What do the mushroom bodies do for the insect brain? an introduction.

Despite public claims to the contrary, our functional understanding of the brain is still rudimentary. Starting with F.J. Gall’s Phrenology of the late eighteenth century, one of the major drives has been to assign functions to discrete regions of the brain. In humans and other primates, lesions and noninvasive imaging techniques have provided fascinating insights into the underlying functional topology of the brain. However, lesions in humans relate brain areas comprising millions of neurons to clinical tests, interrogation, and life histories. Similarly, functional imaging usually ties regions of increased blood flow to mental activity conveyed by verbal or visual instructions. The striking specificity of behavioral and mental deficits after local brain damage is difficult to reconcile with the high degree of integration in the neural circuitry. The situation is as perplexing as that met in brain stimulation experiments in which gross perturbations of sophisticated neural activity patterns in the brain lead, often with long delays, to highly organized behaviors or mental experiences. These approaches, therefore, reveal structure–function relationships that are difficult to interpret in terms of network-based brain models. After all, assigning behavioral and mental functions to locations in the brain does not explain how the brain works. Brain regions need first to be interpreted as parts of a neural circuitry. One then can hope to obtain cues about the functioning of this system by interfering with a certain part of it and observing how the rest still controls behavior. From this perspective, the interventionist approach is a difficult and largely unexplored task. It is not even obvious (to me) that the brain sciences are ready for it. Given the motivational nature of behavior and the enormous diversity of neuronal interactions, can a basic general model of the brain be established at all at the network level? Is the conceptual and methodological inventory of the behavioral sciences sufficiently sophisticated? A basic model of how the brain controls behavior, would, in principle, allow the building of a robot with the same behavioral properties as the respective animal. Such explicit models have been designed for partial aspects of behavior such as color vision in the honeybee (Backhaus 1992), directional hearing in owls (Konishi 1993), or for walking in insects (Graham 1985). However, no such model exists for behavioral control in general. This is where smaller brains can contribute to our understanding of brain function. Animals with small brains, in particular insects, provide the opportunity to analyze the behavioral consequences of interventions (e.g., lesions) in much greater detail and have already, in cases like the ones cited above made it possible to match behavioral functions with the properties of the corresponding neural networks in the brain. The insect mushroom body (MB) may be a uniquely suitable structure for intervention. Its internal cytoarchitecture seems less complex than that of most other neuropil regions and its bizarre shape suggests a highly specialized function. Being closely associated with the chemosensory system, its role in olfaction can serve as a point of entry for the analysis, and a comparison of the MBs from species with different life styles and ecological constraints may provide useful cues for functional studies. Moreover, a variety of new approaches for studying the MBs have recently been developed. They take advantage of the rapid advances in areas such as developmental genetics, transgenics, cell and tissue culture, microchemistry, pharmacology, functional imaging, and patch clamping, to name a few. They all recognize the fact that without knowledge of the cellular properties of the tissues involved, their functional involvement cannot be properly assessed. Several of these new approaches are highlighted in this volume. When Dujardin (1850) first described the MBs in bees and ants, he compared them to the vertebrate cerebral cortex and considered them the seat of intelligence. It took nearly 150 years to establish beyond doubt that they are, indeed, involved in something related to intelligence: They are essential for short term memory in odor discrimination tasks. This is a promising start, but it may still be a long way until their function is understood at the circuit level. I appreciate the editorial decision of Learning & Memory to devote a special issue of the journal to this topic. The papers that have been contributed provide a good overview of the forefront of this field. They are not narrowly focused on learning and memory but address a variety of problems broadly related to MB function. Even if the MBs eventually turn out not to be the high-level integration center of the insect brain envisaged by Dujardin, understanding their contribution to a network model of brain function will be of great importance for learning and memory research.