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First published online March 27, 2009
Journal of Experimental Biology 212, 1191-1201 (2009)
Published by The Company of Biologists 2009
doi: 10.1242/jeb.024166
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Quantitative analysis of sex-pheromone coding in the antennal lobe of the moth Agrotis ipsilon: a tool to study network plasticity

David Jarriault, Christophe Gadenne, Jean-Pierre Rospars and Sylvia Anton*

INRA, UMR1272, Physiologie de l'Insecte: Signalisation et Communication, Versailles, F-78000, France


Figure 1
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  		Fig. 1. Definition of the variables used to quantify the responses of macroglomerular complex (MGC) neurons. (A) Example of a recorded spike train during 500 ms before and 2 s after the stimulation. L0 is the latency of the first spike. (B) Plot of the instantaneous spike frequency F as a function of time after stimulus onset. F was calculated as 1/(ti–ti–1), where ti is the time of occurrence of the spike i. F1 is the maximum instantaneous spike frequency, and L1 is the latency of F1. (C) The firing frequency (F5) is the mean of the instantaneous spike frequency of five spikes surrounding and including the shortest interspike interval (ISI) (1/F1). (D) Definition of the quantities used to characterize the dose–response plots. A line was fitted to the rising part of the curve. The stimulus load at threshold (C0) was taken as the dose at which the fitted line reached the blank frequency. The stimulus loads at saturation were taken, respectively, as the first dose eliciting 95% of Fmax (Cs) or as the dose at which the fitted line reached the maximum firing frequency Fmax (Ces). The horizontal bars (Stim) in A–C indicate the stimulus duration (200 ms).

 

Figure 2
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  		Fig. 2. Typical response pattern of three pheromone-responding macroglomerular complex (MGC) neurons in three different A. ipsilon males. Neurons were stimulated with 0.1 ng of the main pheromone component, Z7-12:OAc. Note the different spontaneous activity rates but a common pattern of excitation followed by an inhibitory phase across different neurons. The grey bar indicates the time during which the stimulus was applied (200 ms). Horizontal scale bar, 500 ms; vertical scale bar, 8 mV.

 

Figure 3
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  		Fig. 3. Responses of three pheromone-responding macroglomerular complex (MGC) neurons to blank stimuli (hexane and clean air) in three different males. Whereas some neurons (neuron 4) did not respond to either hexane or clean air stimulation, others increased their spike frequency slightly (neuron 5) or showed a biphasic response pattern as for the pheromone responses (neuron 6). Similar responses to hexane and clean air indicate the mechanosensory origin of the blank responses. The grey bar indicates the time during which the stimulus was applied (200 ms). Horizontal scale bar, 500 ms; vertical scale bar, 4 mV.

 

Figure 4
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  		Fig. 4. Responses of a neuron inhibited by the pheromone. The neuron was stimulated with 1 ng of the blend. The grey bar indicates the stimulus duration (500 ms). Horizontal scale bar, 500 ms; vertical scale bar, 4 mV.

 

Figure 5
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  		Fig. 5. Response specificity of 93 macroglomerular complex (MGC) neurons for the three components of the pheromone blend. Neurons were stimulated with the three components of the blend separately at the same stimulus load (0.01 ng). Neurons responding specifically to Z7-12:OAc were encountered more often than neurons responding specifically to the two other compounds. Nineteen neurons (20%) responded to all three compounds, and a few neurons responded to different combinations of two of the three compounds.

 

Figure 6
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  		Fig. 6. Histograms of instantaneous spike frequencies, F (as defined in Fig. 1B), of a generalist macroglomerular complex (MGC) neuron responding to the three pheromone components (Z7-12:OAc, Z9-14:OAc, Z11-16:OAc) and their blend (4:1:4). All components were tested at the same stimulus load (0.01 ng). The latency of the maximum instantaneous spike frequency (L1, dotted lines) is shorter for Z9-14:OAc than for the other components. Spike frequencies are higher for Z9-14:OAc and Z11-16:OAc than for Z7-12:OAc and the blend. The grey bar indicates the time during which the compound was applied (200 ms).

 

Figure 7
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  		Fig. 7. Responses of macroglomerular complex (MGC) neurons to increasing stimulus loads of the main pheromone component (Z7-12:OAc). (A) Original recording. The grey bar indicates the stimulus duration (200 ms). Horizontal scale bar, 500 ms; vertical scale bar, 10 mV. (B) Raster plots for 29 MGC neurons. Each row represents the spikes emitted by a single neuron. The grey bar indicates the time during which the compound was applied (200 ms). The response pattern, an excitatory phase followed by an inhibitory phase, is conserved across the different doses.

 

Figure 8
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  		Fig. 8. Temporal response patterns of 29 macroglomerular complex (MGC) neurons to a 0.2 s stimulation with the solvent (blank) and doses of 0.01 ng, 0.1 ng, 1 ng and 10 ng of Z7-12:OAc. Each dot represents the instantaneous frequency F of a spike plotted against its time of occurrence. With increasing stimulus loads, neuron responses change from tonic to phasic–tonic. Latency L1 decreases with increasing stimulus loads. No changes are observed in the inhibitory phase (visible as the period with the lowest density of dots). The grey bar indicates the time during which the compound was applied (200 ms).

 

Figure 9
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  		Fig. 9. Dose–response relationships represented by box plots for 29 macroglomerular complex (MGC) neurons stimulated with Z7-12:OAc. (A) Firing frequency (F5). (B) Total number of spikes during the excitatory phase of the response. (C) Latency of the first spike of the response (L0). (D) Latency (L1) of the spike with highest instantaneous spike frequency (F1). (E) Duration of the excitatory phase. (F) Duration of the inhibitory phase. On each plot, the box represents the interquartile range (IQR) of the data, the horizontal line inside the box represents the median, and the black dot represents the mean. The whiskers show the range of the remaining sample. Outliers (+) are observations greater than 1.5xIQR.

 

Figure 10
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  		Fig. 10. Effect of the stimulus duration (0.01 ng, 0.1 ng and 1 ng of Z7-12:OAc) on the duration of (A) the excitatory phase (N=17 neurons) and (B) the inhibitory phase (N=15 neurons) of macroglomerular complex (MGC) neurons. Only the duration of the excitatory phase was found to be correlated with the stimulus duration.

 

Figure 11
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  		Fig. 11. Phasic–tonic pattern of macroglomerular complex (MGC) neuron responses. The figure shows the spike frequency (calculated from the number of spikes per 50-ms bin) averaged across responses of nine neurons to a 800-ms stimulation with the major component (same doses as in Fig. 10). Here, the division of the response into a phasic and a tonic part is clearly visible. Spike frequency was averaged in two bins of 200 ms (vertical grey bars), 200 ms and 500 ms after the stimulus onset. The frequency in the first bin was 107±5 spikes s–1 and in the second bin, 56±9 spikes s–1. The horizontal black bar indicates the time during which the stimulus was applied.

 

Figure 12
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  		Fig. 12. Morphology of a pheromone-responding projection neuron (PN) stained with NeurobiotinTM. (A) Maximum projection of 161 frontal optical sections through the antennal lobe, showing a stained PN arborising in the cumulus (Cu) of the macroglomerular complex (MGC). The cell body (arrowhead) is situated in the medial cell body cluster. Scale bar, 100 µm. (B) Three-dimensional reconstruction of the neuron in A in a frontal view, showing the axon projecting via the inner antennocerebral tract towards the calyces of the mushroom bodies. AL, antennal lobe; Ca, calyces of the mushroom bodies; Cu, cumulus; IACT, inner antennocerebral tract; LP, lateral protocerebrum; MB, mushroom bodies; MCB, medial cell body cluster. Scale bar, 200 µm.

 

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© The Company of Biologists Ltd 2009