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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 Chain Length(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 chain lengths, C6, C7, C8, and C9 molecules (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 for a given odour. Each quadrant in the figure represents generalisation responses to one chain length after training for the same (grey quadrants) or to a different chain length (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 chain-length categories. The left ordinate represents the percentage of proboscis extensions to each of these categories after being trained for a given chain-length category. Grey bars correspond to grey quadrants in (A) and represent generalisation to the same chain length as the conditioned one. White bars correspond to white quadrants in (A) and represent generalisation to a chain length different from the conditioned one: C6, C7, C8, and C9 mean chain length of 6, 7, 8, and 9 carbons, respectively. Asterisks indicate significant differences along a row or a column (p < 0.001).(C) Within chain-length generalisation as depending on functional group. The abscissa represents the chain lengths tested. The ordinate represents the percentage of proboscis extensions to the same chain length after being trained to a given functional group (lines). Thus, the first point to the left for ketones (red circles) represents generalisation to 1-hexanol, 2-hexanol, and hexanal after conditioning to 2-hexanone; the second point represents generalisation to 1-heptanol, 2-heptanol, and heptanal after conditioning to 2-heptanone. A significant heterogeneity was found in within-chain-length generalisation for aldehydes and ketones.(D) Generalisation within-chain lengths. The figure results from pooling the data of (C) corresponding to each chain length. Each point shows the percentage of proboscis extensions to odours of the same chain length as the conditioned odour. Within-chain-length generalisation was significantly heterogeneous (asterisks, p < 0.001). Pairwise comparisons showed that generalisation within C9 molecules was significantly higher than within C7 and C6 molecules and marginally higher than within C8 molecules (different letters indicate significant differences).
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pbio-0030060-g004: Generalisation Depending on Chain Length(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 chain lengths, C6, C7, C8, and C9 molecules (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 for a given odour. Each quadrant in the figure represents generalisation responses to one chain length after training for the same (grey quadrants) or to a different chain length (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 chain-length categories. The left ordinate represents the percentage of proboscis extensions to each of these categories after being trained for a given chain-length category. Grey bars correspond to grey quadrants in (A) and represent generalisation to the same chain length as the conditioned one. White bars correspond to white quadrants in (A) and represent generalisation to a chain length different from the conditioned one: C6, C7, C8, and C9 mean chain length of 6, 7, 8, and 9 carbons, respectively. Asterisks indicate significant differences along a row or a column (p < 0.001).(C) Within chain-length generalisation as depending on functional group. The abscissa represents the chain lengths tested. The ordinate represents the percentage of proboscis extensions to the same chain length after being trained to a given functional group (lines). Thus, the first point to the left for ketones (red circles) represents generalisation to 1-hexanol, 2-hexanol, and hexanal after conditioning to 2-hexanone; the second point represents generalisation to 1-heptanol, 2-heptanol, and heptanal after conditioning to 2-heptanone. A significant heterogeneity was found in within-chain-length generalisation for aldehydes and ketones.(D) Generalisation within-chain lengths. The figure results from pooling the data of (C) corresponding to each chain length. Each point shows the percentage of proboscis extensions to odours of the same chain length as the conditioned odour. Within-chain-length generalisation was significantly heterogeneous (asterisks, p < 0.001). Pairwise comparisons showed that generalisation within C9 molecules was significantly higher than within C7 and C6 molecules and marginally higher than within C8 molecules (different letters indicate significant differences).

Mentions: Figure 4A shows the generalisation responses of bees to odours having different (white quadrants) or the same (grey quadrants) chain length as the conditioned odour. In order to better visualise generalisation as depending on chain length, we pooled all the observed responses within each quadrant of Figure 4A and calculated the resulting percentage of PER (Figure 4B). Grey bars correspond to generalisation to the same chain length; white bars correspond to generalisation to different chain lengths. Generalisation was highest in the case of odours with the same or similar chain length.


Perceptual and neural olfactory similarity in honeybees.

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

Generalisation Depending on Chain Length(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 chain lengths, C6, C7, C8, and C9 molecules (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 for a given odour. Each quadrant in the figure represents generalisation responses to one chain length after training for the same (grey quadrants) or to a different chain length (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 chain-length categories. The left ordinate represents the percentage of proboscis extensions to each of these categories after being trained for a given chain-length category. Grey bars correspond to grey quadrants in (A) and represent generalisation to the same chain length as the conditioned one. White bars correspond to white quadrants in (A) and represent generalisation to a chain length different from the conditioned one: C6, C7, C8, and C9 mean chain length of 6, 7, 8, and 9 carbons, respectively. Asterisks indicate significant differences along a row or a column (p < 0.001).(C) Within chain-length generalisation as depending on functional group. The abscissa represents the chain lengths tested. The ordinate represents the percentage of proboscis extensions to the same chain length after being trained to a given functional group (lines). Thus, the first point to the left for ketones (red circles) represents generalisation to 1-hexanol, 2-hexanol, and hexanal after conditioning to 2-hexanone; the second point represents generalisation to 1-heptanol, 2-heptanol, and heptanal after conditioning to 2-heptanone. A significant heterogeneity was found in within-chain-length generalisation for aldehydes and ketones.(D) Generalisation within-chain lengths. The figure results from pooling the data of (C) corresponding to each chain length. Each point shows the percentage of proboscis extensions to odours of the same chain length as the conditioned odour. Within-chain-length generalisation was significantly heterogeneous (asterisks, p < 0.001). Pairwise comparisons showed that generalisation within C9 molecules was significantly higher than within C7 and C6 molecules and marginally higher than within C8 molecules (different letters indicate significant differences).
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Related In: Results  -  Collection

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

pbio-0030060-g004: Generalisation Depending on Chain Length(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 chain lengths, C6, C7, C8, and C9 molecules (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 for a given odour. Each quadrant in the figure represents generalisation responses to one chain length after training for the same (grey quadrants) or to a different chain length (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 chain-length categories. The left ordinate represents the percentage of proboscis extensions to each of these categories after being trained for a given chain-length category. Grey bars correspond to grey quadrants in (A) and represent generalisation to the same chain length as the conditioned one. White bars correspond to white quadrants in (A) and represent generalisation to a chain length different from the conditioned one: C6, C7, C8, and C9 mean chain length of 6, 7, 8, and 9 carbons, respectively. Asterisks indicate significant differences along a row or a column (p < 0.001).(C) Within chain-length generalisation as depending on functional group. The abscissa represents the chain lengths tested. The ordinate represents the percentage of proboscis extensions to the same chain length after being trained to a given functional group (lines). Thus, the first point to the left for ketones (red circles) represents generalisation to 1-hexanol, 2-hexanol, and hexanal after conditioning to 2-hexanone; the second point represents generalisation to 1-heptanol, 2-heptanol, and heptanal after conditioning to 2-heptanone. A significant heterogeneity was found in within-chain-length generalisation for aldehydes and ketones.(D) Generalisation within-chain lengths. The figure results from pooling the data of (C) corresponding to each chain length. Each point shows the percentage of proboscis extensions to odours of the same chain length as the conditioned odour. Within-chain-length generalisation was significantly heterogeneous (asterisks, p < 0.001). Pairwise comparisons showed that generalisation within C9 molecules was significantly higher than within C7 and C6 molecules and marginally higher than within C8 molecules (different letters indicate significant differences).
Mentions: Figure 4A shows the generalisation responses of bees to odours having different (white quadrants) or the same (grey quadrants) chain length as the conditioned odour. In order to better visualise generalisation as depending on chain length, we pooled all the observed responses within each quadrant of Figure 4A and calculated the resulting percentage of PER (Figure 4B). Grey bars correspond to generalisation to the same chain length; white bars correspond to generalisation to different chain lengths. Generalisation was highest in the case of odours with the same or similar chain length.

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