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Long-term avoidance memory formation is associated with a transient increase in mushroom body synaptic complexes in leaf-cutting ants.

Falibene A, Roces F, Rössler W - Front Behav Neurosci (2015)

Bottom Line: Long-term avoidance memory formation was associated with a transient change in MG densities.At days 4 and 15 after learning-when ants still showed plant avoidance-MG densities had decreased to the initial state.Sensory exposure by the simultaneous collection of several, instead of one, non-harmful plant species resulted in a decrease in MG densities in the olfactory lip.

View Article: PubMed Central - PubMed

Affiliation: Department of Behavioral Physiology and Sociobiology, Biozentrum, University of Würzburg Würzburg, Germany.

ABSTRACT
Long-term behavioral changes related to learning and experience have been shown to be associated with structural remodeling in the brain. Leaf-cutting ants learn to avoid previously preferred plants after they have proved harmful for their symbiotic fungus, a process that involves long-term olfactory memory. We studied the dynamics of brain microarchitectural changes after long-term olfactory memory formation following avoidance learning in Acromyrmex ambiguus. After performing experiments to control for possible neuronal changes related to age and body size, we quantified synaptic complexes (microglomeruli, MG) in olfactory regions of the mushroom bodies (MBs) at different times after learning. Long-term avoidance memory formation was associated with a transient change in MG densities. Two days after learning, MG density was higher than before learning. At days 4 and 15 after learning-when ants still showed plant avoidance-MG densities had decreased to the initial state. The structural reorganization of MG triggered by long-term avoidance memory formation clearly differed from changes promoted by pure exposure to and collection of novel plants with distinct odors. Sensory exposure by the simultaneous collection of several, instead of one, non-harmful plant species resulted in a decrease in MG densities in the olfactory lip. We hypothesize that while sensory exposure leads to MG pruning in the MB olfactory lip, the formation of long-term avoidance memory involves an initial growth of new MG followed by subsequent pruning.

No MeSH data available.


Related in: MedlinePlus

Age-dependent structural plasticity in the MB calyces. (A) Bouton density in both the ND and D lip subregions of the MB calyces. Number of boutons per area increased with age in the ND lip and remained constant in the D lip, where the overall density was higher. (B) Total lip volume varied with ant age. Dots represent the mean value of each group and lines the S.D. Asterisks indicate significant differences between lip subregions (ND vs. D lip): ** p < 0.01; *** p < 0.001. Different letters indicate significant differences in ND lip or lip volume among ages. One-day old, N = 9; 1-week old, N = 8; 1-month old, N = 5; outside-workers, N = 6.
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Figure 2: Age-dependent structural plasticity in the MB calyces. (A) Bouton density in both the ND and D lip subregions of the MB calyces. Number of boutons per area increased with age in the ND lip and remained constant in the D lip, where the overall density was higher. (B) Total lip volume varied with ant age. Dots represent the mean value of each group and lines the S.D. Asterisks indicate significant differences between lip subregions (ND vs. D lip): ** p < 0.01; *** p < 0.001. Different letters indicate significant differences in ND lip or lip volume among ages. One-day old, N = 9; 1-week old, N = 8; 1-month old, N = 5; outside-workers, N = 6.

Mentions: Age-related differences were found in the olfactory lip region of the MB in A. ambiguus (Figure 1). In 1-day old workers, the inner subregion of the lip (ND lip) showed an overall weaker staining compared to the outer subregion (D lip) (Figures 1A–C). These differences were less obvious in older individuals (Figures 1D–I). The density of synapsin-IR boutons in the ND lip was lower than in the D lip for all age groups (age x lip-subregion: F3,23 = 5.15, p = 0.007. Lip-subregion simple effect: p ≤ 0.005, for all ages; RM-ANOVA; Figure 2A). This is in accordance with the results found in A. vollenweideri leaf-cutting ants of unknown ages (Groh et al., 2014). Boutons continuously increased in density with age from 1-day to 1-month old workers specifically in the ND lip (age in ND lip simple effect: F3,46 = 13.44, p < 0.0001; RM-ANOVA). The ND lip in one-day old ants, on average, contained only 57% of the boutons found in 1-month old ants, and 1-week after eclosion this number rose to 86%. The differences between 1-month old ants and outside workers, however, were no longer significant. Here, no significant age-related difference was found for the D lip density (age in D lip simple effect: F3,46 = 2.20, p = 0.10; RM-ANOVA).


Long-term avoidance memory formation is associated with a transient increase in mushroom body synaptic complexes in leaf-cutting ants.

Falibene A, Roces F, Rössler W - Front Behav Neurosci (2015)

Age-dependent structural plasticity in the MB calyces. (A) Bouton density in both the ND and D lip subregions of the MB calyces. Number of boutons per area increased with age in the ND lip and remained constant in the D lip, where the overall density was higher. (B) Total lip volume varied with ant age. Dots represent the mean value of each group and lines the S.D. Asterisks indicate significant differences between lip subregions (ND vs. D lip): ** p < 0.01; *** p < 0.001. Different letters indicate significant differences in ND lip or lip volume among ages. One-day old, N = 9; 1-week old, N = 8; 1-month old, N = 5; outside-workers, N = 6.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4389540&req=5

Figure 2: Age-dependent structural plasticity in the MB calyces. (A) Bouton density in both the ND and D lip subregions of the MB calyces. Number of boutons per area increased with age in the ND lip and remained constant in the D lip, where the overall density was higher. (B) Total lip volume varied with ant age. Dots represent the mean value of each group and lines the S.D. Asterisks indicate significant differences between lip subregions (ND vs. D lip): ** p < 0.01; *** p < 0.001. Different letters indicate significant differences in ND lip or lip volume among ages. One-day old, N = 9; 1-week old, N = 8; 1-month old, N = 5; outside-workers, N = 6.
Mentions: Age-related differences were found in the olfactory lip region of the MB in A. ambiguus (Figure 1). In 1-day old workers, the inner subregion of the lip (ND lip) showed an overall weaker staining compared to the outer subregion (D lip) (Figures 1A–C). These differences were less obvious in older individuals (Figures 1D–I). The density of synapsin-IR boutons in the ND lip was lower than in the D lip for all age groups (age x lip-subregion: F3,23 = 5.15, p = 0.007. Lip-subregion simple effect: p ≤ 0.005, for all ages; RM-ANOVA; Figure 2A). This is in accordance with the results found in A. vollenweideri leaf-cutting ants of unknown ages (Groh et al., 2014). Boutons continuously increased in density with age from 1-day to 1-month old workers specifically in the ND lip (age in ND lip simple effect: F3,46 = 13.44, p < 0.0001; RM-ANOVA). The ND lip in one-day old ants, on average, contained only 57% of the boutons found in 1-month old ants, and 1-week after eclosion this number rose to 86%. The differences between 1-month old ants and outside workers, however, were no longer significant. Here, no significant age-related difference was found for the D lip density (age in D lip simple effect: F3,46 = 2.20, p = 0.10; RM-ANOVA).

Bottom Line: Long-term avoidance memory formation was associated with a transient change in MG densities.At days 4 and 15 after learning-when ants still showed plant avoidance-MG densities had decreased to the initial state.Sensory exposure by the simultaneous collection of several, instead of one, non-harmful plant species resulted in a decrease in MG densities in the olfactory lip.

View Article: PubMed Central - PubMed

Affiliation: Department of Behavioral Physiology and Sociobiology, Biozentrum, University of Würzburg Würzburg, Germany.

ABSTRACT
Long-term behavioral changes related to learning and experience have been shown to be associated with structural remodeling in the brain. Leaf-cutting ants learn to avoid previously preferred plants after they have proved harmful for their symbiotic fungus, a process that involves long-term olfactory memory. We studied the dynamics of brain microarchitectural changes after long-term olfactory memory formation following avoidance learning in Acromyrmex ambiguus. After performing experiments to control for possible neuronal changes related to age and body size, we quantified synaptic complexes (microglomeruli, MG) in olfactory regions of the mushroom bodies (MBs) at different times after learning. Long-term avoidance memory formation was associated with a transient change in MG densities. Two days after learning, MG density was higher than before learning. At days 4 and 15 after learning-when ants still showed plant avoidance-MG densities had decreased to the initial state. The structural reorganization of MG triggered by long-term avoidance memory formation clearly differed from changes promoted by pure exposure to and collection of novel plants with distinct odors. Sensory exposure by the simultaneous collection of several, instead of one, non-harmful plant species resulted in a decrease in MG densities in the olfactory lip. We hypothesize that while sensory exposure leads to MG pruning in the MB olfactory lip, the formation of long-term avoidance memory involves an initial growth of new MG followed by subsequent pruning.

No MeSH data available.


Related in: MedlinePlus