Bitter flavours often mean that something is poisonous. But most plants are bitter tasting, so it is important for plant eaters to distinguish between bitter flavours that are toxic, and those that are not. Until now, its has been readily accepted that animals could not tell bitter tastes apart when individual bitter taste receptors sent messages to one part of the brain, or a single receptor was responsible for detecting both flavours. This study by John Glendinning and colleagues, Adrienne Davis and Sudha Ramaswamy, contests these assumptions.
The experiments use taste habituation as a model system to determine whether bitterness receptors on the mouthparts of Manduca sextacaterpillars can discriminate between five bitter tasting diets: salicin,caffeine, aristolochic acid, and two bitter tasting plant extracts. The caterpillars have four different classes of taste receptor. Each receptor houses many different taste cells, but only one cell in each receptor responds to bitterness. These cells respond with varying efficacies to any given zest.
Caterpillars were first fed with a training diet containing salicin. When they no longer rejected the food, they were considered to have habituated to the chemical. The larvae were then given an edible control-disc, followed by a distasteful bitter test-disc, and munching rates were monitored throughout. If the caterpillars rejected the new bitter flavour after habituation, then they must be able to distinguish between salicin and the new flavour.
After habituation, the caterpillars no longer showed their usual aversion to caffeine. But the caterpillars still rejected the bitter flavours of aristolochic acid, and the two plant extracts.
When they looked at the way that the caterpillars responded to aristolochic acid, they realised that the neural mechanism was different from that used to encode the taste of the plant extracts. Discriminating the plant extracts relied on one cell responding to the extract, and a different cell responding to salicin. The team knew that the caterpillars have two receptors that both respond to aristolochic acid. They wondered about the relative importance of these receptors, so they surgically removed one of them. The ability to discriminate the aristolochic acid from salicin remained, so a single taste cell somehow managed to distinguish between the two flavours! The team already knew that some taste cells could signal the presence of two different bitter flavours as opposed to one, by sending distinct nerve signals for each flavour they detect. When the team measured the remaining taste cell's response to aristolochic acid, they found that this was indeed the case. The cell's response to aristolochic acid was very different from the signals it sent when recognising salicin. It now seems that caterpillars are equally able to discriminate tastes whether they are using two different taste cells or two pathways within one cell.
The authors argue that bitter taste discrimination does not occur at the level of the receptor but at the central nervous system, which can respond selectively to different coding pathways. This has implications for future studies of taste processing, since it is still unknown whether the whole animal can sense different sub-tastes of bitterness. It seems we can learn still more from watching other animals eat their greens.
