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Development of laminar organization in the mushroom bodies of the cockroach: Kenyon cell proliferation, outgrowth, and maturation

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Abstract

The mushroom bodies of the insect brain are lobed integration centers made up of tens of thousands of parallel-projecting axons of intrinsic (Kenyon) cells. Most of the axons in the medial and vertical lobes of adult cockroach mushroom bodies derive from class I Kenyon cells and are organized into regular, alternating pairs (doublets) of pale and dark laminae. Organization of Kenyon cell axons into the adult pattern of laminae occurs gradually over the course of nymphal development. Newly hatched nymphs possess tiny mushroom bodies with lobes containing a posterior lamina of ingrowing axons, followed by a single doublet, which is flanked anteriorly by a γ layer composed of class II Kenyon cells. Golgi impregnations show that throughout nymphal development, regardless of the number of doublets present, the most posterior lamina serves as the “ingrowth lamina” for axons of newborn Kenyon cells. Axons of the ingrowth lamina are taurine- and synaptotagmin-immunonegative. They produce fine growth cone tipped filaments and long perpendicularly oriented collaterals along their length. The maturation of these Kenyon cells and the formation of a new lamina are marked by the loss of filaments and collaterals, as well as the onset of taurine and synaptotagmin expression. Class I Kenyon cells thus show plasticity in both morphology and transmitter expression during development. In a hemimetabolous insect such as the cockroach, juvenile stages are morphologically and behaviorally similar to the adult. The mushroom bodies of these insects must be functional from hatching onward, while thousands of new neurons are added to the existing structure. The observed developmental plasticity may serve as a mechanism by which extensive postembryonic development of the mushroom bodies can occur without disrupting function. This contrasts with the more evolutionarily derived holometabolous insects, such as the honey bee and the fruit fly, in which nervous system development is accomplished in a behaviorally simple larval stage and a quiescent pupal stage. J. Comp. Neurol. 430:331–351, 2001. © 2001 Wiley-Liss, Inc.

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