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In the laboratory and during free-flight: old honey bees reveal learning and extinction deficits that mirror mammalian functional decline.

Münch D, Baker N, Kreibich CD, Bråten AT, Amdam GV - PLoS ONE (2010)

Bottom Line: Such studies could demonstrate that afflicted individuals show the loss of several and often-diverse memory faculties, and that performance usually varies more between aged individuals, as compared to conspecifics from younger groups.We demonstrate that reduced olfactory learning performance correlates with a reduced ability to extinguish the spatial memory of an abandoned nest location (spatial memory extinction).Taken together, our findings point to generic features of brain aging and provide the prerequisites to model individual aspects of learning dysfunction with insect models.

View Article: PubMed Central - PubMed

Affiliation: Department of Chemistry, Biotechnology and Food Science, Norwegian University of Life Sciences, Aas, Norway. daniel.munch@umb.no

ABSTRACT
Loss of brain function is one of the most negative and feared aspects of aging. Studies of invertebrates have taught us much about the physiology of aging and how this progression may be slowed. Yet, how aging affects complex brain functions, e.g., the ability to acquire new memory when previous experience is no longer valid, is an almost exclusive question of studies in humans and mammalian models. In these systems, age related cognitive disorders are assessed through composite paradigms that test different performance tasks in the same individual. Such studies could demonstrate that afflicted individuals show the loss of several and often-diverse memory faculties, and that performance usually varies more between aged individuals, as compared to conspecifics from younger groups. No comparable composite surveying approaches are established yet for invertebrate models in aging research. Here we test whether an insect can share patterns of decline similar to those that are commonly observed during mammalian brain aging. Using honey bees, we combine restrained learning with free-flight assays. We demonstrate that reduced olfactory learning performance correlates with a reduced ability to extinguish the spatial memory of an abandoned nest location (spatial memory extinction). Adding to this, we show that learning performance is more variable in old honey bees. Taken together, our findings point to generic features of brain aging and provide the prerequisites to model individual aspects of learning dysfunction with insect models.

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Related in: MedlinePlus

Experimental design used for inducing spatial memory extinction of a nest site and relating this extinction performance with olfactory learning decline.e1–e6 denote the separate events that constituted the spatial memory experiment. The upper row “days to age” depicts the overall timeline of the experiment. To control for foraging duration, foragers of random age were marked in two rounds. The initial day of olfactory learning performance scoring, these foragers constituted a heterogeneous age cohort with fully mature to old individuals that had been foraging for more than 15 respectively 11 days. The middle (“experiment. setup”) and lower rows (“learning rules and tests”) show the sequence of events that were used to induce spatial memories of the different nest sites. Bees returning from foraging flights were marked (event e1). Subsequently, they were moved to a distant test arena with four hive boxes (e2). Except for A, all other hive boxes (‘dummies’) were empty. After foraging, bees were given 4 days for learning to orient towards A. Thereafter, an artificial swarm was produced (e3, compare Fig. 2A) and was moved to location B (e4). Colonies were then given another 4–6 days to learn the spatial setting of the new home site B, while learning to extinguish the memory of the previous home site A, which remained closed (unrewarded ‘dummy’ location). Lastly, the entire worker population of the colony was dumped to the ground (e5). The hive box at B was removed, forcing foragers to orient towards the previous location A or alternative locations C, D (e6). At this time all locations A, C, D were similarly equipped with unrelated queens, young workers (<48 h old) and combs to resemble functioning hives. The next day, marked bees were collected, individual orientation preference was logged, and specimens were subjected to olfactory memory acquisition tests in the laboratory.
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pone-0013504-g003: Experimental design used for inducing spatial memory extinction of a nest site and relating this extinction performance with olfactory learning decline.e1–e6 denote the separate events that constituted the spatial memory experiment. The upper row “days to age” depicts the overall timeline of the experiment. To control for foraging duration, foragers of random age were marked in two rounds. The initial day of olfactory learning performance scoring, these foragers constituted a heterogeneous age cohort with fully mature to old individuals that had been foraging for more than 15 respectively 11 days. The middle (“experiment. setup”) and lower rows (“learning rules and tests”) show the sequence of events that were used to induce spatial memories of the different nest sites. Bees returning from foraging flights were marked (event e1). Subsequently, they were moved to a distant test arena with four hive boxes (e2). Except for A, all other hive boxes (‘dummies’) were empty. After foraging, bees were given 4 days for learning to orient towards A. Thereafter, an artificial swarm was produced (e3, compare Fig. 2A) and was moved to location B (e4). Colonies were then given another 4–6 days to learn the spatial setting of the new home site B, while learning to extinguish the memory of the previous home site A, which remained closed (unrewarded ‘dummy’ location). Lastly, the entire worker population of the colony was dumped to the ground (e5). The hive box at B was removed, forcing foragers to orient towards the previous location A or alternative locations C, D (e6). At this time all locations A, C, D were similarly equipped with unrelated queens, young workers (<48 h old) and combs to resemble functioning hives. The next day, marked bees were collected, individual orientation preference was logged, and specimens were subjected to olfactory memory acquisition tests in the laboratory.

Mentions: (A) Artificial swarm with foragers attracted to a queen. The queen is caged and attached to an iron cross. Swarms, as shown here, were produced prior to moving entire colonies to a new location within an arena of four similar hive boxes (B). Spatial extinction was tested in three separate arenas with four hive boxes. One arena is exemplified here. Colony translocations (white arrow) were used to test the ability of aged bees to extinguish the spatial memory of a previous hive location. (C) Paint marks were applied to track individual foraging age and colony source. (D) In the laboratory, differences in acquisition of olfactory memory were quantified by monitoring the proboscis extension response (PER, black arrow) to the CS (odor, white arrow) during a sequence of 6 CS-US pairings. (e3 and e6 refer to events illustrated in Fig. 3).


In the laboratory and during free-flight: old honey bees reveal learning and extinction deficits that mirror mammalian functional decline.

Münch D, Baker N, Kreibich CD, Bråten AT, Amdam GV - PLoS ONE (2010)

Experimental design used for inducing spatial memory extinction of a nest site and relating this extinction performance with olfactory learning decline.e1–e6 denote the separate events that constituted the spatial memory experiment. The upper row “days to age” depicts the overall timeline of the experiment. To control for foraging duration, foragers of random age were marked in two rounds. The initial day of olfactory learning performance scoring, these foragers constituted a heterogeneous age cohort with fully mature to old individuals that had been foraging for more than 15 respectively 11 days. The middle (“experiment. setup”) and lower rows (“learning rules and tests”) show the sequence of events that were used to induce spatial memories of the different nest sites. Bees returning from foraging flights were marked (event e1). Subsequently, they were moved to a distant test arena with four hive boxes (e2). Except for A, all other hive boxes (‘dummies’) were empty. After foraging, bees were given 4 days for learning to orient towards A. Thereafter, an artificial swarm was produced (e3, compare Fig. 2A) and was moved to location B (e4). Colonies were then given another 4–6 days to learn the spatial setting of the new home site B, while learning to extinguish the memory of the previous home site A, which remained closed (unrewarded ‘dummy’ location). Lastly, the entire worker population of the colony was dumped to the ground (e5). The hive box at B was removed, forcing foragers to orient towards the previous location A or alternative locations C, D (e6). At this time all locations A, C, D were similarly equipped with unrelated queens, young workers (<48 h old) and combs to resemble functioning hives. The next day, marked bees were collected, individual orientation preference was logged, and specimens were subjected to olfactory memory acquisition tests in the laboratory.
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2957435&req=5

pone-0013504-g003: Experimental design used for inducing spatial memory extinction of a nest site and relating this extinction performance with olfactory learning decline.e1–e6 denote the separate events that constituted the spatial memory experiment. The upper row “days to age” depicts the overall timeline of the experiment. To control for foraging duration, foragers of random age were marked in two rounds. The initial day of olfactory learning performance scoring, these foragers constituted a heterogeneous age cohort with fully mature to old individuals that had been foraging for more than 15 respectively 11 days. The middle (“experiment. setup”) and lower rows (“learning rules and tests”) show the sequence of events that were used to induce spatial memories of the different nest sites. Bees returning from foraging flights were marked (event e1). Subsequently, they were moved to a distant test arena with four hive boxes (e2). Except for A, all other hive boxes (‘dummies’) were empty. After foraging, bees were given 4 days for learning to orient towards A. Thereafter, an artificial swarm was produced (e3, compare Fig. 2A) and was moved to location B (e4). Colonies were then given another 4–6 days to learn the spatial setting of the new home site B, while learning to extinguish the memory of the previous home site A, which remained closed (unrewarded ‘dummy’ location). Lastly, the entire worker population of the colony was dumped to the ground (e5). The hive box at B was removed, forcing foragers to orient towards the previous location A or alternative locations C, D (e6). At this time all locations A, C, D were similarly equipped with unrelated queens, young workers (<48 h old) and combs to resemble functioning hives. The next day, marked bees were collected, individual orientation preference was logged, and specimens were subjected to olfactory memory acquisition tests in the laboratory.
Mentions: (A) Artificial swarm with foragers attracted to a queen. The queen is caged and attached to an iron cross. Swarms, as shown here, were produced prior to moving entire colonies to a new location within an arena of four similar hive boxes (B). Spatial extinction was tested in three separate arenas with four hive boxes. One arena is exemplified here. Colony translocations (white arrow) were used to test the ability of aged bees to extinguish the spatial memory of a previous hive location. (C) Paint marks were applied to track individual foraging age and colony source. (D) In the laboratory, differences in acquisition of olfactory memory were quantified by monitoring the proboscis extension response (PER, black arrow) to the CS (odor, white arrow) during a sequence of 6 CS-US pairings. (e3 and e6 refer to events illustrated in Fig. 3).

Bottom Line: Such studies could demonstrate that afflicted individuals show the loss of several and often-diverse memory faculties, and that performance usually varies more between aged individuals, as compared to conspecifics from younger groups.We demonstrate that reduced olfactory learning performance correlates with a reduced ability to extinguish the spatial memory of an abandoned nest location (spatial memory extinction).Taken together, our findings point to generic features of brain aging and provide the prerequisites to model individual aspects of learning dysfunction with insect models.

View Article: PubMed Central - PubMed

Affiliation: Department of Chemistry, Biotechnology and Food Science, Norwegian University of Life Sciences, Aas, Norway. daniel.munch@umb.no

ABSTRACT
Loss of brain function is one of the most negative and feared aspects of aging. Studies of invertebrates have taught us much about the physiology of aging and how this progression may be slowed. Yet, how aging affects complex brain functions, e.g., the ability to acquire new memory when previous experience is no longer valid, is an almost exclusive question of studies in humans and mammalian models. In these systems, age related cognitive disorders are assessed through composite paradigms that test different performance tasks in the same individual. Such studies could demonstrate that afflicted individuals show the loss of several and often-diverse memory faculties, and that performance usually varies more between aged individuals, as compared to conspecifics from younger groups. No comparable composite surveying approaches are established yet for invertebrate models in aging research. Here we test whether an insect can share patterns of decline similar to those that are commonly observed during mammalian brain aging. Using honey bees, we combine restrained learning with free-flight assays. We demonstrate that reduced olfactory learning performance correlates with a reduced ability to extinguish the spatial memory of an abandoned nest location (spatial memory extinction). Adding to this, we show that learning performance is more variable in old honey bees. Taken together, our findings point to generic features of brain aging and provide the prerequisites to model individual aspects of learning dysfunction with insect models.

Show MeSH
Related in: MedlinePlus