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Representation of thermal information in the antennal lobe of leaf-cutting ants.

Ruchty M, Helmchen F, Wehner R, Kleineidam CJ - Front Behav Neurosci (2010)

Bottom Line: Here we selectively stained the three neurons found in single Sc and tracked their axons into the brain of Atta vollenweideri workers.Based on the general representation of thermal information in the antennal lobe and functional data on the Sc-glomeruli we conclude that temperature stimuli received by Sc are processed in the medial of the three target glomeruli.The present study reveals an important role of the antennal lobe in temperature processing and links a specific thermosensitive neuron to its central target glomerulus.

View Article: PubMed Central - PubMed

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

ABSTRACT
Insects are equipped with various types of antennal sensilla, which house thermosensitive neurons adapted to receive different parameters of the thermal environment for a variety of temperature-guided behaviors. In the leaf-cutting ant Atta vollenweideri, the physiology and the morphology of the thermosensitive sensillum coeloconicum (Sc) has been thoroughly investigated. However, the central projections of its receptor neurons are unknown. Here we selectively stained the three neurons found in single Sc and tracked their axons into the brain of Atta vollenweideri workers. Each of the three axons terminates in a single glomerulus of the antennal lobe (Sc-glomeruli). Two of the innervated glomeruli are adjacent to each other and are located laterally, while the third one is clearly separated and located medially in the antennal lobe. Using two-photon Ca(2+) imaging of antennal lobe projection neurons, we studied where in the antennal lobe thermal information is represented. In the 11 investigated antennal lobes, we found up to 10 different glomeruli in a single specimen responding to temperature stimulation. Both, warm- and cold-sensitive glomeruli could be identified. The thermosensitive glomeruli were mainly located in the medial part of the antennal lobe. Based on the general representation of thermal information in the antennal lobe and functional data on the Sc-glomeruli we conclude that temperature stimuli received by Sc are processed in the medial of the three target glomeruli. The present study reveals an important role of the antennal lobe in temperature processing and links a specific thermosensitive neuron to its central target glomerulus.

No MeSH data available.


Temperature-evoked neuronal activity in antennal lobe projection neurons. (A,B) Upon stimulation with 15°C cold air (indicated as blue bars), two glomeruli of this optical section change their neuronal activity. Based on their response properties, the glomeruli classify as warm- and cold-sensitive, respectively (red and blue/white ROI). The repeated stimulation (n = 4) induced changes in ΔF/F of up to 20% in the cold-sensitive glomerulus and about 10% in the warm-sensitive glomerulus (raw data traces shown). (C) The average fluorescence change in antennal lobe projection neurons in response to the four individual stimulation trials (30°C, indicated as red bars) is shown as false color image sequence. Based on the color code used, cold-sensitive glomeruli appear in blue whereas warm-sensitivity is indicated by red pixels. (D) The average fluorescence change (mean of four stimulation trials) of individual glomeruli is shown. Cold- and warm-sensitivity is indicated by blue and red boxes, respectively. D, dorsal; L, lateral; M, medial; V, ventral. Scale: 10 μm.
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Figure 3: Temperature-evoked neuronal activity in antennal lobe projection neurons. (A,B) Upon stimulation with 15°C cold air (indicated as blue bars), two glomeruli of this optical section change their neuronal activity. Based on their response properties, the glomeruli classify as warm- and cold-sensitive, respectively (red and blue/white ROI). The repeated stimulation (n = 4) induced changes in ΔF/F of up to 20% in the cold-sensitive glomerulus and about 10% in the warm-sensitive glomerulus (raw data traces shown). (C) The average fluorescence change in antennal lobe projection neurons in response to the four individual stimulation trials (30°C, indicated as red bars) is shown as false color image sequence. Based on the color code used, cold-sensitive glomeruli appear in blue whereas warm-sensitivity is indicated by red pixels. (D) The average fluorescence change (mean of four stimulation trials) of individual glomeruli is shown. Cold- and warm-sensitivity is indicated by blue and red boxes, respectively. D, dorsal; L, lateral; M, medial; V, ventral. Scale: 10 μm.

Mentions: Using two-photon microscopy we screened the whole antennal lobe and investigated where thermal information is represented. In 11 specimens we successfully recorded changes in neuronal activity within antennal lobe glomeruli in response to temperature stimuli. By using repeated stimulation with temperature steps, both, warm- and cold-sensitive glomeruli, could be identified. In the example of Figures 3A,B the fluorescent changes in response to repeated cold stimulation (15°C, n = 4) are visualized as raw data traces (depth = 49 μm). Two glomeruli respond to cold stimulation (step change to 15°C; ambient temperature = 24°C) with different response properties. The medial glomerulus (blue/white ROI and blue trace in Figures 3A,B) responds with a drop in fluorescence upon stimulation (cold-sensitive glomerulus). In contrast, a central glomerulus (red ROI and red trace in Figures 3A,B) seemed to be inhibited during the cold-stimuli and responded with increased activity after termination of the cold-stimuli (warm-sensitive glomerulus). There is a stronger Ca2+ signal in response to the temperature change in the cold-sensitive glomerulus (ΔF/F ≈ 20%) than in the warm-sensitive glomerulus (ΔF/F ≈ 10%). In Figure 3C the average response to four warm stimuli (30°C) is shown as false color image sequence (depth = 100 μm). Cold-sensitive glomeruli appear in blue, whereas red indicates warm-sensitive glomeruli (Figure 3C). Based on our criteria used to analyze the data, three warm-sensitive glomeruli and six cold-sensitive glomeruli can be detected within this example. The response kinetics of the individual glomeruli vary to some extent. For example, they exhibit different response latencies to the stimulus application (Figure 3D). The changes in relative fluorescence seem sometimes to be rapid, step-like (e.g., ROI 33, 34 or ROI 39), and sometimes the maximum change is reached considerably more slowly, e.g., in ROI 14.


Representation of thermal information in the antennal lobe of leaf-cutting ants.

Ruchty M, Helmchen F, Wehner R, Kleineidam CJ - Front Behav Neurosci (2010)

Temperature-evoked neuronal activity in antennal lobe projection neurons. (A,B) Upon stimulation with 15°C cold air (indicated as blue bars), two glomeruli of this optical section change their neuronal activity. Based on their response properties, the glomeruli classify as warm- and cold-sensitive, respectively (red and blue/white ROI). The repeated stimulation (n = 4) induced changes in ΔF/F of up to 20% in the cold-sensitive glomerulus and about 10% in the warm-sensitive glomerulus (raw data traces shown). (C) The average fluorescence change in antennal lobe projection neurons in response to the four individual stimulation trials (30°C, indicated as red bars) is shown as false color image sequence. Based on the color code used, cold-sensitive glomeruli appear in blue whereas warm-sensitivity is indicated by red pixels. (D) The average fluorescence change (mean of four stimulation trials) of individual glomeruli is shown. Cold- and warm-sensitivity is indicated by blue and red boxes, respectively. D, dorsal; L, lateral; M, medial; V, ventral. Scale: 10 μm.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2991144&req=5

Figure 3: Temperature-evoked neuronal activity in antennal lobe projection neurons. (A,B) Upon stimulation with 15°C cold air (indicated as blue bars), two glomeruli of this optical section change their neuronal activity. Based on their response properties, the glomeruli classify as warm- and cold-sensitive, respectively (red and blue/white ROI). The repeated stimulation (n = 4) induced changes in ΔF/F of up to 20% in the cold-sensitive glomerulus and about 10% in the warm-sensitive glomerulus (raw data traces shown). (C) The average fluorescence change in antennal lobe projection neurons in response to the four individual stimulation trials (30°C, indicated as red bars) is shown as false color image sequence. Based on the color code used, cold-sensitive glomeruli appear in blue whereas warm-sensitivity is indicated by red pixels. (D) The average fluorescence change (mean of four stimulation trials) of individual glomeruli is shown. Cold- and warm-sensitivity is indicated by blue and red boxes, respectively. D, dorsal; L, lateral; M, medial; V, ventral. Scale: 10 μm.
Mentions: Using two-photon microscopy we screened the whole antennal lobe and investigated where thermal information is represented. In 11 specimens we successfully recorded changes in neuronal activity within antennal lobe glomeruli in response to temperature stimuli. By using repeated stimulation with temperature steps, both, warm- and cold-sensitive glomeruli, could be identified. In the example of Figures 3A,B the fluorescent changes in response to repeated cold stimulation (15°C, n = 4) are visualized as raw data traces (depth = 49 μm). Two glomeruli respond to cold stimulation (step change to 15°C; ambient temperature = 24°C) with different response properties. The medial glomerulus (blue/white ROI and blue trace in Figures 3A,B) responds with a drop in fluorescence upon stimulation (cold-sensitive glomerulus). In contrast, a central glomerulus (red ROI and red trace in Figures 3A,B) seemed to be inhibited during the cold-stimuli and responded with increased activity after termination of the cold-stimuli (warm-sensitive glomerulus). There is a stronger Ca2+ signal in response to the temperature change in the cold-sensitive glomerulus (ΔF/F ≈ 20%) than in the warm-sensitive glomerulus (ΔF/F ≈ 10%). In Figure 3C the average response to four warm stimuli (30°C) is shown as false color image sequence (depth = 100 μm). Cold-sensitive glomeruli appear in blue, whereas red indicates warm-sensitive glomeruli (Figure 3C). Based on our criteria used to analyze the data, three warm-sensitive glomeruli and six cold-sensitive glomeruli can be detected within this example. The response kinetics of the individual glomeruli vary to some extent. For example, they exhibit different response latencies to the stimulus application (Figure 3D). The changes in relative fluorescence seem sometimes to be rapid, step-like (e.g., ROI 33, 34 or ROI 39), and sometimes the maximum change is reached considerably more slowly, e.g., in ROI 14.

Bottom Line: Here we selectively stained the three neurons found in single Sc and tracked their axons into the brain of Atta vollenweideri workers.Based on the general representation of thermal information in the antennal lobe and functional data on the Sc-glomeruli we conclude that temperature stimuli received by Sc are processed in the medial of the three target glomeruli.The present study reveals an important role of the antennal lobe in temperature processing and links a specific thermosensitive neuron to its central target glomerulus.

View Article: PubMed Central - PubMed

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

ABSTRACT
Insects are equipped with various types of antennal sensilla, which house thermosensitive neurons adapted to receive different parameters of the thermal environment for a variety of temperature-guided behaviors. In the leaf-cutting ant Atta vollenweideri, the physiology and the morphology of the thermosensitive sensillum coeloconicum (Sc) has been thoroughly investigated. However, the central projections of its receptor neurons are unknown. Here we selectively stained the three neurons found in single Sc and tracked their axons into the brain of Atta vollenweideri workers. Each of the three axons terminates in a single glomerulus of the antennal lobe (Sc-glomeruli). Two of the innervated glomeruli are adjacent to each other and are located laterally, while the third one is clearly separated and located medially in the antennal lobe. Using two-photon Ca(2+) imaging of antennal lobe projection neurons, we studied where in the antennal lobe thermal information is represented. In the 11 investigated antennal lobes, we found up to 10 different glomeruli in a single specimen responding to temperature stimulation. Both, warm- and cold-sensitive glomeruli could be identified. The thermosensitive glomeruli were mainly located in the medial part of the antennal lobe. Based on the general representation of thermal information in the antennal lobe and functional data on the Sc-glomeruli we conclude that temperature stimuli received by Sc are processed in the medial of the three target glomeruli. The present study reveals an important role of the antennal lobe in temperature processing and links a specific thermosensitive neuron to its central target glomerulus.

No MeSH data available.