The seat of insect learning?

Natural History, Sept, 1997 by Fred C. Dyer

Widely perceived as hard-wired slaves of instinct, many insects are capable of learning about their environment as rapidly and flexibly as some vertebrates. That then. do so with much smaller brains presents an opportunity, to neurobiologists interested in explaining the cellular basis of learning and complex behavior.

Small as it is, the insect brain is a highly complex assemblage of regions serving distinct functions. Most likely, several of these regions are involved in learning, each with its own role to play. Various lines of evidence have focused attention on the mushroom bodies: cup-shaped structures perched atop the insect's brain that receive signals from multiple sensory organs and in turn send signals to centers of the brain that control behavior.

Several experimental studies of fruit flies have suggested that mushroom bodies play an important role in learning what scientists call meaningful odors. In the laboratory, fruit flies can be taught to associate an odor with a particular stimulus -- usually a small electric shock. (When the flies have made the connection, they avoid the odor.) By administering a toxin to fruit flies during their larval stage, Steven De Belle and his colleagues at the University of Wurzburg, Germany, produced individuals without mushroom bodies. As adults, these flies performed poorly on the odor association tests, although they could still smell, were normal in all other respects, and did well on other sorts of learning tests. Complementing De Belle's findings, other researchers have found that mutations of the genes active in mushroom bodies impair the flies' ability to learn odors.

The mushroom bodies of cockroaches seem to be important to spatial learning. At the University of Arizona, Nick Strausfeld and his colleagues employ what they call the "Tennessee Willams paradigm" to test the ability of cockroaches to find a small, cool region on an otherwise lethally hot plate. Roaches can be trained to find the cool zone (which bears no identifying visual or chemical features) by referring to landmarks on the wall surrounding the hot plate. If, however, the researchers sever the connection between the mushroom bodies and the rest of the brain, the insect is lost; its ability to orient itself in space is destroyed. When the researchers color the cool zone to distinguish it from the rest of the plate, the roaches once again learn to orient to the cool zone, suggesting that removal of the mushroom bodies does not affect all learning circuits, just those involved in spatial learning.

Randolf Menzel, Martin Hammer, and their colleagues at the Free University of Berlin have taken still another approach to the neurobiology of learning. First the researchers taught honeybees to stick out their tongues in response to specific odors; the bees' reward was a sip of sugar water. With the help of fine electrodes inserted into the (unharmed) bee brain, the biologists identified a neuron responsible for notifying the insect when it has received a reward. The cell governing this crucial part of the learning process lies outside the mushroom bodies but makes connections with them (and with some other brain regions as well). Menzel and his colleagues found that they could train a bee just as well by skipping the sugar reward and either stimulating the neuron artificially with an electrode or injecting chemicals produced by the neuron directly into the bee's mushroom bodies.

Another intriguing line of inquiry comes from the work of Susan Farbach and Gene Robinson at the University of Illinois, who showed that the mushroom bodies, but not other brain structures, of worker honeybees enlarge as the bees undergo an age-related transition from working inside the nest to foraging outside. This neural growth is primarily under hormonal control and mainly occurs before a bee can fly. It is as though the mushroom bodies are preparing for the challenges of life outside the nest -- the need to locate sources of pollen and nectar, for example, and then to navigate back to the colony to "report" their discovery.

This finding is reminiscent of the correlation in several vertebrates between the size of the hippocampus and an animal's ability to remember where it has stored food or how to get around in its home range. We must of course be cautious about inferring causation from correlation, but such studies could pave the way for insights into the precise relationship between neural volume and behavioral sophistication.

As Nick Strausfeld points out, for any brain region implicated in learning, we need to ask whether the tissue is where the knowledge is stored or whether it plays an auxiliary role, encoding information prior to storage or decoding it later on. The research on mushroom bodies provides an exciting starting point for answering the question.

Are We There Yet?

Long John Silver, in Robert Louis Stevenson's Treasure Island, understood well that navigating an ocean voyage was no walk in the park. Attempting to dissuade his shipmates on the Hispaniola from killing Cap'n Smollett, he asked, "We can steer a course, but who's to set one?"