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Structure and flexibility in cortical representations of odour space.

ABSTRACT: The cortex organizes sensory information to enable discrimination and generalization^1-4. As systematic representations of chemical odour space have not yet been described in the olfactory cortex, it remains unclear how odour relationships are encoded to place chemically distinct but similar odours, such as lemon and orange, into perceptual categories, such as citrus^5-7. Here, by combining chemoinformatics and multiphoton imaging in the mouse, we show that both the piriform cortex and its sensory inputs from the olfactory bulb represent chemical odour relationships through correlated patterns of activity. However, cortical odour codes differ from those in the bulb: cortex more strongly clusters together representations for related odours, selectively rewrites pairwise odour relationships, and better matches odour perception. The bulb-to-cortex transformation depends on the associative network originating within the piriform cortex, and can be reshaped by passive odour experience. Thus, cortex actively builds a structured representation of chemical odour space that highlights odour relationships; this representation is similar across individuals but remains plastic, suggesting a means through which the olfactory system can assign related odour cues to common and yet personalized percepts.

SUBMITTER: Pashkovski SL

PROVIDER: S-EPMC7450987 | biostudies-literature | 2020 Jul

REPOSITORIES: biostudies-literature

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Structure and flexibility in cortical representations of odour space.

Pashkovski Stan L SL Iurilli Giuliano G Brann David D Chicharro Daniel D Drummey Kristen K Franks Kevin M KM Panzeri Stefano S Datta Sandeep Robert SR

Nature 20200701 7815

The cortex organizes sensory information to enable discrimination and generalization<sup>1-4</sup>. As systematic representations of chemical odour space have not yet been described in the olfactory cortex, it remains unclear how odour relationships are encoded to place chemically distinct but similar odours, such as lemon and orange, into perceptual categories, such as citrus<sup>5-7</sup>. Here, by combining chemoinformatics and multiphoton imaging in the mouse, we show that both the piriform ...[more]

PMID: 32612230

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Project description:A perceptual space is a mental workspace of points in a sensory domain that supports similarity and difference judgments and enables further processing such as classification and naming. Perceptual spaces are present across sensory modalities; examples include colors, faces, auditory textures, and odors. Color is perhaps the best-studied perceptual space, but it is atypical in two respects. First, the dimensions of color space are directly linked to the three cone absorption spectra, but the dimensions of generic perceptual spaces are not as readily traceable to single-neuron properties. Second, generic perceptual spaces have more than three dimensions. This is important because representing each distinguishable point in a high-dimensional space by a separate neuron or population is unwieldy; combinatorial strategies may be needed to overcome this hurdle. To study the representation of a complex perceptual space, we focused on a well-characterized 10-dimensional domain of visual textures. Within this domain, we determine perceptual distances in a threshold task (segmentation) and a suprathreshold task (border salience comparison). In N=4 human observers, we find both quantitative and qualitative differences between these sets of measurements. Quantitatively, observers' segmentation thresholds were inconsistent with their uncertainty determined from border salience comparisons. Qualitatively, segmentation thresholds suggested that distances are determined by a coordinate representation with Euclidean geometry. Border salience comparisons, in contrast, indicated a global curvature of the space, and that distances are determined by activity patterns across broadly tuned elements. Thus, our results indicate two representations of this perceptual space, and suggest that they use differing combinatorial strategies.To move from sensory signals to decisions and actions, the brain carries out a sequence of transformations. An important stage in this process is the construction of a "perceptual space" - an internal workspace of sensory information that captures similarities and differences, and enables further processing, such as classification and naming. Perceptual spaces for color, faces, visual and haptic textures and shapes, sounds, and odors (among others) are known to exist. How such spaces are represented is at present unknown. Here, using visual textures as a model, we investigate this. Psychophysical measurements suggest roles for two combinatorial strategies: one based on projections onto coordinate-like axes, and one based on patterns of activity across broadly tuned elements scattered throughout the space.

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Structure and flexibility in cortical representations of odour space.

Publications

Structure and flexibility in cortical representations of odour space.

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