memory.

(A) Silencing of Gr61a-expressing neurons with Kir2.1 impaired D > L discrimination and preference; silencing Gr64e- and Gr64f-expressing neurons nearly eliminated detection of both sugars. (B) …

https://doi.org/10.7554/eLife.22283.010
Figure 3—figure supplement 1
Gr expressing neurons involved in D- and L-arabinose detection.

(A) Fifty male flies per trial were given water alone for 24–36 hr, then put on a microtiter plate checkered with food-dye-labeled water and 1 M L-arabinose. After 5 min, flies were removed and the …

https://doi.org/10.7554/eLife.22283.011
Figure 3—figure supplement 2
L- and D-arabinose detection do not rely on any single receptor.

(A) Gr43a mutants have a small L-arabinose detection deficit while Gr61a mutants have a moderate detection deficit. (B) No single receptor removal impairs D-arabinose detection. Results with error …

https://doi.org/10.7554/eLife.22283.012
Figure 4 with 1 supplement
Tarsal Gr43a neurons are critical for L-arabinose memory.

(A) Gr43aGAL4 neurons are observed in the dorsolateral protocerebrum, central brain, proboscis, leg, and gut (not shown). (B) Silencing only the dorsal protocerebral (DLP) and VCSO neurons does not …

https://doi.org/10.7554/eLife.22283.013
Figure 4—figure supplement 1
Expression patterns of Gr-GAL4s.

(A) Distal tarsi expression patterns of Gr5aGAL4 (3 neurons), Gr43aGAL4 (2 neurons), and Gr61aGAL4 (6 neurons). Scale bar 50 μm. (B) Gr5a-Gr43a splitGal4 labeling (Pfeiffer et al., 2010). GAL4 …

https://doi.org/10.7554/eLife.22283.014
Figure 5 with 1 supplement
Tarsal Gr43a neurons respond differentially to D- and L-arabinose.

(A) Spikes per second of recorded f5V tarsal neuron in response to D- or L-arabinose at various concentrations. (B) Spikes per second binned by 100 ms over the first two seconds of response. (C) The …

https://doi.org/10.7554/eLife.22283.015
Figure 5—figure supplement 1
Evoked-calcium activity of Gr43a neurons in response to D- and L-arabinose.

(A) Imaging of calcium responses of LSO neurons in proboscis. The left panel shows curve-aligned fluorescence to compare the shape of the responses, and the right panel plots peak magnitudes as ∆F/Fo

https://doi.org/10.7554/eLife.22283.016
Figure 6 with 1 supplement
Activation of Gr43a neurons is sufficient to form rewarding associative memory.

(A) Schematic of heat and light-activated associative olfactory training. (B) Activation of Gr43aGAL4 neurons by dTrpA1 (at 31 °C) does not induce long-term memory. (C) A 20 Hz, 15 ms pulse-width …

https://doi.org/10.7554/eLife.22283.017
Figure 6—figure supplement 1
dTrpA1 activation of R58E02 neurons does not produce long-term memory.

(A) Activation of R58E02GAL4 dopaminergic neurons, either with light (ReaChR; 1 Hz, 500 ms pulse-width for 20 s, repeated three times over 2 min, or 10 Hz, 10 ms pulse-width, repeated continuously …

https://doi.org/10.7554/eLife.22283.018

Download links