Organization of olfactory and multimodal afferent neurons supplying the calyx and pedunculus of the cockroach mushroom bodies

The mushroom bodies of neopteran insects are considered to be higher olfact ory centers because their calyces receive abundant collaterals of projectio n neurons from the antennal lobes. However, intracellular recordings of mus hroom body efferent neurons demonstrate that they respond to multimodal sti muli, implying that the mushroom bodies receive a variety of sensory cues. The present account describes new features of the organization of afferent neurons supplying the calyces of the cockroach Periplaneta americana. Affer ent terminals segment the calyces into discrete zones, I, II, III, and IIIA , which receive afferents from 1) two discrete populations of sexually isom orphic olfactory glomeruli, 2) two types of male-specific olfactory glomeru li, 3) the optic lobes, and 4) multimodal interneurons that originate in pr otocerebral neuropils. In addition, intracellular recordings and dye fills show that at least four morphologically distinct GABAergic elements link ma ny regions of the protocerebrum to the calyces. A new type of touch-sensiti ve centrifugal neuron has been identified terminating in the pedunculus. Th e dendrites of this afferent reside in satellite neuropil, beneath the mush room body's medial lobe, which is supplied by collaterals from medial lobe efferent neurons and by terminals from the central complex. The role of thi s centrifugal cell in odorant sampling is considered. Golgi impregnation id entifies other afferents in proximal regions of the calyx (zone IIIA) that also originate from satellite neuropils, suggesting major reafference from the medial lobes channeled through this region. The relevance of multimodal supply to the calyx in odorant discrimination is discussed as are comparis ons between mushroom body organization in this phylogenetically basal neopt eran and other taxa. (C) 1999 Wiley-Liss, Inc.