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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

Extinction response of early olfactory memories during five testing events in the proboscis extension response (PER). Schedules along the adult lifespan were indicated above for each experimental series. (A) Caged bees were offered a scented sugar solution for four consecutive days (gray boxes), and their olfactory memories evaluated at 17 days of age (black arrow). PER to LIO (left panel) or PHE (right panel) were tested when they were offered alone in the sugar solution. (B) In addition to the scented solution received for four consecutive days at 5–8 and 9–12 days of age (gray boxes, see A), an alternative scented food was previously offered (1–4 or 5–8 days old, dark gray boxes). As result three different treatments were obtained: 1–4 + 5–8, 1–4 + 9–12, and 5–8 + 9–12. (C) An odor was exposed as volatile compound for four consecutive days (crossed boxes) before caged bees were offered the scented sugar solution (gray boxes). Whenever LIO was used as the rewarded odor, PHE was used as the non-rewarded or exposed one and vice versa. The asterisks indicate statistical differences between age classes (***p < 0.001, *p < 0.05; post-doc comparison after RM-ANOVA test). The number of subjects within each experimental series was balanced and the number per treatment is indicated on each graph. (After Arenas et al., 2009a. With permission).
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Figure 2: Extinction response of early olfactory memories during five testing events in the proboscis extension response (PER). Schedules along the adult lifespan were indicated above for each experimental series. (A) Caged bees were offered a scented sugar solution for four consecutive days (gray boxes), and their olfactory memories evaluated at 17 days of age (black arrow). PER to LIO (left panel) or PHE (right panel) were tested when they were offered alone in the sugar solution. (B) In addition to the scented solution received for four consecutive days at 5–8 and 9–12 days of age (gray boxes, see A), an alternative scented food was previously offered (1–4 or 5–8 days old, dark gray boxes). As result three different treatments were obtained: 1–4 + 5–8, 1–4 + 9–12, and 5–8 + 9–12. (C) An odor was exposed as volatile compound for four consecutive days (crossed boxes) before caged bees were offered the scented sugar solution (gray boxes). Whenever LIO was used as the rewarded odor, PHE was used as the non-rewarded or exposed one and vice versa. The asterisks indicate statistical differences between age classes (***p < 0.001, *p < 0.05; post-doc comparison after RM-ANOVA test). The number of subjects within each experimental series was balanced and the number per treatment is indicated on each graph. (After Arenas et al., 2009a. With permission).

Mentions: Because consolidation of olfactory memories established at 5–8 days of age might take place through changes that modify structure-function relations when the olfactory system finally matures (Masson and Arnold, 1987; Masson et al., 1993; Winnington et al., 1996; Farris et al., 2001), early olfactory experiences could be important for the complete maturation of the neural pathways. To test whether olfactory memories established later in life are better retrieved if the honeybees have been previously exposed to an early olfactory stimulation, memories established in 5–8 or 9/12-day-old bees were tested after the exposure to a rewarded or unrewarded experience (Arenas et al., 2009a). Briefly, memories established at 5–8 or 9–12 days of age (by means of the offering of scented food, for details see Arenas and Farina, 2008; Figure 2A) were contrasted against those obtained in bees that, in addition to the latter experience, had been subjected to the offering of a second and different scented food at 1–4 or 5–8 days of age (Figure 2B), or exposed to a pure volatile compound delivered in the rearing environment (Figure 2C). Memories quantified in the PER-paradigm by the repeated presentation of the conditioned stimulus (CS) without reinforcement (i.e., 5-trials extinction test; Garelick and Storm, 2005) differed according to the timing and the nature of the prior sensory input (Figure 2). Memories recorded in bees pre-exposed to the rewarded olfactory input (Figure 2B) differed from those obtained in single-odor exposure bees (Figure 2A). These results indicate that early experiences either at the first 4 days of adulthood or at 5–8 days of age clearly enhanced the level of retention of odor-rewarded memories established later in life (at 5–8 or 9–12 days of age). Interestingly, memories established at 9–12 days of age were also improved by the pre-exposure of volatiles in the rearing environment, though its effect was weaker than the one found for the odor-rewarded experiences (Figure 2C). Results coming from rewarded and non-rewarded experiences that precede associative learning showed that relatively brief olfactory stimulations at the early stages of the adult bee's lifespan improve the memorizing process of new learning events.


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)

Extinction response of early olfactory memories during five testing events in the proboscis extension response (PER). Schedules along the adult lifespan were indicated above for each experimental series. (A) Caged bees were offered a scented sugar solution for four consecutive days (gray boxes), and their olfactory memories evaluated at 17 days of age (black arrow). PER to LIO (left panel) or PHE (right panel) were tested when they were offered alone in the sugar solution. (B) In addition to the scented solution received for four consecutive days at 5–8 and 9–12 days of age (gray boxes, see A), an alternative scented food was previously offered (1–4 or 5–8 days old, dark gray boxes). As result three different treatments were obtained: 1–4 + 5–8, 1–4 + 9–12, and 5–8 + 9–12. (C) An odor was exposed as volatile compound for four consecutive days (crossed boxes) before caged bees were offered the scented sugar solution (gray boxes). Whenever LIO was used as the rewarded odor, PHE was used as the non-rewarded or exposed one and vice versa. The asterisks indicate statistical differences between age classes (***p < 0.001, *p < 0.05; post-doc comparison after RM-ANOVA test). The number of subjects within each experimental series was balanced and the number per treatment is indicated on each graph. (After Arenas et al., 2009a. With permission).
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 2: Extinction response of early olfactory memories during five testing events in the proboscis extension response (PER). Schedules along the adult lifespan were indicated above for each experimental series. (A) Caged bees were offered a scented sugar solution for four consecutive days (gray boxes), and their olfactory memories evaluated at 17 days of age (black arrow). PER to LIO (left panel) or PHE (right panel) were tested when they were offered alone in the sugar solution. (B) In addition to the scented solution received for four consecutive days at 5–8 and 9–12 days of age (gray boxes, see A), an alternative scented food was previously offered (1–4 or 5–8 days old, dark gray boxes). As result three different treatments were obtained: 1–4 + 5–8, 1–4 + 9–12, and 5–8 + 9–12. (C) An odor was exposed as volatile compound for four consecutive days (crossed boxes) before caged bees were offered the scented sugar solution (gray boxes). Whenever LIO was used as the rewarded odor, PHE was used as the non-rewarded or exposed one and vice versa. The asterisks indicate statistical differences between age classes (***p < 0.001, *p < 0.05; post-doc comparison after RM-ANOVA test). The number of subjects within each experimental series was balanced and the number per treatment is indicated on each graph. (After Arenas et al., 2009a. With permission).
Mentions: Because consolidation of olfactory memories established at 5–8 days of age might take place through changes that modify structure-function relations when the olfactory system finally matures (Masson and Arnold, 1987; Masson et al., 1993; Winnington et al., 1996; Farris et al., 2001), early olfactory experiences could be important for the complete maturation of the neural pathways. To test whether olfactory memories established later in life are better retrieved if the honeybees have been previously exposed to an early olfactory stimulation, memories established in 5–8 or 9/12-day-old bees were tested after the exposure to a rewarded or unrewarded experience (Arenas et al., 2009a). Briefly, memories established at 5–8 or 9–12 days of age (by means of the offering of scented food, for details see Arenas and Farina, 2008; Figure 2A) were contrasted against those obtained in bees that, in addition to the latter experience, had been subjected to the offering of a second and different scented food at 1–4 or 5–8 days of age (Figure 2B), or exposed to a pure volatile compound delivered in the rearing environment (Figure 2C). Memories quantified in the PER-paradigm by the repeated presentation of the conditioned stimulus (CS) without reinforcement (i.e., 5-trials extinction test; Garelick and Storm, 2005) differed according to the timing and the nature of the prior sensory input (Figure 2). Memories recorded in bees pre-exposed to the rewarded olfactory input (Figure 2B) differed from those obtained in single-odor exposure bees (Figure 2A). These results indicate that early experiences either at the first 4 days of adulthood or at 5–8 days of age clearly enhanced the level of retention of odor-rewarded memories established later in life (at 5–8 or 9–12 days of age). Interestingly, memories established at 9–12 days of age were also improved by the pre-exposure of volatiles in the rearing environment, though its effect was weaker than the one found for the odor-rewarded experiences (Figure 2C). Results coming from rewarded and non-rewarded experiences that precede associative learning showed that relatively brief olfactory stimulations at the early stages of the adult bee's lifespan improve the memorizing process of new learning events.

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