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First published online August 17, 2007
Journal of Experimental Biology 210, 3054-3067 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.004671
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The hungry caterpillar: an analysis of how carbohydrates stimulate feeding in Manduca sexta

John I. Glendinning*, Adrienne Jerud and Ariella T. Reinherz

Department of Biological Sciences, Barnard College, Columbia University, 3009 Broadway, New York, NY 10027, USA


Figure 1
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Fig. 1. (A) Cartoon of the head of an M. sexta caterpillar, as viewed from below. An enlargement of the maxilla (indicated with an arrow) is provided to clarify the location of the medial and lateral styloconic sensilla. This cartoon was adapted from Bernays and Chapman, fig. 3.4 (Bernays and Chapman, 1994Go). (B) Illustration of the tip-recording method, which was used to record excitatory responses of individual taste cells located within a taste sensillum. During a tip recording (Hodgson et al., 1955Go), the tip of a taste sensillum is inserted into the end of a glass recording/stimulating electrode, which is filled with a taste stimulus dissolved in an electrolyte solution (0.1 mol l–1 KCl in deionized water). The taste stimulus solution diffuses through a pore in the tip of the sensillum and activates transduction mechanism(s) on the distal end of a taste cell's dendritic process; the electrode detects the ensuing action potentials. For clarity, only one taste cell is indicated. Note that the taste cell's axonal process projects directly to the central nervous system without synapsing.

 

Figure 2
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Fig. 2. Total excitatory responses of the medial (A,C) and lateral (B,D) sensilla to stimulation with the control solution (i.e. 100 mmol l–1 KCl) or one of the carbohydrates: Polycose (100 mmol l–1), maltose (200 mmol l–1), trehalose (200 mmol l–1), fructose (200 mmol l–1), glucose (200 mmol l–1), sucrose (200 mmol l–1) and myo-inositol (1 mmol l–1). We presented each carbohydrate in the control solution. In panels A and B, we show the total number of spikes elicited in the medial and lateral styloconic sensilla, across the initial 1 s of stimulation. Within each panel, we compare means with a post-hoc test (Tukey's HSD test); different letters (a, b, c or a combination of each) above the bars indicate means that differ significantly from one another (P<=0.05). In panels C and D, we show concentration–response functions for a range of inositol, glucose and sucrose concentrations in both the medial and lateral styloconic sensilla. Each bar or symbol indicates mean ± s.e.m.; N=7–18 sensilla per tastant (each from a different caterpillar).

 

Figure 3
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Fig. 3. Demonstration that sucrose and inositol stimulate different taste cells in the lateral styloconic sensillum. In panel A, we show representative neural responses of a lateral styloconic sensillum to sucrose (200 mmol l–1), inositol (1 mmol l–1) and the binary mixture of both. We provide the initial 250 ms of response. Below each trace, we indicate dominant spikes with a filled circle, and non-dominant spikes with an arrowhead; see text for a description of how we distinguished these two classes of spikes. We dissolved the carbohydrates in a 100 mmol–1 KCl solution. In panels B and C, we show the number of dominant and non-dominant spikes elicited by each of the taste stimuli. Each bar indicates mean ± s.e.m.; N=13 sensilla (each from a different caterpillar). We compare the means within each panel with a post-hoc test (Tukey's HSD test); different letters (a or b) above the bars within a panel indicate means that differ significantly from one another (P<=0.05).

 

Figure 4
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Fig. 4. Demonstration that sucrose and glucose stimulate different taste cells in the lateral styloconic sensillum. In panel A, we show representative neural responses of a lateral styloconic sensillum to sucrose (200 mmol l–1), glucose (200 mmol l–1) and the binary mixture of both. We provide the initial 250 ms of response. Below each trace, we indicate dominant spikes with a filled circle, and non-dominant spikes with an arrowhead; see text for a description of how we distinguished these two classes of spikes. We dissolved the carbohydrates in a 100 mmol–1 KCl solution. In panels B and C, we show the number of dominant and non-dominant spikes elicited by each of the taste stimuli. Each bar indicates mean ± s.e.m.; N=12 sensilla (each from a different caterpillar). We compare the means within each panel with a post-hoc test (Tukey's HSD test); different letters (a or b) above the bars within a panel indicate means that differ significantly from one another (P<=0.05).

 

Figure 5
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Fig. 5. Demonstration that glucose and inositol stimulate the same taste cell in the lateral styloconic sensillum. In panel A, we show representative neural responses of a lateral styloconic sensillum to glucose (200 mmol l–1), inositol (1 mmol l–1) and the binary mixture of both. We provide the initial 250 ms of response. Below each trace, we indicate dominant spikes with a filled circle, and non-dominant spikes with an arrowhead; see text for a description of how we distinguished these two classes of spikes. We dissolved the carbohydrates in a 100 mmol–1 KCl solution. In panels B and C, we show the number of dominant and non-dominant spikes elicited by each of the taste stimuli. Each bar indicates mean ± s.e.m.; N=16 sensilla (each from a different caterpillar). We compare the means within each panel with a post-hoc test (Tukey's HSD test); different letters (a or b) above the bars within a panel indicate means that differ significantly from one another (P<=0.05).

 

Figure 6
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Fig. 6. Demonstration that glucose and inositol stimulate the same taste cell in the medial styloconic sensillum. In panel A, we show representative neural responses of a medial styloconic sensillum to glucose (200 mmol l–1), inositol (1 mmol l–1) and the binary mixture of both. We provide the initial 250 ms of response. Below each trace, we indicate dominant spikes with a filled circle, and non-dominant spikes with an arrowhead; see text for a description of how we distinguished these two classes of spikes. We dissolved the carbohydrates in a 100 mmol–1 KCl solution. In panels B and C, we show the number of dominant and non-dominant spikes elicited by each of the taste stimuli. Each bar indicates mean ± s.e.m.; N=12 sensilla (each from a different caterpillar). We compare the means within each panel with a post-hoc test (Tukey's HSD test); different letters (a or b) above the bars within a panel indicate means that differ significantly from one another (P<=0.05).

 

Figure 7
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Fig. 7. Instantaneous firing rates of the carbohydrate-sensitive taste cells. (A) Response of the carbohydrate-sensitive taste cell in the medial styloconic sensillum to 1 mmol l–1 inositol, 200 mmol l–1 glucose and the mixture of both. (B) Response of one carbohydrate-sensitive taste cell in the lateral styloconic sensillum to 1 mmol l–1 inositol, 200 mmol l–1 glucose and the mixture of both. (C) Response of the second carbohydrate-sensitive taste cell in the lateral styloconic sensillum to 200 mmol l–1 sucrose. We show mean ± s.e.m.; N=8–16 taste cells per panel (each from a different caterpillar).

 

Figure 8
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Fig. 8. Analysis of the initial biting responses of caterpillars to disks containing water (H2O), 200 mmol l–1 glucose, 200 mmol l–1 sucrose, 1 mmol l–1 inositol or binary mixtures of the carbohydrates. We show (A) latency to initiate biting, and number of bites taken across the initial (B) 10 s and (C) 120 s of the meal. Within each panel, we compared medians (±median absolute deviation) with Dunn's multiple comparison test; different letters (a, b, c or combinations of each) above the bars indicate medians that differ significantly from one another (P<=0.05). The absence of letters above the bars in panels B and C reflects a lack of significant difference among the medians (according to a Kruskal–Wallis test, P>0.05). N=19–25 caterpillars per taste stimulus.

 

Figure 9
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Fig. 9. Analysis of biting activity across the first meal on disks containing water (H2O), 200 mmol l–1 glucose, 200 mmol l–1 sucrose, 1 mmol l–1 inositol or binary mixtures of the carbohydrates. We show (A) bite size, (B) total number of bites emitted and (C) meal duration. Within each panel, we compare medians (±median absolute deviation) with Dunn's multiple comparison test; different letters (a, b, c or combinations of each) above the bars indicate medians that differ significantly from one another (P<=0.05). The absence of letters above the bars in panel A reflects a lack of significant difference among the medians (according to a Kruskal–Wallis test, P>0.05). N=19–25 caterpillars per taste stimulus.

 





© The Company of Biologists Ltd 2007