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Daily Thermal Fluctuations Experienced by Pupae via Rhythmic Nursing Behavior Increase Numbers of Mushroom Body Microglomeruli in the Adult Ant Brain.

Falibene A, Roces F, Rössler W, Groh C - Front Behav Neurosci (2016)

Bottom Line: Thermal regimes significantly affected the large (non-dense) olfactory lip region of the adult MB calyx, while changes in the dense lip and the visual collar were less evident.We conclude that rhythmic control of brood temperature by nursing ants optimizes brain development by increasing MG densities and numbers in specific brain areas.Resulting differences in synaptic microcircuits are expected to affect sensory processing and learning abilities in adult ants, and may also promote interindividual behavioral variability within colonies.

View Article: PubMed Central - PubMed

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

ABSTRACT
Social insects control brood development by using different thermoregulatory strategies. Camponotus mus ants expose their brood to daily temperature fluctuations by translocating them inside the nest following a circadian rhythm of thermal preferences. At the middle of the photophase brood is moved to locations at 30.8°C; 8 h later, during the night, the brood is transferred back to locations at 27.5°C. We investigated whether daily thermal fluctuations experienced by developing pupae affect the neuroarchitecture in the adult brain, in particular in sensory input regions of the mushroom bodies (MB calyces). The complexity of synaptic microcircuits was estimated by quantifying MB-calyx volumes together with densities of presynaptic boutons of microglomeruli (MG) in the olfactory lip and visual collar regions. We compared young adult workers that were reared either under controlled daily thermal fluctuations of different amplitudes, or at different constant temperatures. Thermal regimes significantly affected the large (non-dense) olfactory lip region of the adult MB calyx, while changes in the dense lip and the visual collar were less evident. Thermal fluctuations mimicking the amplitudes of natural temperature fluctuations via circadian rhythmic translocation of pupae by nurses (amplitude 3.3°C) lead to higher numbers of MG in the MB calyces compared to those in pupae reared at smaller or larger thermal amplitudes (0.0, 1.5, 9.6°C), or at constant temperatures (25.4, 35.0°C). We conclude that rhythmic control of brood temperature by nursing ants optimizes brain development by increasing MG densities and numbers in specific brain areas. Resulting differences in synaptic microcircuits are expected to affect sensory processing and learning abilities in adult ants, and may also promote interindividual behavioral variability within colonies.

No MeSH data available.


Related in: MedlinePlus

Immunofluorescence staining with anti-synapsin antibody, 3D reconstruction, and MG quantification in brains of 2-day old C. mus workers. (A) Frontal overview of a brain in a central plane. Higher magnification of the area marked by the box is shown in (D). (B) 3D reconstruction of the brain showing the major neuropils. (C) Frontal plane of the 3D reconstruction of the MB calyx showing the visual collar, and the dense (D) and non-dense (ND) olfactory lip subregions. (D) Higher magnification of the medial MB calyx (box shown in A). Boxes 1–2, 3–4, and 5–6 indicate the volumes used for quantification of the presynaptic boutons in the ND lip, D lip and collar regions of the MB calyces, respectively. AL, antennal lobe; co, collar; CX, central complex; LCA, lateral calyx; MB, mushroom bodies; MCA, medial calyx; OL, optic lobe; PED, pedunculus. Scale bars: (A,B) 100 μm; (C,D) 20 μm.
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Figure 1: Immunofluorescence staining with anti-synapsin antibody, 3D reconstruction, and MG quantification in brains of 2-day old C. mus workers. (A) Frontal overview of a brain in a central plane. Higher magnification of the area marked by the box is shown in (D). (B) 3D reconstruction of the brain showing the major neuropils. (C) Frontal plane of the 3D reconstruction of the MB calyx showing the visual collar, and the dense (D) and non-dense (ND) olfactory lip subregions. (D) Higher magnification of the medial MB calyx (box shown in A). Boxes 1–2, 3–4, and 5–6 indicate the volumes used for quantification of the presynaptic boutons in the ND lip, D lip and collar regions of the MB calyces, respectively. AL, antennal lobe; co, collar; CX, central complex; LCA, lateral calyx; MB, mushroom bodies; MCA, medial calyx; OL, optic lobe; PED, pedunculus. Scale bars: (A,B) 100 μm; (C,D) 20 μm.

Mentions: During the pupal phase in holometabolous insects such as Hymenoptera, major anatomical changes take place. The central nervous system is extensively remodeled, including for example the metamorphic reorganization of the mushroom bodies (MBs) (ants: Ishii et al., 2005; bees: Farris et al., 1999; Schröter and Malun, 2000; Fahrbach, 2006; Groh and Rössler, 2008). The MBs are high-level sensory integration centers in the insect brain involved in learning, memory formation, and orientation (Erber et al., 1980; Menzel, 1990, 1999; Hammer and Menzel, 1995; Strausfeld et al., 1998; Heisenberg, 2003; Davis, 2005; Giurfa, 2007; Hourcade et al., 2010; Falibene et al., 2015). In social Hymenoptera, the MBs are particularly large and receive olfactory (MB calyx lip) and visual (MB calyx collar) information (Gronenberg, 2001; Groh et al., 2014; Yilmaz et al., 2016; Figures 1A–C). In the calyces, projection neurons (PNs) originating from the antennal and optic lobes terminate in large presynaptic boutons surrounded by postsynaptic dendritic spines of MB intrinsic neurons (Kenyon cells, KCs) forming characteristic synaptic complexes termed microglomeruli (MG) (Ganeshina and Menzel, 2001; Gronenberg, 2001; Frambach et al., 2004; Groh et al., 2004, 2006; Seid and Wehner, 2008). Several studies in ants and bees have demonstrated a high level of plasticity of MG associated with behavioral transitions, age, sensory exposure, as well as associative learning and long-term memory formation (Seid et al., 2005; Seid and Wehner, 2009; Hourcade et al., 2010; Stieb et al., 2010, 2012; Groh et al., 2012; Scholl et al., 2014; Falibene et al., 2015; Muenz et al., 2015; Yilmaz et al., 2016). In the honeybee, differences in constant temperatures experienced during pupal development were shown to affect the MB-calyx neuroarchitecture in the adult brain (Groh et al., 2004, 2006).


Daily Thermal Fluctuations Experienced by Pupae via Rhythmic Nursing Behavior Increase Numbers of Mushroom Body Microglomeruli in the Adult Ant Brain.

Falibene A, Roces F, Rössler W, Groh C - Front Behav Neurosci (2016)

Immunofluorescence staining with anti-synapsin antibody, 3D reconstruction, and MG quantification in brains of 2-day old C. mus workers. (A) Frontal overview of a brain in a central plane. Higher magnification of the area marked by the box is shown in (D). (B) 3D reconstruction of the brain showing the major neuropils. (C) Frontal plane of the 3D reconstruction of the MB calyx showing the visual collar, and the dense (D) and non-dense (ND) olfactory lip subregions. (D) Higher magnification of the medial MB calyx (box shown in A). Boxes 1–2, 3–4, and 5–6 indicate the volumes used for quantification of the presynaptic boutons in the ND lip, D lip and collar regions of the MB calyces, respectively. AL, antennal lobe; co, collar; CX, central complex; LCA, lateral calyx; MB, mushroom bodies; MCA, medial calyx; OL, optic lobe; PED, pedunculus. Scale bars: (A,B) 100 μm; (C,D) 20 μm.
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Related In: Results  -  Collection

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Figure 1: Immunofluorescence staining with anti-synapsin antibody, 3D reconstruction, and MG quantification in brains of 2-day old C. mus workers. (A) Frontal overview of a brain in a central plane. Higher magnification of the area marked by the box is shown in (D). (B) 3D reconstruction of the brain showing the major neuropils. (C) Frontal plane of the 3D reconstruction of the MB calyx showing the visual collar, and the dense (D) and non-dense (ND) olfactory lip subregions. (D) Higher magnification of the medial MB calyx (box shown in A). Boxes 1–2, 3–4, and 5–6 indicate the volumes used for quantification of the presynaptic boutons in the ND lip, D lip and collar regions of the MB calyces, respectively. AL, antennal lobe; co, collar; CX, central complex; LCA, lateral calyx; MB, mushroom bodies; MCA, medial calyx; OL, optic lobe; PED, pedunculus. Scale bars: (A,B) 100 μm; (C,D) 20 μm.
Mentions: During the pupal phase in holometabolous insects such as Hymenoptera, major anatomical changes take place. The central nervous system is extensively remodeled, including for example the metamorphic reorganization of the mushroom bodies (MBs) (ants: Ishii et al., 2005; bees: Farris et al., 1999; Schröter and Malun, 2000; Fahrbach, 2006; Groh and Rössler, 2008). The MBs are high-level sensory integration centers in the insect brain involved in learning, memory formation, and orientation (Erber et al., 1980; Menzel, 1990, 1999; Hammer and Menzel, 1995; Strausfeld et al., 1998; Heisenberg, 2003; Davis, 2005; Giurfa, 2007; Hourcade et al., 2010; Falibene et al., 2015). In social Hymenoptera, the MBs are particularly large and receive olfactory (MB calyx lip) and visual (MB calyx collar) information (Gronenberg, 2001; Groh et al., 2014; Yilmaz et al., 2016; Figures 1A–C). In the calyces, projection neurons (PNs) originating from the antennal and optic lobes terminate in large presynaptic boutons surrounded by postsynaptic dendritic spines of MB intrinsic neurons (Kenyon cells, KCs) forming characteristic synaptic complexes termed microglomeruli (MG) (Ganeshina and Menzel, 2001; Gronenberg, 2001; Frambach et al., 2004; Groh et al., 2004, 2006; Seid and Wehner, 2008). Several studies in ants and bees have demonstrated a high level of plasticity of MG associated with behavioral transitions, age, sensory exposure, as well as associative learning and long-term memory formation (Seid et al., 2005; Seid and Wehner, 2009; Hourcade et al., 2010; Stieb et al., 2010, 2012; Groh et al., 2012; Scholl et al., 2014; Falibene et al., 2015; Muenz et al., 2015; Yilmaz et al., 2016). In the honeybee, differences in constant temperatures experienced during pupal development were shown to affect the MB-calyx neuroarchitecture in the adult brain (Groh et al., 2004, 2006).

Bottom Line: Thermal regimes significantly affected the large (non-dense) olfactory lip region of the adult MB calyx, while changes in the dense lip and the visual collar were less evident.We conclude that rhythmic control of brood temperature by nursing ants optimizes brain development by increasing MG densities and numbers in specific brain areas.Resulting differences in synaptic microcircuits are expected to affect sensory processing and learning abilities in adult ants, and may also promote interindividual behavioral variability within colonies.

View Article: PubMed Central - PubMed

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

ABSTRACT
Social insects control brood development by using different thermoregulatory strategies. Camponotus mus ants expose their brood to daily temperature fluctuations by translocating them inside the nest following a circadian rhythm of thermal preferences. At the middle of the photophase brood is moved to locations at 30.8°C; 8 h later, during the night, the brood is transferred back to locations at 27.5°C. We investigated whether daily thermal fluctuations experienced by developing pupae affect the neuroarchitecture in the adult brain, in particular in sensory input regions of the mushroom bodies (MB calyces). The complexity of synaptic microcircuits was estimated by quantifying MB-calyx volumes together with densities of presynaptic boutons of microglomeruli (MG) in the olfactory lip and visual collar regions. We compared young adult workers that were reared either under controlled daily thermal fluctuations of different amplitudes, or at different constant temperatures. Thermal regimes significantly affected the large (non-dense) olfactory lip region of the adult MB calyx, while changes in the dense lip and the visual collar were less evident. Thermal fluctuations mimicking the amplitudes of natural temperature fluctuations via circadian rhythmic translocation of pupae by nurses (amplitude 3.3°C) lead to higher numbers of MG in the MB calyces compared to those in pupae reared at smaller or larger thermal amplitudes (0.0, 1.5, 9.6°C), or at constant temperatures (25.4, 35.0°C). We conclude that rhythmic control of brood temperature by nursing ants optimizes brain development by increasing MG densities and numbers in specific brain areas. Resulting differences in synaptic microcircuits are expected to affect sensory processing and learning abilities in adult ants, and may also promote interindividual behavioral variability within colonies.

No MeSH data available.


Related in: MedlinePlus