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Social Eavesdropping in Zebrafish: Tuning of Attention to Social Interactions.

Abril-de-Abreu R, Cruz J, Oliveira RF - Sci Rep (2015)

Bottom Line: This ability (aka social eavesdropping) is expected to impact Darwinian fitness, and hence predicts the evolution of cognitive processes that enable social animals to use public information available in the environment.These adaptive specializations in cognition may have evolved both at the level of learning and memory mechanisms, and at the level of input mechanisms, such as attention, which select the information that is available for learning.Here we used zebrafish to test if attention in a social species is tuned to the exchange of information between conspecifics.

View Article: PubMed Central - PubMed

Affiliation: 1] Instituto Gulbenkian de Ciência, Rua da Quinta Grande 6, 2780-156, Oeiras, Portugal [2] ISPA - Instituto Universitário, Rua Jardim do Tabaco 34, 1149-041 Lisboa, Portugal [3] Champalimaud Neuroscience Programme, Champalimaud Centre for the Unknown, Av. de Brasilia, 1400-038 Lisboa, Portugal.

ABSTRACT
Group living animals may eavesdrop on signalling interactions between conspecifics in order to collect adaptively relevant information obtained from others, without incurring in the costs of first-hand information acquisition. This ability (aka social eavesdropping) is expected to impact Darwinian fitness, and hence predicts the evolution of cognitive processes that enable social animals to use public information available in the environment. These adaptive specializations in cognition may have evolved both at the level of learning and memory mechanisms, and at the level of input mechanisms, such as attention, which select the information that is available for learning. Here we used zebrafish to test if attention in a social species is tuned to the exchange of information between conspecifics. Our results show that zebrafish are more attentive towards interacting (i.e. fighting) than towards non-interacting pairs of conspecifics, with the exposure to fighting not increasing activity or stress levels. Moreover, using video playbacks to manipulate form features of the fighting fish, we show that during the assessment phase of the fight, bystanders' attention is more driven by form features of the interacting opponents; whereas during the post-resolution phase, it is driven by biological movement features of the dominant fish chasing the subordinate fish.

No MeSH data available.


Related in: MedlinePlus

Bystanders’ behavioural and hormonal results.(a) 2D heatmaps and linear histograms of the time spent in each position of the tracking arena by a representative focal fish from each treatment: bystander to fighting conspecifics (BIC); bystander to non-interacting conspecifics (BNIC); and socially isolated (ISOL). The heatmaps are scaled from maximum relative value (red) to minimum relative value (dark blue). Linear histograms represented in arbitrary scale. (b) Circular plots of the focal fishes’ individual mean orientations for each treatment (BIC – magenta triangles, BNIC – lime triangles, ISOL – blue triangles) and the corresponding group mean resultant vector (black arrows). BIC fish deviate significantly from a uniform distribution, clustering around its group mean resultant vector. (c) Scatter plot (n = 10 to 12 / treatment) of the individual (coloured dots) and mean (black lines) percentage of time spent in the ROI for each treatment (BIC– magenta; BNIC– lime; ISOL– blue) during the 30 minutes test. Dashed grey line represents the value expected from a random distribution in the arena (25%). (d) Polar scatter plot of the focal fishes’ (coloured dots) individual mean resultant vector’s angles α (0˚ to 360˚) combined with corresponding vector lengths R (0 to 1), for each treatment. (e) Scatter plot of the individual (coloured dots) resultant vector’s lengths R projected (R proj) onto the stimulus direction (180˚) and corresponding group mean value Rgproj (black lines), for each treatment. Positive values indicate directional focus towards the stimulus; zero indicates no directionality (dashed grey line); negative values indicate directional focus opposite to the stimulus. (f,g,h) Scatter plots of the individual (coloured dots) and mean values (black lines) of the focal fishes’ total distance covered in the arena, mean speed in ROI and whole-body cortisol levels, for each treatment. * P < 0.05, ** P < 0.01, *** P < 0.001.
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f2: Bystanders’ behavioural and hormonal results.(a) 2D heatmaps and linear histograms of the time spent in each position of the tracking arena by a representative focal fish from each treatment: bystander to fighting conspecifics (BIC); bystander to non-interacting conspecifics (BNIC); and socially isolated (ISOL). The heatmaps are scaled from maximum relative value (red) to minimum relative value (dark blue). Linear histograms represented in arbitrary scale. (b) Circular plots of the focal fishes’ individual mean orientations for each treatment (BIC – magenta triangles, BNIC – lime triangles, ISOL – blue triangles) and the corresponding group mean resultant vector (black arrows). BIC fish deviate significantly from a uniform distribution, clustering around its group mean resultant vector. (c) Scatter plot (n = 10 to 12 / treatment) of the individual (coloured dots) and mean (black lines) percentage of time spent in the ROI for each treatment (BIC– magenta; BNIC– lime; ISOL– blue) during the 30 minutes test. Dashed grey line represents the value expected from a random distribution in the arena (25%). (d) Polar scatter plot of the focal fishes’ (coloured dots) individual mean resultant vector’s angles α (0˚ to 360˚) combined with corresponding vector lengths R (0 to 1), for each treatment. (e) Scatter plot of the individual (coloured dots) resultant vector’s lengths R projected (R proj) onto the stimulus direction (180˚) and corresponding group mean value Rgproj (black lines), for each treatment. Positive values indicate directional focus towards the stimulus; zero indicates no directionality (dashed grey line); negative values indicate directional focus opposite to the stimulus. (f,g,h) Scatter plots of the individual (coloured dots) and mean values (black lines) of the focal fishes’ total distance covered in the arena, mean speed in ROI and whole-body cortisol levels, for each treatment. * P < 0.05, ** P < 0.01, *** P < 0.001.

Mentions: We started the analysis by individually profiling the time spent by the focal fish in each position of the arena during the test. Qualitative analysis using 2D heatmaps and histogram representation, revealed different spatial distribution patterns for each treatment (Fig. 2a). On average BIC fish spent more time closer to the tank wall on the side of the fighting stimulus fish than did BNIC fish, which showed a more dispersed distribution in the arena. A few BNIC fish spent more time in the area closer to one of the two non-interacting stimulus fish. ISOL fish showed on average a dispersed distribution in the arena. As a quantitative measure of proximity towards the stimuli, we analysed for each treatment the group mean percentage of time spent in the region of interest (ROI), comprising 25% of the tank (see Methods, Fig. 1c). BIC fish spent significantly more time in the ROI than ISOL fish, whereas there were no differences between BNIC and ISOL fish (see Fig. 2c and Table 1). The differences between BIC and BNIC fish were also not significant (Table 1). The ISOL fish results (time in ROI = 22.67 ± 3.17%, mean ± SEM, n = 10) matched what would be expected from a uniform distribution in the arena, with the fish showing no particular preference for the ROI and spending on average 25% of the time in 25% (ROI) of the total area (One-sample t-test, t9 = –0.73, P = 0.48). In the BNIC treatment, three (time in ROI = 84.39 ± 4.48%, n = 3) out of the 12 tested fish showed a strong proximity towards the stimuli, which differed from the other nine fish (time in ROI = 27.03 ± 4.46%; n = 9) suggesting a possible bimodality of a subset of the sampled population. To measure the focal fish’s directionality, we analysed individual and group preferred orientations, and also directional focus (see Methods for details) towards the stimulus fish. Circular scatter plots of the individual mean resultant vector’s orientations and directional focus (see Methods), revealed different distribution patterns for each treatment (Fig. 2b,d). We observed that BIC fishes’ mean orientations, strongly clustered around the fighting conspecifics tank’s direction (at 180 degrees). BNIC fish also oriented predominately towards the stimulus direction although scattered as well around other directions, whereas ISOL fish showed a dispersed distribution along different directions. Correspondingly, determination of the group mean resultant vector for each treatment (see Methods, Fig. 2b) revealed that all group mean resultant vectors were oriented towards the stimuli at 180°[αg (BIC) = 182.59°, 95% C.I. = 158.43° – 191.91°, Rg = 0.25, n = 11; αg (BNIC) = 179.07°, Rg = 0.14, n = 12; αg (ISOL) = 186.21°, Rg = 0.042, n = 10], with the corresponding mean vector’ lengths Rg, a measure of directional focus (see Methods for details), showing a higher value for the BIC treatment. Likewise, the individual fish vector’s length projection (R proj) onto the stimulus direction and the corresponding group mean projection (Rgproj) (see Methods and Fig. 2e), were significantly higher for BIC fish than ISOL fish, whereas there were no differences between BNIC and ISOL fish (see Table 1). The differences between BIC and BNIC fish were also not significant (Table 1). Reassuringly, circular uniformity analysis confirmed that only the BIC fish showed a significant directional focus towards the stimulus, with their individual mean orientations’ distribution (Fig. 2b) deviating significantly from uniformity and clustering around the corresponding group mean direction[Moore’s Test, (BIC): P < 0.001; (BNIC): P > 0.1; (ISOL): P > 0.1].


Social Eavesdropping in Zebrafish: Tuning of Attention to Social Interactions.

Abril-de-Abreu R, Cruz J, Oliveira RF - Sci Rep (2015)

Bystanders’ behavioural and hormonal results.(a) 2D heatmaps and linear histograms of the time spent in each position of the tracking arena by a representative focal fish from each treatment: bystander to fighting conspecifics (BIC); bystander to non-interacting conspecifics (BNIC); and socially isolated (ISOL). The heatmaps are scaled from maximum relative value (red) to minimum relative value (dark blue). Linear histograms represented in arbitrary scale. (b) Circular plots of the focal fishes’ individual mean orientations for each treatment (BIC – magenta triangles, BNIC – lime triangles, ISOL – blue triangles) and the corresponding group mean resultant vector (black arrows). BIC fish deviate significantly from a uniform distribution, clustering around its group mean resultant vector. (c) Scatter plot (n = 10 to 12 / treatment) of the individual (coloured dots) and mean (black lines) percentage of time spent in the ROI for each treatment (BIC– magenta; BNIC– lime; ISOL– blue) during the 30 minutes test. Dashed grey line represents the value expected from a random distribution in the arena (25%). (d) Polar scatter plot of the focal fishes’ (coloured dots) individual mean resultant vector’s angles α (0˚ to 360˚) combined with corresponding vector lengths R (0 to 1), for each treatment. (e) Scatter plot of the individual (coloured dots) resultant vector’s lengths R projected (R proj) onto the stimulus direction (180˚) and corresponding group mean value Rgproj (black lines), for each treatment. Positive values indicate directional focus towards the stimulus; zero indicates no directionality (dashed grey line); negative values indicate directional focus opposite to the stimulus. (f,g,h) Scatter plots of the individual (coloured dots) and mean values (black lines) of the focal fishes’ total distance covered in the arena, mean speed in ROI and whole-body cortisol levels, for each treatment. * P < 0.05, ** P < 0.01, *** P < 0.001.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4525141&req=5

f2: Bystanders’ behavioural and hormonal results.(a) 2D heatmaps and linear histograms of the time spent in each position of the tracking arena by a representative focal fish from each treatment: bystander to fighting conspecifics (BIC); bystander to non-interacting conspecifics (BNIC); and socially isolated (ISOL). The heatmaps are scaled from maximum relative value (red) to minimum relative value (dark blue). Linear histograms represented in arbitrary scale. (b) Circular plots of the focal fishes’ individual mean orientations for each treatment (BIC – magenta triangles, BNIC – lime triangles, ISOL – blue triangles) and the corresponding group mean resultant vector (black arrows). BIC fish deviate significantly from a uniform distribution, clustering around its group mean resultant vector. (c) Scatter plot (n = 10 to 12 / treatment) of the individual (coloured dots) and mean (black lines) percentage of time spent in the ROI for each treatment (BIC– magenta; BNIC– lime; ISOL– blue) during the 30 minutes test. Dashed grey line represents the value expected from a random distribution in the arena (25%). (d) Polar scatter plot of the focal fishes’ (coloured dots) individual mean resultant vector’s angles α (0˚ to 360˚) combined with corresponding vector lengths R (0 to 1), for each treatment. (e) Scatter plot of the individual (coloured dots) resultant vector’s lengths R projected (R proj) onto the stimulus direction (180˚) and corresponding group mean value Rgproj (black lines), for each treatment. Positive values indicate directional focus towards the stimulus; zero indicates no directionality (dashed grey line); negative values indicate directional focus opposite to the stimulus. (f,g,h) Scatter plots of the individual (coloured dots) and mean values (black lines) of the focal fishes’ total distance covered in the arena, mean speed in ROI and whole-body cortisol levels, for each treatment. * P < 0.05, ** P < 0.01, *** P < 0.001.
Mentions: We started the analysis by individually profiling the time spent by the focal fish in each position of the arena during the test. Qualitative analysis using 2D heatmaps and histogram representation, revealed different spatial distribution patterns for each treatment (Fig. 2a). On average BIC fish spent more time closer to the tank wall on the side of the fighting stimulus fish than did BNIC fish, which showed a more dispersed distribution in the arena. A few BNIC fish spent more time in the area closer to one of the two non-interacting stimulus fish. ISOL fish showed on average a dispersed distribution in the arena. As a quantitative measure of proximity towards the stimuli, we analysed for each treatment the group mean percentage of time spent in the region of interest (ROI), comprising 25% of the tank (see Methods, Fig. 1c). BIC fish spent significantly more time in the ROI than ISOL fish, whereas there were no differences between BNIC and ISOL fish (see Fig. 2c and Table 1). The differences between BIC and BNIC fish were also not significant (Table 1). The ISOL fish results (time in ROI = 22.67 ± 3.17%, mean ± SEM, n = 10) matched what would be expected from a uniform distribution in the arena, with the fish showing no particular preference for the ROI and spending on average 25% of the time in 25% (ROI) of the total area (One-sample t-test, t9 = –0.73, P = 0.48). In the BNIC treatment, three (time in ROI = 84.39 ± 4.48%, n = 3) out of the 12 tested fish showed a strong proximity towards the stimuli, which differed from the other nine fish (time in ROI = 27.03 ± 4.46%; n = 9) suggesting a possible bimodality of a subset of the sampled population. To measure the focal fish’s directionality, we analysed individual and group preferred orientations, and also directional focus (see Methods for details) towards the stimulus fish. Circular scatter plots of the individual mean resultant vector’s orientations and directional focus (see Methods), revealed different distribution patterns for each treatment (Fig. 2b,d). We observed that BIC fishes’ mean orientations, strongly clustered around the fighting conspecifics tank’s direction (at 180 degrees). BNIC fish also oriented predominately towards the stimulus direction although scattered as well around other directions, whereas ISOL fish showed a dispersed distribution along different directions. Correspondingly, determination of the group mean resultant vector for each treatment (see Methods, Fig. 2b) revealed that all group mean resultant vectors were oriented towards the stimuli at 180°[αg (BIC) = 182.59°, 95% C.I. = 158.43° – 191.91°, Rg = 0.25, n = 11; αg (BNIC) = 179.07°, Rg = 0.14, n = 12; αg (ISOL) = 186.21°, Rg = 0.042, n = 10], with the corresponding mean vector’ lengths Rg, a measure of directional focus (see Methods for details), showing a higher value for the BIC treatment. Likewise, the individual fish vector’s length projection (R proj) onto the stimulus direction and the corresponding group mean projection (Rgproj) (see Methods and Fig. 2e), were significantly higher for BIC fish than ISOL fish, whereas there were no differences between BNIC and ISOL fish (see Table 1). The differences between BIC and BNIC fish were also not significant (Table 1). Reassuringly, circular uniformity analysis confirmed that only the BIC fish showed a significant directional focus towards the stimulus, with their individual mean orientations’ distribution (Fig. 2b) deviating significantly from uniformity and clustering around the corresponding group mean direction[Moore’s Test, (BIC): P < 0.001; (BNIC): P > 0.1; (ISOL): P > 0.1].

Bottom Line: This ability (aka social eavesdropping) is expected to impact Darwinian fitness, and hence predicts the evolution of cognitive processes that enable social animals to use public information available in the environment.These adaptive specializations in cognition may have evolved both at the level of learning and memory mechanisms, and at the level of input mechanisms, such as attention, which select the information that is available for learning.Here we used zebrafish to test if attention in a social species is tuned to the exchange of information between conspecifics.

View Article: PubMed Central - PubMed

Affiliation: 1] Instituto Gulbenkian de Ciência, Rua da Quinta Grande 6, 2780-156, Oeiras, Portugal [2] ISPA - Instituto Universitário, Rua Jardim do Tabaco 34, 1149-041 Lisboa, Portugal [3] Champalimaud Neuroscience Programme, Champalimaud Centre for the Unknown, Av. de Brasilia, 1400-038 Lisboa, Portugal.

ABSTRACT
Group living animals may eavesdrop on signalling interactions between conspecifics in order to collect adaptively relevant information obtained from others, without incurring in the costs of first-hand information acquisition. This ability (aka social eavesdropping) is expected to impact Darwinian fitness, and hence predicts the evolution of cognitive processes that enable social animals to use public information available in the environment. These adaptive specializations in cognition may have evolved both at the level of learning and memory mechanisms, and at the level of input mechanisms, such as attention, which select the information that is available for learning. Here we used zebrafish to test if attention in a social species is tuned to the exchange of information between conspecifics. Our results show that zebrafish are more attentive towards interacting (i.e. fighting) than towards non-interacting pairs of conspecifics, with the exposure to fighting not increasing activity or stress levels. Moreover, using video playbacks to manipulate form features of the fighting fish, we show that during the assessment phase of the fight, bystanders' attention is more driven by form features of the interacting opponents; whereas during the post-resolution phase, it is driven by biological movement features of the dominant fish chasing the subordinate fish.

No MeSH data available.


Related in: MedlinePlus