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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 associated changes in MB synaptic organization at different times after avoidance learning in 2-day treatment experiments. (A) Foragers’ plant preferences for treated and (B) control subcolonies. Workers had to choose between firethorn (fir) and privet (pri) untreated leaf discs. During two consecutive days after the preference test they were offered treated (firCHX) or untreated (firCtrl) firethorn leaves. Bars show the proportion of taken plant discs. 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). ND lip density increased without volumetric changes of the lip after plant avoidance learning. (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 < 0.01. Treatment: day 0, density: N = 6, volume: N = 7; day 2, N = 6; day 4, density: N = 7, volume: N = 8. Control: day 0, N = 7; day 2, N = 7; day 4, N = 7.
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Figure 5: Long-term memory assessment and associated changes in MB synaptic organization at different times after avoidance learning in 2-day treatment experiments. (A) Foragers’ plant preferences for treated and (B) control subcolonies. Workers had to choose between firethorn (fir) and privet (pri) untreated leaf discs. During two consecutive days after the preference test they were offered treated (firCHX) or untreated (firCtrl) firethorn leaves. Bars show the proportion of taken plant discs. 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). ND lip density increased without volumetric changes of the lip after plant avoidance learning. (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 < 0.01. Treatment: day 0, density: N = 6, volume: N = 7; day 2, N = 6; day 4, density: N = 7, volume: N = 8. Control: day 0, N = 7; day 2, N = 7; day 4, N = 7.

Mentions: Preference tests showed that foragers from both treated and control subcolonies had an initial preference for firethorn leaves (Figures 5A,B, day 0). Foragers from the treated subcolony—in which CHX-infiltrated firethorn leaves were incorporated—showed a clear rejection behavior from the second day after incorporation of the treated leaves into the fungus garden (hereafter referred to as “incorporation”) (GH = 16.95, p = 0.0007, N = 117, df = 3; G-test; Figure 5A). On the other hand, workers from the control subcolony did not change their preference after incorporation of the untreated leaves (GH = 6.48, p = 0.09, N = 125, df = 3; G-Test; Figure 5B). This means that the plant itself was not harmful for the fungus and was still preferred by the ants 4 days after its incorporation. We conclude that ants from the treated subcolony showed long-term avoidance memory evidenced by the rejection of the plant species previously associated with the CHX effects on the fungus.


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 associated changes in MB synaptic organization at different times after avoidance learning in 2-day treatment experiments. (A) Foragers’ plant preferences for treated and (B) control subcolonies. Workers had to choose between firethorn (fir) and privet (pri) untreated leaf discs. During two consecutive days after the preference test they were offered treated (firCHX) or untreated (firCtrl) firethorn leaves. Bars show the proportion of taken plant discs. 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). ND lip density increased without volumetric changes of the lip after plant avoidance learning. (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 < 0.01. Treatment: day 0, density: N = 6, volume: N = 7; day 2, N = 6; day 4, density: N = 7, volume: N = 8. Control: day 0, N = 7; day 2, N = 7; day 4, N = 7.
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Related In: Results  -  Collection

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Figure 5: Long-term memory assessment and associated changes in MB synaptic organization at different times after avoidance learning in 2-day treatment experiments. (A) Foragers’ plant preferences for treated and (B) control subcolonies. Workers had to choose between firethorn (fir) and privet (pri) untreated leaf discs. During two consecutive days after the preference test they were offered treated (firCHX) or untreated (firCtrl) firethorn leaves. Bars show the proportion of taken plant discs. 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). ND lip density increased without volumetric changes of the lip after plant avoidance learning. (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 < 0.01. Treatment: day 0, density: N = 6, volume: N = 7; day 2, N = 6; day 4, density: N = 7, volume: N = 8. Control: day 0, N = 7; day 2, N = 7; day 4, N = 7.
Mentions: Preference tests showed that foragers from both treated and control subcolonies had an initial preference for firethorn leaves (Figures 5A,B, day 0). Foragers from the treated subcolony—in which CHX-infiltrated firethorn leaves were incorporated—showed a clear rejection behavior from the second day after incorporation of the treated leaves into the fungus garden (hereafter referred to as “incorporation”) (GH = 16.95, p = 0.0007, N = 117, df = 3; G-test; Figure 5A). On the other hand, workers from the control subcolony did not change their preference after incorporation of the untreated leaves (GH = 6.48, p = 0.09, N = 125, df = 3; G-Test; Figure 5B). This means that the plant itself was not harmful for the fungus and was still preferred by the ants 4 days after its incorporation. We conclude that ants from the treated subcolony showed long-term avoidance memory evidenced by the rejection of the plant species previously associated with the CHX effects on the fungus.

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