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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 Yet, how aging affects complex brain functions, e.g., the ability to acquire new memory when previous experience is no longer valid, is an almost exclusive question of studies in humans and mammalian models.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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Acquisition, memory retention and extinction in old forager bees as compared to mature controls.The foraging durations in the two test groups were either less than 10 days (control) or longer than 15 days (old). (A) The learning performance in the old group was significantly reduced, as compared to the mature controls. Higher LS (up to LS = 5) indicate good learning performance, while lower LS indicate positive responses to the conditioned stimulus (CS, carnation oil) only in few or none (LS = 0) of the CS-US pairings. The graph shows medians and interquartile ranges with n = 133/134 for control and old, respectively. (B) Reduced learning performance in the old group is contrasted by increased performance heterogeneity (F = 1.65, p = 0.002, df1 = 132, df2 = 133, F-test; compare also interquartile ranges in A). Histograms of individual learning scores with n = 133/134 for control and old, respectively). (C) Acquisition, memory retention and extinction. To test acquisition a subset of bees was subjected to 6 CS-US pairings on day 1 (left). On day 3 bees were presented 6 times with the CS alone for testing memory retention (1st trial) and extinction (response decay in the 6th as compared to 1st trial). The y-axis displays the percentage of individuals that responded to the CS by extending the proboscis (PER+). Day 1 with n = 94/92, day 3 with n = 85/64 for control and old, respectively. Differences in individual numbers between day 1 and 3 are mainly caused by mortality, specifically affecting the group of old foragers. (D) No significant difference in memory retention was detected when comparing the response of the two age groups to the first CS only presentation (n = 85/64 for control and old, respectively). After six extinction trials, PER- individuals do not respond to the learned CS-US association, and thereby show extinction. While response decline after extinction trials was less significant in the old group, a direct comparison of both groups does not reveal a significant age affect for extinction of olfactory memory (for details see results section). Asterisks in A, B, D denote significance (A, Chi-square; B, Mann-Whitney U; D, McNemar χ2).
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pone-0013504-g001: Acquisition, memory retention and extinction in old forager bees as compared to mature controls.The foraging durations in the two test groups were either less than 10 days (control) or longer than 15 days (old). (A) The learning performance in the old group was significantly reduced, as compared to the mature controls. Higher LS (up to LS = 5) indicate good learning performance, while lower LS indicate positive responses to the conditioned stimulus (CS, carnation oil) only in few or none (LS = 0) of the CS-US pairings. The graph shows medians and interquartile ranges with n = 133/134 for control and old, respectively. (B) Reduced learning performance in the old group is contrasted by increased performance heterogeneity (F = 1.65, p = 0.002, df1 = 132, df2 = 133, F-test; compare also interquartile ranges in A). Histograms of individual learning scores with n = 133/134 for control and old, respectively). (C) Acquisition, memory retention and extinction. To test acquisition a subset of bees was subjected to 6 CS-US pairings on day 1 (left). On day 3 bees were presented 6 times with the CS alone for testing memory retention (1st trial) and extinction (response decay in the 6th as compared to 1st trial). The y-axis displays the percentage of individuals that responded to the CS by extending the proboscis (PER+). Day 1 with n = 94/92, day 3 with n = 85/64 for control and old, respectively. Differences in individual numbers between day 1 and 3 are mainly caused by mortality, specifically affecting the group of old foragers. (D) No significant difference in memory retention was detected when comparing the response of the two age groups to the first CS only presentation (n = 85/64 for control and old, respectively). After six extinction trials, PER- individuals do not respond to the learned CS-US association, and thereby show extinction. While response decline after extinction trials was less significant in the old group, a direct comparison of both groups does not reveal a significant age affect for extinction of olfactory memory (for details see results section). Asterisks in A, B, D denote significance (A, Chi-square; B, Mann-Whitney U; D, McNemar χ2).

Mentions: For appetitive olfactory acquisition, bees were trained using six odor-sucrose (CS-US) pairings to assess olfactory learning performance. We found that foraging age explained the variation in memory acquisition (Fig. 1A, B). As previously established [14], the median learning score (LS) of bees that foraged for >15 days (old) was significantly lower than for the control (Mann-Whitney U-test Z = -5.24, p<0.001, n = 133/134, df = 1 for control/old, respectively). Also, fewer old forager bees expressed the learned response to the CS-US association (Chi-square test: χ2 = 33.88, p<0.001, n = 133/134, df = 1), where those showing a conditioned behavior showed at least one response (LS≥1) by extending the proboscis (PER+, proboscis extension response), and those not showing the conditioned behavior never responded to the CS alone (LS = 0). Furthermore, an F-test of variance established that old bees were significantly more heterogeneous in their performance than the control (F = 1.65, p = 0.002, df1 = 132, df2 = 133). This increased heterogeneity due to longer foraging is illustrated by larger interquartile ranges for the group of old foragers in Fig. 1A, and by histograms for learning performance values (LS) in Fig. 1B.


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)

Acquisition, memory retention and extinction in old forager bees as compared to mature controls.The foraging durations in the two test groups were either less than 10 days (control) or longer than 15 days (old). (A) The learning performance in the old group was significantly reduced, as compared to the mature controls. Higher LS (up to LS = 5) indicate good learning performance, while lower LS indicate positive responses to the conditioned stimulus (CS, carnation oil) only in few or none (LS = 0) of the CS-US pairings. The graph shows medians and interquartile ranges with n = 133/134 for control and old, respectively. (B) Reduced learning performance in the old group is contrasted by increased performance heterogeneity (F = 1.65, p = 0.002, df1 = 132, df2 = 133, F-test; compare also interquartile ranges in A). Histograms of individual learning scores with n = 133/134 for control and old, respectively). (C) Acquisition, memory retention and extinction. To test acquisition a subset of bees was subjected to 6 CS-US pairings on day 1 (left). On day 3 bees were presented 6 times with the CS alone for testing memory retention (1st trial) and extinction (response decay in the 6th as compared to 1st trial). The y-axis displays the percentage of individuals that responded to the CS by extending the proboscis (PER+). Day 1 with n = 94/92, day 3 with n = 85/64 for control and old, respectively. Differences in individual numbers between day 1 and 3 are mainly caused by mortality, specifically affecting the group of old foragers. (D) No significant difference in memory retention was detected when comparing the response of the two age groups to the first CS only presentation (n = 85/64 for control and old, respectively). After six extinction trials, PER- individuals do not respond to the learned CS-US association, and thereby show extinction. While response decline after extinction trials was less significant in the old group, a direct comparison of both groups does not reveal a significant age affect for extinction of olfactory memory (for details see results section). Asterisks in A, B, D denote significance (A, Chi-square; B, Mann-Whitney U; D, McNemar χ2).
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Related In: Results  -  Collection

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pone-0013504-g001: Acquisition, memory retention and extinction in old forager bees as compared to mature controls.The foraging durations in the two test groups were either less than 10 days (control) or longer than 15 days (old). (A) The learning performance in the old group was significantly reduced, as compared to the mature controls. Higher LS (up to LS = 5) indicate good learning performance, while lower LS indicate positive responses to the conditioned stimulus (CS, carnation oil) only in few or none (LS = 0) of the CS-US pairings. The graph shows medians and interquartile ranges with n = 133/134 for control and old, respectively. (B) Reduced learning performance in the old group is contrasted by increased performance heterogeneity (F = 1.65, p = 0.002, df1 = 132, df2 = 133, F-test; compare also interquartile ranges in A). Histograms of individual learning scores with n = 133/134 for control and old, respectively). (C) Acquisition, memory retention and extinction. To test acquisition a subset of bees was subjected to 6 CS-US pairings on day 1 (left). On day 3 bees were presented 6 times with the CS alone for testing memory retention (1st trial) and extinction (response decay in the 6th as compared to 1st trial). The y-axis displays the percentage of individuals that responded to the CS by extending the proboscis (PER+). Day 1 with n = 94/92, day 3 with n = 85/64 for control and old, respectively. Differences in individual numbers between day 1 and 3 are mainly caused by mortality, specifically affecting the group of old foragers. (D) No significant difference in memory retention was detected when comparing the response of the two age groups to the first CS only presentation (n = 85/64 for control and old, respectively). After six extinction trials, PER- individuals do not respond to the learned CS-US association, and thereby show extinction. While response decline after extinction trials was less significant in the old group, a direct comparison of both groups does not reveal a significant age affect for extinction of olfactory memory (for details see results section). Asterisks in A, B, D denote significance (A, Chi-square; B, Mann-Whitney U; D, McNemar χ2).
Mentions: For appetitive olfactory acquisition, bees were trained using six odor-sucrose (CS-US) pairings to assess olfactory learning performance. We found that foraging age explained the variation in memory acquisition (Fig. 1A, B). As previously established [14], the median learning score (LS) of bees that foraged for >15 days (old) was significantly lower than for the control (Mann-Whitney U-test Z = -5.24, p<0.001, n = 133/134, df = 1 for control/old, respectively). Also, fewer old forager bees expressed the learned response to the CS-US association (Chi-square test: χ2 = 33.88, p<0.001, n = 133/134, df = 1), where those showing a conditioned behavior showed at least one response (LS≥1) by extending the proboscis (PER+, proboscis extension response), and those not showing the conditioned behavior never responded to the CS alone (LS = 0). Furthermore, an F-test of variance established that old bees were significantly more heterogeneous in their performance than the control (F = 1.65, p = 0.002, df1 = 132, df2 = 133). This increased heterogeneity due to longer foraging is illustrated by larger interquartile ranges for the group of old foragers in Fig. 1A, and by histograms for learning performance values (LS) in Fig. 1B.

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