Contrasting patterns of specificity and transfer in human odor discrimination learning
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eLife Assessment
This potentially important study explores the specificity of olfactory perceptual learning. In keeping with previous work, the authors found that learning to discriminate between two enantiomers does not generalize across the nostrils or to unrelated enantiomers, whereas learning to discriminate odor mixtures does generalize across the nostrils and to other odor mixtures, with this learning effect persisting over at least two weeks. While the evidence presented to support these findings is convincing, it remains unclear why the results differ for enantiomers and why training on odor mixtures generalizes to other odor mixtures.
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Abstract
Practice enhances olfactory performance. However, laboratory studies to date suggest that olfactory learning is largely restricted to the trained odors, posing a significant challenge for training-based rehabilitation therapies for olfactory loss. In this study, we introduce various types of odors to olfactory discrimination training, conducted unilaterally. We demonstrate contrasting patterns of specificity and transfer of learning, independent of adaptation and task difficulty. Individuals trained with odor mixtures of different ratios show long-term perceptual gains that completely transfer to the untrained nostril and effectively generalize to untrained mixtures dissimilar in structure and odor quality from the trained ones. Conversely, those trained with odor enantiomers show no transfer of learning across nostrils or to unrelated enantiomers, replicating our earlier findings (Feng & Zhou, 2019). Our observations indicate that concentration ratio and chirality represent distinct olfactory attributes. Furthermore, discrimination learning occurs at different stages of olfactory processing, depending on which attribute is task-relevant. These findings open up new avenues to enhance the effectiveness of olfactory training.
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eLife Assessment
This potentially important study explores the specificity of olfactory perceptual learning. In keeping with previous work, the authors found that learning to discriminate between two enantiomers does not generalize across the nostrils or to unrelated enantiomers, whereas learning to discriminate odor mixtures does generalize across the nostrils and to other odor mixtures, with this learning effect persisting over at least two weeks. While the evidence presented to support these findings is convincing, it remains unclear why the results differ for enantiomers and why training on odor mixtures generalizes to other odor mixtures.
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Reviewer #1 (Public Review):
This study extends a previous study by the same group on the generalization of odor discrimination from one nostril to the other. In their earlier study, the group showed that learning to discriminate between two enantiomers does not generalize across nostrils. This was surprising given the Mainland & Sobel 2001 study that found that detecting androstenone in people who do not detect it can generalize across the two nostrils. In this study, they confirmed their previous results and reported that, unlike enantiomers, learning to discriminate odor mixtures generalizes across nostrils, generalizes to other odor mixtures, and is persistent over at least two weeks. This interesting and important result extends our knowledge of this phenomenon and will likely steer more research. It may also help develop new …
Reviewer #1 (Public Review):
This study extends a previous study by the same group on the generalization of odor discrimination from one nostril to the other. In their earlier study, the group showed that learning to discriminate between two enantiomers does not generalize across nostrils. This was surprising given the Mainland & Sobel 2001 study that found that detecting androstenone in people who do not detect it can generalize across the two nostrils. In this study, they confirmed their previous results and reported that, unlike enantiomers, learning to discriminate odor mixtures generalizes across nostrils, generalizes to other odor mixtures, and is persistent over at least two weeks. This interesting and important result extends our knowledge of this phenomenon and will likely steer more research. It may also help develop new training protocols for people with impairments in their sense of smell.
The main weakness of this study is its scope, as it does not provide substantial insight into why the results differ for enantiomers and why training on odor mixtures generalizes to other odor mixtures.
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Reviewer #2 (Public Review):
The manuscript from Chang et al. taps on an important issue in olfactory perceptual plasticity, named the generalization of perceptual learning effect by training using odors. They employed a discrimination training/learning task with either binary odor mixture or odor enantiomers, and tested for post-training effect at several time intervals. Their results showed contrasting patterns of specificity (enantiomers) and transfer (odor mixtures), and the learning effect persisted at 2 weeks post-training. They demonstrated that the effect was independent of task difficulty, olfactory adaptation and gender.
Overall this was a well-controlled study and shows novel results. The strength of the study includes the consideration of odor structure and perceptual (dis)similarity and the control training condition. I …
Reviewer #2 (Public Review):
The manuscript from Chang et al. taps on an important issue in olfactory perceptual plasticity, named the generalization of perceptual learning effect by training using odors. They employed a discrimination training/learning task with either binary odor mixture or odor enantiomers, and tested for post-training effect at several time intervals. Their results showed contrasting patterns of specificity (enantiomers) and transfer (odor mixtures), and the learning effect persisted at 2 weeks post-training. They demonstrated that the effect was independent of task difficulty, olfactory adaptation and gender.
Overall this was a well-controlled study and shows novel results. The strength of the study includes the consideration of odor structure and perceptual (dis)similarity and the control training condition. I have two minor issues that hope the authors could address in the next version of the manuscript.
The author used a binary odor mixture with a ration 7:9 or 9:11, why is this ratio chosen and used for the experiment?
Over the course of training, has the valence of odor (odor mixture) changed, it would be helpful to include these results in the supplements. As the author indicated in the discussion, the potential site underlying the transfer effect is the OFC, which has been found to represent odor valence previously (Anderson, Christoff et al. 2003). It would be nice to see the author replicate the results with odor/odor mixture valence (change) controlled.
Anderson, A. K., K. Christoff, I. Stappen, D. Panitz, D. G. Ghahremani, G. Glover, J. D. Gabrieli and N. Sobel (2003). "Dissociated neural representations of intensity and valence in human olfaction." Nat Neurosci 6(2): 196-202.
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eLife Assessment
This potentially important study explores the specificity of olfactory perceptual learning. In keeping with previous work, the authors found that learning to discriminate between two enantiomers does not generalize across the nostrils or to unrelated enantiomers, whereas learning to discriminate odor mixtures does generalize across the nostrils and to other odor mixtures, with this learning effect persisting over at least two weeks. While the evidence presented to support these findings is convincing, it remains unclear why the results differ for enantiomers and why training on odor mixtures generalizes to other odor mixtures.
Discrimination of odor enantiomers ultimately relies on the enantioselectivity of olfactory receptors, whereas mixture discrimination likely depends on relative differences in perceived …
eLife Assessment
This potentially important study explores the specificity of olfactory perceptual learning. In keeping with previous work, the authors found that learning to discriminate between two enantiomers does not generalize across the nostrils or to unrelated enantiomers, whereas learning to discriminate odor mixtures does generalize across the nostrils and to other odor mixtures, with this learning effect persisting over at least two weeks. While the evidence presented to support these findings is convincing, it remains unclear why the results differ for enantiomers and why training on odor mixtures generalizes to other odor mixtures.
Discrimination of odor enantiomers ultimately relies on the enantioselectivity of olfactory receptors, whereas mixture discrimination likely depends on relative differences in perceived configural odor notes. These processes probably engage plasticity at different stages of the olfactory pathway. The revised Discussion (p.16-18) now elaborates on this distinction and the potential underlying mechanisms. Please also refer to our responses to Reviewer 1’s Point 1 and Reviewer 2’s Points 2 and 3 below.
Reviewer #1 (Public Review):
This study extends a previous study by the same group on the generalization of odor discrimination from one nostril to the other. In their earlier study, the group showed that learning to discriminate between two enantiomers does not generalize across nostrils. This was surprising given the Mainland & Sobel 2001 study that found that detecting androstenone in people who do not detect it can generalize across the two nostrils. In this study, they confirmed their previous results and reported that, unlike enantiomers, learning to discriminate odor mixtures generalizes across nostrils, generalizes to other odor mixtures, and is persistent over at least two weeks.
This interesting and important result extends our knowledge of this phenomenon and will likely steer more research. It may also help develop new training protocols for people with impairments in their sense of smell.
We thank the reviewer for the encouraging remarks.
The main weakness of this study is its scope, as it does not provide substantial insight into why the results differ for enantiomers and why training on odor mixtures generalizes to other odor mixtures.
We thank the reviewer for this insightful comment. While the present study does not directly identify the neural mechanisms underlying these differences, it provides behavioral constraints on where specificity and generalization may arise within the olfactory system. Further neuroimaging and neurophysiological work will be needed to fully elucidate the underlying mechanisms.
Reviewer #2 (Public Review):
The manuscript from Chang et al. taps on an important issue in olfactory perceptual plasticity, named the generalization of perceptual learning effect by training using odors. They employed a discrimination training/learning task with either binary odor mixture or odor enantiomers, and tested for post-training effect at several time intervals. Their results showed contrasting patterns of specificity (enantiomers) and transfer (odor mixtures), and the learning effect persisted at 2 weeks post-training. They demonstrated that the effect was independent of task difficulty, olfactory adaptation and gender.
Overall this was a well-controlled study and shows novel results. The strength of the study includes the consideration of odor structure and perceptual (dis)similarity and the control training condition.
We appreciate the reviewer’s positive assessment of our work.
I have two minor issues that hope the authors could address in the next version of the manuscript.
(1). The author used a binary odor mixture with a ration 7:9 or 9:11, why is this ratio chosen and used for the experiment?
This ratio was selected based on pilot testing and practical constraints. During piloting, we evaluated several mixing ratios to identify those that met two key criteria: (1) Baseline indiscriminability: Most participants were unable to reliably discriminate between the two binary mixtures in a:b and b:a ratios at baseline. (2)Trainability: With 1–5 weeks of training, participants could acquire the ability to discriminate between them.
The a:b ratios of 7:9 and 9:11 were the ratios that met both criteria in our pilot testing, making them suitable for assessing training‑induced improvements in mixture discrimination. This clarification has been added to the revised Olfactory Stimuli subsection of the Materials and Methods (p.19-20 of the revised manuscript).
(2) Over the course of training, has the valence of odor (odor mixture) changed, it would be helpful to include these results in the supplements. As the author indicated in the discussion, the potential site underlying the transfer effect is the OFC, which has been found to represent odor valence previously (Anderson, Christoff et al. 2003). It would be nice to see the author replicate the results with odor/odor mixture valence (change) controlled.
Anderson, A. K., K. Christoff, I. Stappen, D. Panitz, D. G. Ghahremani, G. Glover, J. D. Gabrieli and N. Sobel (2003). "Dissociated neural representations of intensity and valence in human olfaction." Nat Neurosci 6(2): 196-202.
Odor valence ratings were not collected in Experiments 1 and 2. However, we have since conducted a new experiment examining concentration discrimination learning (see our response to Reviewer 1, Point 1), using the constituents of the mixtures from Experiment 2 as stimuli (i.e., concentration pairs of acetophenone, 2 octanone, methyl salicylate, and isoamyl butyrate). In this new experiment (now incorporated as Experiment 3 in the revised manuscript), unilateral odor valence ratings were collected at baseline (Day 0) and at the post training test and retests on Days N, N+1, N+3, N+7, and N+14.
For all odor pairs (training and controls), there was no significant change in perceived valence from baseline to Day N, regardless of nostril (ps > 0.05 for the main effects of session and nostril, as well as their interaction; Figure S5D). Moreover, odor valence ratings remained stable across the five post training test sessions (ps ≥ 0.29 for the main and interaction effects involving session), showing the same pattern as at baseline (Figure S5D, F). Thus, training appeared to have no measurable influence on odor valence perception. These results have been incorporated into the revised manuscript on p.14-15.
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