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Tripartite Mushroom Body Architecture
Revealed by Antigenic Markers
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Jill R. Crittenden1*, Efthimios M.C. Skoulakis1,
Kyung-An Han1, Daniel Kalderon3
and Ronald L. Davis1,2
1Department of Cell Biology
2Department of Psychiatry and Behavioral Sciences, Baylor College of Medicine, Houston, Texas 77030 USA
3Department of Biology, Columbia University, New York, New York 10027 USA
Originially published in: Crittenden et al., 1998, Learning and Memory, 5: 38-51
*Correspondence: Jill Crittenden jr691194@bcm.tmc.edu
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Summary
We have explored the organization of the axonal lobes in Drosphila mushroom
bodies by using a panel of immunohistochemical markers. These markers consist of
antibodies to eight proteins expressed preferentially in the mushroom bodies:
DAMB, DCO, DRK, FASIL, LEO, OAMB, PKA RII, and RUT. Previous to this work, four
axonal lobes, two projecting dorsally (alpha and alpha') and two medially (beta
and gamma), had been described in Drosphila mushroom bodies. However, our
analysis of immunohistochemically stained frontal and sagittal sections of the
brain revealed three medially projecting lobes. The newly distinguished lobe,
which we term beta', lies along the dorsal surface of beta, just posterior to
gamma. In addition to resolving a fifth lobe, our studies revealed that there are
specific lobe sets defined by equivalent marker expression levels. These sets are
(1) the alpha and beta lobes, (2) the alpha' and beta' lobes, and (3) the gamma
lobe and heel (a lateral projection formed by a hairpin turn of some of the
peduncle fibers). All of the markers we have examined are consistent with these
three sets. Previous Golgi studies demonstrate that each mushroom body cell
projects one axon that branches into a dorsal lobe and a medial lobe, or one
unbranched axon that projects medially. Taken together with the lobe sets listed
above, we propose that there are three major projection configurations of
mushroom body cell axons: (1) one branch inthe alpha and one in the beta lobe,
(2) one branch inthe alpha' and one in the beta' lobe, and (3) one unbranched
axon projecting to the heel and the gamma lobe. The fact that these neuron types
exhibit differential expression levels of a number of mushroom body genes suggest
that they may have corresponding functional differences. These functions may be
conserved in the larvae, as several of these genes were expressed in larval and
embryonic mushroom bodies as well. The basic mushroom body structure, including
the denritic calyx, peduncle, and lobes, was already visible by the late stages
of embryogenesis. With new insights into mushroom body organization, and the
characterization of markers for developing mushroom bodies, we are beginning to
understand how these structures form and function.
Figure 1 - Cartoon of the Mushroom Body Lobes Depicted from an Anterior View-point
Figure 2 - Cartoon of a Cross-section Through the Peduncle at the Level of the Fan-shaped Body
Figure 3 - Frontal Sections Through the Adult Brain Stained for Mushroom Body Markers
Figure 4 - Sagittal Sections Through the Adult Brain
Figure 5 - Frontal Sections Through the Brain of a Wandering Third Instar
Larva Stained with anti-FASII
Figure 6 - Sagittal Sections Through Single Brain Hemispheres of Wandering Third Instar Larvae
Figure 7 - Frontal Section of the Mushroom Body from a Wandering Third Instar Larva Stained for LEO
Figure 8 - Sections of Embryonic Central Nervous System Stained to Detect anti-FASII
Figure 9 - Sagittal Sections of Embryonic Brains Stained for Markers
Figure 10 - Frontal Paraffin Sections Through an Adult Brain Challenged with anti-HRP
Atlas