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Behavioral and neural plasticity caused by early social experiences: the case of the honeybee.

Arenas A, Ramírez GP, Balbuena MS, Farina WM - Front Physiol (2013)

Bottom Line: Early olfactory experiences lead to stable and long-term associative memories that can be successfully recalled after many days, even at foraging ages.Early rewarded experiences have relevant consequences at the social level too, biasing dance and trophallaxis partner choice and affecting recruitment.Here, we revised recent results in bees' physiology, behavior, and sociobiology to depict how the early experiences affect their cognition abilities and neural-related circuits.

View Article: PubMed Central - PubMed

Affiliation: Grupo de Estudio de Insectos Sociales, Departamento de Biodiversidad y Biología Experimental, Facultad de Ciencias Exactas y Naturales, IFIBYNE-CONICET, Universidad de Buenos Aires Buenos Aires, Argentina.

ABSTRACT
Cognitive experiences during the early stages of life play an important role in shaping future behavior. Behavioral and neural long-term changes after early sensory and associative experiences have been recently reported in the honeybee. This invertebrate is an excellent model for assessing the role of precocious experiences on later behavior due to its extraordinarily tuned division of labor based on age polyethism. These studies are mainly focused on the role and importance of experiences occurred during the first days of the adult lifespan, their impact on foraging decisions, and their contribution to coordinate food gathering. Odor-rewarded experiences during the first days of honeybee adulthood alter the responsiveness to sucrose, making young hive bees more sensitive to assess gustatory features about the nectar brought back to the hive and affecting the dynamic of the food transfers and the propagation of food-related information within the colony. Early olfactory experiences lead to stable and long-term associative memories that can be successfully recalled after many days, even at foraging ages. Also they improve memorizing of new associative learning events later in life. The establishment of early memories promotes stable reorganization of the olfactory circuits inducing structural and functional changes in the antennal lobe (AL). Early rewarded experiences have relevant consequences at the social level too, biasing dance and trophallaxis partner choice and affecting recruitment. Here, we revised recent results in bees' physiology, behavior, and sociobiology to depict how the early experiences affect their cognition abilities and neural-related circuits.

No MeSH data available.


Related in: MedlinePlus

Gustatory responsiveness and memory retention of free-flying bees after the influx of scented sucrose solution. Bees of different age groups: 6/9 days old, 12/16 days old, and foragers were captured from the hive. Gustatory response scores (GRSs) (A) and proboscis extension responses (PER) (B) to the odor solution (LIO, black bars), a novel test odor (phenylacetaldehyde, PHE, gray bars), or both (dark gray bars) were measured during the incoming of unscented sucrose solution (15% w/w) (0 h) or after 8 h and 24 h of foraging on a scented sucrose solution (linalool, LIO, 15% w/w). In addition, number of trophallaxis events per bee during a 10min-observation period was counted from the experimental colony while foragers collected 15% w/w sucrose solution for 8 h (C). White boxes represent the reward program number 1 (P1) in which the colony collected unscented 15% w/w sucrose solution. Gray boxes represent the reward program number 2 (P2) in which bees fed for 4 h from a LIO-scented sucrose solution (15% w/w) and afterwards from an unscented solution of equal concentration. The asterisks indicate statistical differences (Panel A: *p < 0.05, ***p < 0.001, n.s., not significant; Dunn comparison after Kruskal–Wallis test; Panel B: **p < 0.01; G-test; Panel C: **p < 0.01; Mann–Whitney test. After Ramírez et al., 2010. With permission).
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Figure 1: Gustatory responsiveness and memory retention of free-flying bees after the influx of scented sucrose solution. Bees of different age groups: 6/9 days old, 12/16 days old, and foragers were captured from the hive. Gustatory response scores (GRSs) (A) and proboscis extension responses (PER) (B) to the odor solution (LIO, black bars), a novel test odor (phenylacetaldehyde, PHE, gray bars), or both (dark gray bars) were measured during the incoming of unscented sucrose solution (15% w/w) (0 h) or after 8 h and 24 h of foraging on a scented sucrose solution (linalool, LIO, 15% w/w). In addition, number of trophallaxis events per bee during a 10min-observation period was counted from the experimental colony while foragers collected 15% w/w sucrose solution for 8 h (C). White boxes represent the reward program number 1 (P1) in which the colony collected unscented 15% w/w sucrose solution. Gray boxes represent the reward program number 2 (P2) in which bees fed for 4 h from a LIO-scented sucrose solution (15% w/w) and afterwards from an unscented solution of equal concentration. The asterisks indicate statistical differences (Panel A: *p < 0.05, ***p < 0.001, n.s., not significant; Dunn comparison after Kruskal–Wallis test; Panel B: **p < 0.01; G-test; Panel C: **p < 0.01; Mann–Whitney test. After Ramírez et al., 2010. With permission).

Mentions: In a second experiment performed in queen right colonies, Ramírez et al. (2010) showed that 6/9- and 12/16-day-old bees were able to increase their responsiveness 8 h after a controlled influx of scented food (Figure 1A). Concomitantly with changes in GRSs, olfactory memories to the incoming odor were clearly detected in 12/16-day-old bees over the 24 h period, but not in younger bees (Figure 1B). Interestingly gustatory responsiveness did not change in foragers (Figure 1A), indicating that not all the age groups respond equally to variations in chemosensory information. One possibility is that variations among bees of different ages were related to the currently activity the workers perform. Higher sensitivity to sugar in middle age receivers might play a role during nectar distribution, adjusting the probability of accepting food from incoming foragers according to both gustatory and olfactory nectar characteristics (Pankiw et al., 2004). Lowering sucrose response threshold after memory formation could be thereafter a mechanism that, by increasing the occurrence of mouth-to-mouth food exchanges (trophallaxis) between incoming foragers and food-receiving bees, contributes to the coordination of collective tasks soon after an influx of scented nectar. Higher number of trophallaxis events quantified 4 h after a controlled influx of scented food into the hive (Figure 1C) supports this hypothesis.


Behavioral and neural plasticity caused by early social experiences: the case of the honeybee.

Arenas A, Ramírez GP, Balbuena MS, Farina WM - Front Physiol (2013)

Gustatory responsiveness and memory retention of free-flying bees after the influx of scented sucrose solution. Bees of different age groups: 6/9 days old, 12/16 days old, and foragers were captured from the hive. Gustatory response scores (GRSs) (A) and proboscis extension responses (PER) (B) to the odor solution (LIO, black bars), a novel test odor (phenylacetaldehyde, PHE, gray bars), or both (dark gray bars) were measured during the incoming of unscented sucrose solution (15% w/w) (0 h) or after 8 h and 24 h of foraging on a scented sucrose solution (linalool, LIO, 15% w/w). In addition, number of trophallaxis events per bee during a 10min-observation period was counted from the experimental colony while foragers collected 15% w/w sucrose solution for 8 h (C). White boxes represent the reward program number 1 (P1) in which the colony collected unscented 15% w/w sucrose solution. Gray boxes represent the reward program number 2 (P2) in which bees fed for 4 h from a LIO-scented sucrose solution (15% w/w) and afterwards from an unscented solution of equal concentration. The asterisks indicate statistical differences (Panel A: *p < 0.05, ***p < 0.001, n.s., not significant; Dunn comparison after Kruskal–Wallis test; Panel B: **p < 0.01; G-test; Panel C: **p < 0.01; Mann–Whitney test. After Ramírez et al., 2010. With permission).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3750948&req=5

Figure 1: Gustatory responsiveness and memory retention of free-flying bees after the influx of scented sucrose solution. Bees of different age groups: 6/9 days old, 12/16 days old, and foragers were captured from the hive. Gustatory response scores (GRSs) (A) and proboscis extension responses (PER) (B) to the odor solution (LIO, black bars), a novel test odor (phenylacetaldehyde, PHE, gray bars), or both (dark gray bars) were measured during the incoming of unscented sucrose solution (15% w/w) (0 h) or after 8 h and 24 h of foraging on a scented sucrose solution (linalool, LIO, 15% w/w). In addition, number of trophallaxis events per bee during a 10min-observation period was counted from the experimental colony while foragers collected 15% w/w sucrose solution for 8 h (C). White boxes represent the reward program number 1 (P1) in which the colony collected unscented 15% w/w sucrose solution. Gray boxes represent the reward program number 2 (P2) in which bees fed for 4 h from a LIO-scented sucrose solution (15% w/w) and afterwards from an unscented solution of equal concentration. The asterisks indicate statistical differences (Panel A: *p < 0.05, ***p < 0.001, n.s., not significant; Dunn comparison after Kruskal–Wallis test; Panel B: **p < 0.01; G-test; Panel C: **p < 0.01; Mann–Whitney test. After Ramírez et al., 2010. With permission).
Mentions: In a second experiment performed in queen right colonies, Ramírez et al. (2010) showed that 6/9- and 12/16-day-old bees were able to increase their responsiveness 8 h after a controlled influx of scented food (Figure 1A). Concomitantly with changes in GRSs, olfactory memories to the incoming odor were clearly detected in 12/16-day-old bees over the 24 h period, but not in younger bees (Figure 1B). Interestingly gustatory responsiveness did not change in foragers (Figure 1A), indicating that not all the age groups respond equally to variations in chemosensory information. One possibility is that variations among bees of different ages were related to the currently activity the workers perform. Higher sensitivity to sugar in middle age receivers might play a role during nectar distribution, adjusting the probability of accepting food from incoming foragers according to both gustatory and olfactory nectar characteristics (Pankiw et al., 2004). Lowering sucrose response threshold after memory formation could be thereafter a mechanism that, by increasing the occurrence of mouth-to-mouth food exchanges (trophallaxis) between incoming foragers and food-receiving bees, contributes to the coordination of collective tasks soon after an influx of scented nectar. Higher number of trophallaxis events quantified 4 h after a controlled influx of scented food into the hive (Figure 1C) supports this hypothesis.

Bottom Line: Early olfactory experiences lead to stable and long-term associative memories that can be successfully recalled after many days, even at foraging ages.Early rewarded experiences have relevant consequences at the social level too, biasing dance and trophallaxis partner choice and affecting recruitment.Here, we revised recent results in bees' physiology, behavior, and sociobiology to depict how the early experiences affect their cognition abilities and neural-related circuits.

View Article: PubMed Central - PubMed

Affiliation: Grupo de Estudio de Insectos Sociales, Departamento de Biodiversidad y Biología Experimental, Facultad de Ciencias Exactas y Naturales, IFIBYNE-CONICET, Universidad de Buenos Aires Buenos Aires, Argentina.

ABSTRACT
Cognitive experiences during the early stages of life play an important role in shaping future behavior. Behavioral and neural long-term changes after early sensory and associative experiences have been recently reported in the honeybee. This invertebrate is an excellent model for assessing the role of precocious experiences on later behavior due to its extraordinarily tuned division of labor based on age polyethism. These studies are mainly focused on the role and importance of experiences occurred during the first days of the adult lifespan, their impact on foraging decisions, and their contribution to coordinate food gathering. Odor-rewarded experiences during the first days of honeybee adulthood alter the responsiveness to sucrose, making young hive bees more sensitive to assess gustatory features about the nectar brought back to the hive and affecting the dynamic of the food transfers and the propagation of food-related information within the colony. Early olfactory experiences lead to stable and long-term associative memories that can be successfully recalled after many days, even at foraging ages. Also they improve memorizing of new associative learning events later in life. The establishment of early memories promotes stable reorganization of the olfactory circuits inducing structural and functional changes in the antennal lobe (AL). Early rewarded experiences have relevant consequences at the social level too, biasing dance and trophallaxis partner choice and affecting recruitment. Here, we revised recent results in bees' physiology, behavior, and sociobiology to depict how the early experiences affect their cognition abilities and neural-related circuits.

No MeSH data available.


Related in: MedlinePlus