Higher-order unimodal olfactory sensory preconditioning in Drosophila
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Evaluation Summary:
This paper shows that Drosophila can perform olfactory unimodal sensory preconditioning, an example of higher-order conditioning that may guide behaviour through inferred value. This is of conceptual significance for the brain, behavioural, and to some extent, the social sciences, because it shows that a conditioned response to a stimulus can occur even when the stimulus itself was never paired with punishment, for example.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. The reviewers remained anonymous to the authors.)
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Abstract
Learning and memory storage is a complex process that has proven challenging to tackle. It is likely that, in nature, the instructive value of reinforcing experiences is acquired rather than innate. The association between seemingly neutral stimuli increases the gamut of possibilities to create meaningful associations and the predictive power of moment-by-moment experiences. Here, we report physiological and behavioral evidence of olfactory unimodal sensory preconditioning in fruit flies. We show that the presentation of a pair of odors (S1 and S2) before one of them (S1) is associated with electric shocks elicits a conditional response not only to the trained odor (S1) but to the odor previously paired with it (S2). This occurs even if the S2 odor was never presented in contiguity with the aversive stimulus. In addition, we show that inhibition of the small G protein Rac1 , a known forgetting regulator, facilitates the association between S1/S2 odors. These results indicate that flies can infer value to olfactory stimuli based on the previous associative structure between odors, and that inhibition of Rac1 lengthens the time window of the olfactory ‘sensory buffer’, allowing the establishment of associations between odors presented in sequence.
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Author response
Reviewer #3 (Public Review):
Sensory preconditioning (SPC) refers to a conceptually important, higher-order form of Pavlovian conditioning. It involves two training phases and a final test. In the first, pre-conditioning training phase two 'neutral' stimuli are presented together (S1, S2). In the second training phase, one of them is paired with for example a punishment (S1+). In the final test conditioned response to the respective other stimulus is assessed (S2).
The conclusion that sensory preconditioning does indeed occur requires showing that i) conditioned responding is observed for S2 but not for other, not pre-conditioned stimuli (S3); ii) that conditioned responding to S2 depends on the jointness of presentation of S1 and S2; iii) that conditioned responding to S2 depends on S1 indeed being paired with …
Author response
Reviewer #3 (Public Review):
Sensory preconditioning (SPC) refers to a conceptually important, higher-order form of Pavlovian conditioning. It involves two training phases and a final test. In the first, pre-conditioning training phase two 'neutral' stimuli are presented together (S1, S2). In the second training phase, one of them is paired with for example a punishment (S1+). In the final test conditioned response to the respective other stimulus is assessed (S2).
The conclusion that sensory preconditioning does indeed occur requires showing that i) conditioned responding is observed for S2 but not for other, not pre-conditioned stimuli (S3); ii) that conditioned responding to S2 depends on the jointness of presentation of S1 and S2; iii) that conditioned responding to S2 depends on S1 indeed being paired with punishment. It is a strength of the current paper that these requirements are met and that this is the case both at the behavioural level and for a plausible stand-in at the physiological level.
A weakness is that key data belonging together are not shown and analysed together.
We have rearranged the data.
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Evaluation Summary:
This paper shows that Drosophila can perform olfactory unimodal sensory preconditioning, an example of higher-order conditioning that may guide behaviour through inferred value. This is of conceptual significance for the brain, behavioural, and to some extent, the social sciences, because it shows that a conditioned response to a stimulus can occur even when the stimulus itself was never paired with punishment, for example.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. The reviewers remained anonymous to the authors.)
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Reviewer #1 (Public Review):
Martinez-Cervantes et al. investigate unimodal sensory preconditioning which affects odor responses even to a non-trained odor. In a previous publication, they could show that this effect was only revealed when they inhibited Rac1 in the mushroom bodies. Now, by performing functional imaging, they could additionally show that this effect is detectable in the activity level of the MBON-y1 after training. Performing rigorous experiments further revealed that the sensory preconditioning effect is strongly dependent on sensory preconditioning ISI and trial repetition, but independent of the odor type used.
The authors nicely dissected the sensory preconditioning effect itself by varying the odor exposures, the gap between odor exposures, and the odors they used. With this, they could show that under certain …
Reviewer #1 (Public Review):
Martinez-Cervantes et al. investigate unimodal sensory preconditioning which affects odor responses even to a non-trained odor. In a previous publication, they could show that this effect was only revealed when they inhibited Rac1 in the mushroom bodies. Now, by performing functional imaging, they could additionally show that this effect is detectable in the activity level of the MBON-y1 after training. Performing rigorous experiments further revealed that the sensory preconditioning effect is strongly dependent on sensory preconditioning ISI and trial repetition, but independent of the odor type used.
The authors nicely dissected the sensory preconditioning effect itself by varying the odor exposures, the gap between odor exposures, and the odors they used. With this, they could show that under certain conditions (short ISI of 1s), the effect is also prominent in WT flies with functioning Rac1. Furthermore, they could show that Rac1 inhibition only reveals the effect for intermediate ISIs (30s), but not very long ISIs (5 min.). Another interesting point they make is that the effect is odor type independent, and thus a general phenomenon. This characterization will be helpful to compare the effect between species and other learning paradigms. An interesting finding is also that the sensory preconditioning can affect neural activity levels, however, does not show in the behavior under certain conditions. Thus, the brain activity of a certain cell type per se not always affects the behavioral output. A very important point for the field of neuroscience.
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Reviewer #2 (Public Review):
In this manuscript, the authors provide physiological and behavioral evidence to support that fruit flies can perform olfactory unimodal sensory preconditioning, an example of higher-order conditioning. And they report that a small G protein Rac1 plays an important role in such sensory preconditioning. These results indicate that a simple brain may have the ability to guide behavior through inferred value.
The current findings are interesting and based on in vivo calcium imaging and behavioral data. They can provide instructive help to researchers in the learning and memory field. However, the behavioral data should be further strengthened by adding more controls. And calcium imaging results only partially explain the behavioral data, more discussion should be provided. More detailed information about …
Reviewer #2 (Public Review):
In this manuscript, the authors provide physiological and behavioral evidence to support that fruit flies can perform olfactory unimodal sensory preconditioning, an example of higher-order conditioning. And they report that a small G protein Rac1 plays an important role in such sensory preconditioning. These results indicate that a simple brain may have the ability to guide behavior through inferred value.
The current findings are interesting and based on in vivo calcium imaging and behavioral data. They can provide instructive help to researchers in the learning and memory field. However, the behavioral data should be further strengthened by adding more controls. And calcium imaging results only partially explain the behavioral data, more discussion should be provided. More detailed information about methods is required. The writing needs to be improved.
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Reviewer #3 (Public Review):
Sensory preconditioning (SPC) refers to a conceptually important, higher-order form of Pavlovian conditioning. It involves two training phases and a final test. In the first, pre-conditioning training phase two 'neutral' stimuli are presented together (S1, S2). In the second training phase, one of them is paired with for example a punishment (S1+). In the final test conditioned response to the respective other stimulus is assessed (S2).
The conclusion that sensory preconditioning does indeed occur requires showing that i) conditioned responding is observed for S2 but not for other, not pre-conditioned stimuli (S3); ii) that conditioned responding to S2 depends on the jointness of presentation of S1 and S2; iii) that conditioned responding to S2 depends on S1 indeed being paired with punishment. It is a …
Reviewer #3 (Public Review):
Sensory preconditioning (SPC) refers to a conceptually important, higher-order form of Pavlovian conditioning. It involves two training phases and a final test. In the first, pre-conditioning training phase two 'neutral' stimuli are presented together (S1, S2). In the second training phase, one of them is paired with for example a punishment (S1+). In the final test conditioned response to the respective other stimulus is assessed (S2).
The conclusion that sensory preconditioning does indeed occur requires showing that i) conditioned responding is observed for S2 but not for other, not pre-conditioned stimuli (S3); ii) that conditioned responding to S2 depends on the jointness of presentation of S1 and S2; iii) that conditioned responding to S2 depends on S1 indeed being paired with punishment. It is a strength of the current paper that these requirements are met and that this is the case both at the behavioural level and for a plausible stand-in at the physiological level.
A weakness is that key data belonging together are not shown and analysed together.
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