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Perceptual and neural olfactory similarity in honeybees.

Guerrieri F, Schubert M, Sandoz JC, Giurfa M - PLoS Biol. (2005)

Bottom Line: We conditioned bees to odours and tested generalisation responses to different odours.The results obtained by presentation of a total of 16 x 16 odour pairs show that (i) all odorants presented could be learned, although acquisition was lower for short-chain ketones; (ii) generalisation varied depending both on the functional group and the carbon-chain length of odours trained; higher generalisation was found between long-chain than between short-chain molecules and between groups such as primary and secondary alcohols; (iii) for some odour pairs, cross-generalisation between odorants was asymmetric; (iv) a putative olfactory space could be defined for the honeybee with functional group and carbon-chain length as inner dimensions; (v) perceptual distances in such a space correlate well with physiological distances determined from optophysiological recordings of antennal lobe activity.We conclude that functional group and carbon-chain length are inner dimensions of the honeybee olfactory space and that neural activity in the antennal lobe reflects the perceptual quality of odours.

View Article: PubMed Central - PubMed

Affiliation: Centre de Recherches sur la Cognition Animale, CNRS, Université Paul-Sabatier (UMR 5169), Toulouse, France.

ABSTRACT
The question of whether or not neural activity patterns recorded in the olfactory centres of the brain correspond to olfactory perceptual measures remains unanswered. To address this question, we studied olfaction in honeybees Apis mellifera using the olfactory conditioning of the proboscis extension response. We conditioned bees to odours and tested generalisation responses to different odours. Sixteen odours were used, which varied both in their functional group (primary and secondary alcohols, aldehydes and ketones) and in their carbon-chain length (from six to nine carbons). The results obtained by presentation of a total of 16 x 16 odour pairs show that (i) all odorants presented could be learned, although acquisition was lower for short-chain ketones; (ii) generalisation varied depending both on the functional group and the carbon-chain length of odours trained; higher generalisation was found between long-chain than between short-chain molecules and between groups such as primary and secondary alcohols; (iii) for some odour pairs, cross-generalisation between odorants was asymmetric; (iv) a putative olfactory space could be defined for the honeybee with functional group and carbon-chain length as inner dimensions; (v) perceptual distances in such a space correlate well with physiological distances determined from optophysiological recordings of antennal lobe activity. We conclude that functional group and carbon-chain length are inner dimensions of the honeybee olfactory space and that neural activity in the antennal lobe reflects the perceptual quality of odours.

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Generalisation Depending on Functional Groups(A) Data of the generalisation matrix (see Figure 2) represented as two-dimensional graphs for each conditioned odour. The right ordinate represents the CSs categorised in four functional groups, primary alcohols, secondary alcohols, aldehydes, and ketones (from top to bottom). The abscissa represents the test odours aligned in the same order as the conditioned odours (from left to right). The left ordinate represents the percentage of proboscis extensions to the test odours after being trained to a given odour. Each quadrant in the figure represents generalisation responses to one functional group after training for the same (grey quadrants) or to a different functional group (white quadrants).(B) Same data as in (A), but the observed responses within each quadrant were pooled and the resulting percentage of responses per quadrant was calculated. The abscissa and the right ordinate represent the four functional groups. The left ordinate represents the percentage of proboscis extensions to each of these groups after being trained to a given group. Grey bars correspond to grey quadrants in (A) and represent generalisation to the same functional group as the conditioned one. White bars correspond to white quadrants in (A) and represent generalisation to a functional group different from the conditioned one: 1-ol, 2-ol, al, and one mean primary alcohol, secondary alcohol, aldehyde, and ketone, respectively. Asterisks indicate significant differences along a row or a column (p < 0.001)(C) Within-functional group generalisation, depending on chain length. The abscissa represents the functional groups tested. The ordinate represents the percentage of proboscis extensions to the functional groups tested after being trained to a given chain-length (lines). Thus, for instance, the first point to the left for C9 molecules (black circles) represents generalisation to 1-hexanol, 1-heptanol, and 1-octanol after conditioning to 1-nonanol. A significant heterogeneity was found in within-functional group generalisation for C8 and C9 but not for C6 and C7 molecules.(D) Generalisation within-functional groups. The figure shows results from pooling the data of (C) corresponding to each functional group. Each point shows the percentage of proboscis extensions to odours of the same functional group as the conditioned odour. Within-group generalisation was significantly heterogeneous (asterisks, p < 0.001). Pairwise comparisons showed that generalisation within aldehydes was significantly higher than within primary alcohols or ketones and marginally higher than within secondary alcohols (different letters indicate significant differences).
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pbio-0030060-g003: Generalisation Depending on Functional Groups(A) Data of the generalisation matrix (see Figure 2) represented as two-dimensional graphs for each conditioned odour. The right ordinate represents the CSs categorised in four functional groups, primary alcohols, secondary alcohols, aldehydes, and ketones (from top to bottom). The abscissa represents the test odours aligned in the same order as the conditioned odours (from left to right). The left ordinate represents the percentage of proboscis extensions to the test odours after being trained to a given odour. Each quadrant in the figure represents generalisation responses to one functional group after training for the same (grey quadrants) or to a different functional group (white quadrants).(B) Same data as in (A), but the observed responses within each quadrant were pooled and the resulting percentage of responses per quadrant was calculated. The abscissa and the right ordinate represent the four functional groups. The left ordinate represents the percentage of proboscis extensions to each of these groups after being trained to a given group. Grey bars correspond to grey quadrants in (A) and represent generalisation to the same functional group as the conditioned one. White bars correspond to white quadrants in (A) and represent generalisation to a functional group different from the conditioned one: 1-ol, 2-ol, al, and one mean primary alcohol, secondary alcohol, aldehyde, and ketone, respectively. Asterisks indicate significant differences along a row or a column (p < 0.001)(C) Within-functional group generalisation, depending on chain length. The abscissa represents the functional groups tested. The ordinate represents the percentage of proboscis extensions to the functional groups tested after being trained to a given chain-length (lines). Thus, for instance, the first point to the left for C9 molecules (black circles) represents generalisation to 1-hexanol, 1-heptanol, and 1-octanol after conditioning to 1-nonanol. A significant heterogeneity was found in within-functional group generalisation for C8 and C9 but not for C6 and C7 molecules.(D) Generalisation within-functional groups. The figure shows results from pooling the data of (C) corresponding to each functional group. Each point shows the percentage of proboscis extensions to odours of the same functional group as the conditioned odour. Within-group generalisation was significantly heterogeneous (asterisks, p < 0.001). Pairwise comparisons showed that generalisation within aldehydes was significantly higher than within primary alcohols or ketones and marginally higher than within secondary alcohols (different letters indicate significant differences).

Mentions: Figure 3A shows the percentage of PER to odours having different (white quadrants) or the same (grey quadrants) functional group as the conditioned odour. High levels of PER to odours different from the trained one correspond to high generalisation. In order to better visualise generalisation as depending on functional groups, we pooled all the observed responses within each quadrant of Figure 3A (i.e., not considering chain length) and calculated the resulting percentage of PER (Figure 3B). Grey bars correspond to generalisation to the same functional group; white bars correspond to generalisation to different functional groups. Generalisation mainly occurred within a given functional group (grey bars). This pattern was clearest for aldehydes (Figure 3B, 3rd row) because bees conditioned to aldehydes responded with a high probability to other aldehydes but showed lower responses to any other odour (see also the clear aldehyde “response block” in Figure 2).


Perceptual and neural olfactory similarity in honeybees.

Guerrieri F, Schubert M, Sandoz JC, Giurfa M - PLoS Biol. (2005)

Generalisation Depending on Functional Groups(A) Data of the generalisation matrix (see Figure 2) represented as two-dimensional graphs for each conditioned odour. The right ordinate represents the CSs categorised in four functional groups, primary alcohols, secondary alcohols, aldehydes, and ketones (from top to bottom). The abscissa represents the test odours aligned in the same order as the conditioned odours (from left to right). The left ordinate represents the percentage of proboscis extensions to the test odours after being trained to a given odour. Each quadrant in the figure represents generalisation responses to one functional group after training for the same (grey quadrants) or to a different functional group (white quadrants).(B) Same data as in (A), but the observed responses within each quadrant were pooled and the resulting percentage of responses per quadrant was calculated. The abscissa and the right ordinate represent the four functional groups. The left ordinate represents the percentage of proboscis extensions to each of these groups after being trained to a given group. Grey bars correspond to grey quadrants in (A) and represent generalisation to the same functional group as the conditioned one. White bars correspond to white quadrants in (A) and represent generalisation to a functional group different from the conditioned one: 1-ol, 2-ol, al, and one mean primary alcohol, secondary alcohol, aldehyde, and ketone, respectively. Asterisks indicate significant differences along a row or a column (p < 0.001)(C) Within-functional group generalisation, depending on chain length. The abscissa represents the functional groups tested. The ordinate represents the percentage of proboscis extensions to the functional groups tested after being trained to a given chain-length (lines). Thus, for instance, the first point to the left for C9 molecules (black circles) represents generalisation to 1-hexanol, 1-heptanol, and 1-octanol after conditioning to 1-nonanol. A significant heterogeneity was found in within-functional group generalisation for C8 and C9 but not for C6 and C7 molecules.(D) Generalisation within-functional groups. The figure shows results from pooling the data of (C) corresponding to each functional group. Each point shows the percentage of proboscis extensions to odours of the same functional group as the conditioned odour. Within-group generalisation was significantly heterogeneous (asterisks, p < 0.001). Pairwise comparisons showed that generalisation within aldehydes was significantly higher than within primary alcohols or ketones and marginally higher than within secondary alcohols (different letters indicate significant differences).
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Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC1043859&req=5

pbio-0030060-g003: Generalisation Depending on Functional Groups(A) Data of the generalisation matrix (see Figure 2) represented as two-dimensional graphs for each conditioned odour. The right ordinate represents the CSs categorised in four functional groups, primary alcohols, secondary alcohols, aldehydes, and ketones (from top to bottom). The abscissa represents the test odours aligned in the same order as the conditioned odours (from left to right). The left ordinate represents the percentage of proboscis extensions to the test odours after being trained to a given odour. Each quadrant in the figure represents generalisation responses to one functional group after training for the same (grey quadrants) or to a different functional group (white quadrants).(B) Same data as in (A), but the observed responses within each quadrant were pooled and the resulting percentage of responses per quadrant was calculated. The abscissa and the right ordinate represent the four functional groups. The left ordinate represents the percentage of proboscis extensions to each of these groups after being trained to a given group. Grey bars correspond to grey quadrants in (A) and represent generalisation to the same functional group as the conditioned one. White bars correspond to white quadrants in (A) and represent generalisation to a functional group different from the conditioned one: 1-ol, 2-ol, al, and one mean primary alcohol, secondary alcohol, aldehyde, and ketone, respectively. Asterisks indicate significant differences along a row or a column (p < 0.001)(C) Within-functional group generalisation, depending on chain length. The abscissa represents the functional groups tested. The ordinate represents the percentage of proboscis extensions to the functional groups tested after being trained to a given chain-length (lines). Thus, for instance, the first point to the left for C9 molecules (black circles) represents generalisation to 1-hexanol, 1-heptanol, and 1-octanol after conditioning to 1-nonanol. A significant heterogeneity was found in within-functional group generalisation for C8 and C9 but not for C6 and C7 molecules.(D) Generalisation within-functional groups. The figure shows results from pooling the data of (C) corresponding to each functional group. Each point shows the percentage of proboscis extensions to odours of the same functional group as the conditioned odour. Within-group generalisation was significantly heterogeneous (asterisks, p < 0.001). Pairwise comparisons showed that generalisation within aldehydes was significantly higher than within primary alcohols or ketones and marginally higher than within secondary alcohols (different letters indicate significant differences).
Mentions: Figure 3A shows the percentage of PER to odours having different (white quadrants) or the same (grey quadrants) functional group as the conditioned odour. High levels of PER to odours different from the trained one correspond to high generalisation. In order to better visualise generalisation as depending on functional groups, we pooled all the observed responses within each quadrant of Figure 3A (i.e., not considering chain length) and calculated the resulting percentage of PER (Figure 3B). Grey bars correspond to generalisation to the same functional group; white bars correspond to generalisation to different functional groups. Generalisation mainly occurred within a given functional group (grey bars). This pattern was clearest for aldehydes (Figure 3B, 3rd row) because bees conditioned to aldehydes responded with a high probability to other aldehydes but showed lower responses to any other odour (see also the clear aldehyde “response block” in Figure 2).

Bottom Line: We conditioned bees to odours and tested generalisation responses to different odours.The results obtained by presentation of a total of 16 x 16 odour pairs show that (i) all odorants presented could be learned, although acquisition was lower for short-chain ketones; (ii) generalisation varied depending both on the functional group and the carbon-chain length of odours trained; higher generalisation was found between long-chain than between short-chain molecules and between groups such as primary and secondary alcohols; (iii) for some odour pairs, cross-generalisation between odorants was asymmetric; (iv) a putative olfactory space could be defined for the honeybee with functional group and carbon-chain length as inner dimensions; (v) perceptual distances in such a space correlate well with physiological distances determined from optophysiological recordings of antennal lobe activity.We conclude that functional group and carbon-chain length are inner dimensions of the honeybee olfactory space and that neural activity in the antennal lobe reflects the perceptual quality of odours.

View Article: PubMed Central - PubMed

Affiliation: Centre de Recherches sur la Cognition Animale, CNRS, Université Paul-Sabatier (UMR 5169), Toulouse, France.

ABSTRACT
The question of whether or not neural activity patterns recorded in the olfactory centres of the brain correspond to olfactory perceptual measures remains unanswered. To address this question, we studied olfaction in honeybees Apis mellifera using the olfactory conditioning of the proboscis extension response. We conditioned bees to odours and tested generalisation responses to different odours. Sixteen odours were used, which varied both in their functional group (primary and secondary alcohols, aldehydes and ketones) and in their carbon-chain length (from six to nine carbons). The results obtained by presentation of a total of 16 x 16 odour pairs show that (i) all odorants presented could be learned, although acquisition was lower for short-chain ketones; (ii) generalisation varied depending both on the functional group and the carbon-chain length of odours trained; higher generalisation was found between long-chain than between short-chain molecules and between groups such as primary and secondary alcohols; (iii) for some odour pairs, cross-generalisation between odorants was asymmetric; (iv) a putative olfactory space could be defined for the honeybee with functional group and carbon-chain length as inner dimensions; (v) perceptual distances in such a space correlate well with physiological distances determined from optophysiological recordings of antennal lobe activity. We conclude that functional group and carbon-chain length are inner dimensions of the honeybee olfactory space and that neural activity in the antennal lobe reflects the perceptual quality of odours.

Show MeSH