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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

Long-term memory assessment and its associated changes in MB synaptic organization at different times after avoidance learning in 1-day treatment experiments. (A) Foragers’ plant preferences for treated and (B) control subcolonies in a choice experiment between firethorn (fir) and privet (pri) leaves. On day 0, ants were offered treated (firCHX) or untreated (firCtrl) firethorn leaves. Bars show the proportion of taken plant discs at different times after treatment. Different letters indicate significant differences among days (G-Test) and numbers at the bottom of each bar indicate the total number of ants that collected a disc during testing. (C) Density of synapsin-IR boutons in the ND lip and (D) total lip volume at different times after the incorporation of CHX-infiltrated leaves (firCHX, treatment). Following variations during a longer period of time after plant avoidance learning revealed that ND lip density transiently increased without calycal volumetric changes in the treated subcolony. (E) ND lip synapsin-IR boutons density and (F) lip volume at different times after incorporation of the untreated plant (firCtrl, control). Incorporation of control leaves did not promote significant changes in the lip. Dots represent the mean value and solid lines the S.D. Horizontal dotted lines indicate mean bouton density quantified before treatment (day 0). Asterisks indicate significant differences between day 0 and different times after leaves incorporation into the fungus garden; *p < 0.05. Treatment: day 0, N = 5; day 2, N = 8; day 4, N = 8; day 15, N = 6. Control: day 0, N = 7; day 2, N = 7; day 4, N = 8; day 15, N = 8.
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Figure 7: Long-term memory assessment and its associated changes in MB synaptic organization at different times after avoidance learning in 1-day treatment experiments. (A) Foragers’ plant preferences for treated and (B) control subcolonies in a choice experiment between firethorn (fir) and privet (pri) leaves. On day 0, ants were offered treated (firCHX) or untreated (firCtrl) firethorn leaves. Bars show the proportion of taken plant discs at different times after treatment. Different letters indicate significant differences among days (G-Test) and numbers at the bottom of each bar indicate the total number of ants that collected a disc during testing. (C) Density of synapsin-IR boutons in the ND lip and (D) total lip volume at different times after the incorporation of CHX-infiltrated leaves (firCHX, treatment). Following variations during a longer period of time after plant avoidance learning revealed that ND lip density transiently increased without calycal volumetric changes in the treated subcolony. (E) ND lip synapsin-IR boutons density and (F) lip volume at different times after incorporation of the untreated plant (firCtrl, control). Incorporation of control leaves did not promote significant changes in the lip. Dots represent the mean value and solid lines the S.D. Horizontal dotted lines indicate mean bouton density quantified before treatment (day 0). Asterisks indicate significant differences between day 0 and different times after leaves incorporation into the fungus garden; *p < 0.05. Treatment: day 0, N = 5; day 2, N = 8; day 4, N = 8; day 15, N = 6. Control: day 0, N = 7; day 2, N = 7; day 4, N = 8; day 15, N = 8.

Mentions: In accordance with the previous learning experiment, the foragers’ initial preferences for firethorn leaves (Figures 7A,B, day 0) was not modified in control subcolonies after incorporation of the untreated leaves (GH = 3.10, p = 0.54, N = 75, df = 4; G-test; Figure 7B). Ants from treated subcolonies showed a clear rejection behavior at the first day after incorporation, which was still observed 15 days thereafter (GH = 61.11, p < 0.0001, N = 106, df = 4; G-test; Figure 7A), denoting long-term avoidance memory beyond the time observed in the learning experiment 1.


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)

Long-term memory assessment and its associated changes in MB synaptic organization at different times after avoidance learning in 1-day treatment experiments. (A) Foragers’ plant preferences for treated and (B) control subcolonies in a choice experiment between firethorn (fir) and privet (pri) leaves. On day 0, ants were offered treated (firCHX) or untreated (firCtrl) firethorn leaves. Bars show the proportion of taken plant discs at different times after treatment. Different letters indicate significant differences among days (G-Test) and numbers at the bottom of each bar indicate the total number of ants that collected a disc during testing. (C) Density of synapsin-IR boutons in the ND lip and (D) total lip volume at different times after the incorporation of CHX-infiltrated leaves (firCHX, treatment). Following variations during a longer period of time after plant avoidance learning revealed that ND lip density transiently increased without calycal volumetric changes in the treated subcolony. (E) ND lip synapsin-IR boutons density and (F) lip volume at different times after incorporation of the untreated plant (firCtrl, control). Incorporation of control leaves did not promote significant changes in the lip. Dots represent the mean value and solid lines the S.D. Horizontal dotted lines indicate mean bouton density quantified before treatment (day 0). Asterisks indicate significant differences between day 0 and different times after leaves incorporation into the fungus garden; *p < 0.05. Treatment: day 0, N = 5; day 2, N = 8; day 4, N = 8; day 15, N = 6. Control: day 0, N = 7; day 2, N = 7; day 4, N = 8; day 15, N = 8.
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Figure 7: Long-term memory assessment and its associated changes in MB synaptic organization at different times after avoidance learning in 1-day treatment experiments. (A) Foragers’ plant preferences for treated and (B) control subcolonies in a choice experiment between firethorn (fir) and privet (pri) leaves. On day 0, ants were offered treated (firCHX) or untreated (firCtrl) firethorn leaves. Bars show the proportion of taken plant discs at different times after treatment. Different letters indicate significant differences among days (G-Test) and numbers at the bottom of each bar indicate the total number of ants that collected a disc during testing. (C) Density of synapsin-IR boutons in the ND lip and (D) total lip volume at different times after the incorporation of CHX-infiltrated leaves (firCHX, treatment). Following variations during a longer period of time after plant avoidance learning revealed that ND lip density transiently increased without calycal volumetric changes in the treated subcolony. (E) ND lip synapsin-IR boutons density and (F) lip volume at different times after incorporation of the untreated plant (firCtrl, control). Incorporation of control leaves did not promote significant changes in the lip. Dots represent the mean value and solid lines the S.D. Horizontal dotted lines indicate mean bouton density quantified before treatment (day 0). Asterisks indicate significant differences between day 0 and different times after leaves incorporation into the fungus garden; *p < 0.05. Treatment: day 0, N = 5; day 2, N = 8; day 4, N = 8; day 15, N = 6. Control: day 0, N = 7; day 2, N = 7; day 4, N = 8; day 15, N = 8.
Mentions: In accordance with the previous learning experiment, the foragers’ initial preferences for firethorn leaves (Figures 7A,B, day 0) was not modified in control subcolonies after incorporation of the untreated leaves (GH = 3.10, p = 0.54, N = 75, df = 4; G-test; Figure 7B). Ants from treated subcolonies showed a clear rejection behavior at the first day after incorporation, which was still observed 15 days thereafter (GH = 61.11, p < 0.0001, N = 106, df = 4; G-test; Figure 7A), denoting long-term avoidance memory beyond the time observed in the learning experiment 1.

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