Morphology and sensory modality of mushroom body extrinsic neurons in the brain of the cockroach, Periplaneta americana.

Mushroom bodies are paired centers in insect brains that are thought to be crucial in olfactory learning and memory. Early neuroanatomical descriptions suggested that the mushroom bodies comprise rather simple arrangements of nerve cells. Intrinsic neurons within each mushroom body were believed to receive olfactory afferents and to supply long, branched axons to extrinsic neurons that lead from the mushroom body into the protocerebrum. More recent suggestions that the mushroom bodies integrate several sensory modalities find support from intracellular and extracellular recordings of extrinsic neurons in the brains of crickets, honey bees, and cockroaches. Here, we describe two major classes of extrinsic neurons, simple and complex cells, in the mushroom bodies of the cockroach Periplaneta americana. Each class is defined by its pattern of branching in the brain. Simple neurons correspond to extrinsic neurons described from other species that have one set of dendrites only within the mushroom bodies. Complex extrinsic neurons possess dendrite-like branches within and outside the mushroom bodies. This arrangement may account in part for their observed multimodality, as might newly identified afferent neurons that terminate in the mushroom body lobes among the dendrites of extrinsic neurons and that respond to multimodal stimuli. Organizational complexity within the mushroom bodies is suggested by the grouping of intrinsic cell axons into discrete laminae. These are intersected by the block-like arrangements of dendritic fields of extrinsic neurons in a manner reminiscent of Purkinje cell dendrites intersecting parallel fibers in the cerebellum. The present results demonstrate that the cockroach mushroom body processes multimodal sensory information and that its neural arrangements contribute to a precise architecture consisting of discrete longitudinal and transverse subdivisions.