4.6 Article

Paradoxical relationship between speed and accuracy in olfactory figure-background segregation

Journal

PLOS COMPUTATIONAL BIOLOGY
Volume 17, Issue 12, Pages -

Publisher

PUBLIC LIBRARY SCIENCE
DOI: 10.1371/journal.pcbi.1009674

Keywords

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Funding

  1. European Research Council Starting Grant [755764-COFBMIX]
  2. Israel Science foundation [757/16]
  3. DFG [CRC 1080]
  4. Gatsby Charitable Foundation

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This study explores the interference mechanisms of background odors in odor detection tasks. The results show that background odors decrease mouse performance but paradoxically also decrease reaction times, indicating an increase in noise in the decision-making process. By fitting the drift diffusion model to behavioral data, it was found that background odors affect both the signal and noise, leading to a paradoxical relationship between trial difficulty and decision speed.
In natural settings, many stimuli impinge on our sensory organs simultaneously. Parsing these sensory stimuli into perceptual objects is a fundamental task faced by all sensory systems. Similar to other sensory modalities, increased odor backgrounds decrease the detectability of target odors by the olfactory system. The mechanisms by which background odors interfere with the detection and identification of target odors are unknown. Here we utilized the framework of the Drift Diffusion Model (DDM) to consider possible interference mechanisms in an odor detection task. We first considered pure effects of background odors on either signal or noise in the decision-making dynamics and showed that these produce different predictions about decision accuracy and speed. To test these predictions, we trained mice to detect target odors that are embedded in random background mixtures in a two-alternative choice task. In this task, the inter-trial interval was independent of behavioral reaction times to avoid motivating rapid responses. We found that increased backgrounds reduce mouse performance but paradoxically also decrease reaction times, suggesting that noise in the decision making process is increased by backgrounds. We further assessed the contributions of background effects on both noise and signal by fitting the DDM to the behavioral data. The models showed that background odors affect both the signal and the noise, but that the paradoxical relationship between trial difficulty and reaction time is caused by the added noise. Author summary Sensory systems are constantly stimulated by signals from many objects in the environment. Segmentation of important signals from the cluttered background is therefore a task that is faced by all sensory systems. For many mammalians, the sense of smell is the primary sense that guides many daily behaviors. As such, the olfactory system must be able to detect and identify odors of interest against varying and dynamic backgrounds. Here we studied how background odors interfere with the detection of target odors. We trained mice on a task in which they are presented with odor mixtures and are required to report whether they include either of two target odors. We analyze the behavioral data using a common model of sensory-guided decision-making-the drift-diffusion-model. In this model, decisions are influenced by two elements: a drift which is the signal produced by the stimulus, and noise. We show that the addition of background odors has a dual effect-a reduction in the drift, as well as an increase in the noise. The increased noise also causes more rapid decisions, thereby producing a paradoxical relationship between trial difficulty and decision speed; mice make faster decisions on more difficult trials.

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