Scuttling in sewers and crawling through cracked pavements, cockroaches must search for food in the dark by using their antennae to sniff out decaying plant and animal scraps. Being able to distinguish between very similar smells would help them decide what's edible and what's not. A great deal is known about which chemicals the receptor cells in cockroach antennae respond to, but neurophysiology cannot tell us what odours cockroaches can really distinguish in the wild. Sakura and colleagues tackle this problem by training cockroaches to indicate when they can tell alcoholic fragrances apart. Their findings allow the team to draw links for the first time between what happens in nerve cells and what happens in dirty kitchens after dark.
Sakura and team taught cockroaches to choose filter paper soaked in peppermint essence over paper soaked in vanilla by providing a sugary reward for a correct answer and a salty punishment for an error. Testing revealed that cockroaches learn to make preferences very quickly and can retain them for a long time. They also found that these preferences can easily be overridden by training them with different flavours. The team then repeated the training, but substituted three different types of alcohols instead of the peppermint and vanilla. The team knew that if the cockroaches could learn to recognise the alcohol type associated with the reward, it meant that they could distinguish between similar alcohols; and this is exactly what happened. The cockroaches could discriminate a whole range of alcohols, which sometimes differed only by a single carbon atom or by subtleties in the chemical structure. The cockroaches could also tell apart different concentrations of alcohols and mixtures of them – with a few exceptions. Comparisons show that cockroaches' ability to discriminate alcohols is as good as bees and humans!
Some of the alcohols used in the study are plant components, such as green leaf odour, lemons or floral fragrances. In the wild, cockroaches would rarely approach these smells, since they do not usually eat living plants. But they can be taught to favour these plant extracts over other alcohols. This reflects the enormous flexibility in their diet, which makes them such successful scavengers.
Sakura and colleagues compared their behavioural findings with the information available about cockroach antennae. Antennae contain many receptor cells, which taste the surrounding air. These receptors fall into eight categories, only one of which responds to alcohol. This group of alcohol-sensitive cells can be further divided into subclasses, each responding differently to a range of alcohol types. The team noticed that in some cases, the alcohols discriminated during training fell into different subclasses of alcohol-sensitive cells. In these instances, the behavioural findings were in agreement with the neurophysiology. In other cases, however,the cockroaches could discriminate alcohols that fell into the same receptor subclass. This meant that these alcohols are told apart, not in the antennae but by further processing in the brain. Such relationships between neurophysiology and behaviour advance understanding by tugging at the entangled mesh of mechanisms underlying learning and processing in insect nervous systems.