Tripartite mushroom body architecture revealed by antigenic markers.

By J. Crittenden, E. Skoulakis, K. Han, D. Kalderon, Ronald L. Davis. 1998

We have explored the organization of the axonal lobes in Drosophila 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, FASII, 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 Drosophila 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 in the alpha and one in the beta lobe, (2) one branch in the 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 suggests 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.

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Citations in the corpus

Mushroom body output neurons encode valence and guide memory-based action selection in Drosophila (2014, background): “Connections between the projection neurons and the ∼2000 Kenyon cells (KCs), the neurons whose parallel axonal fibers form the MB lobes (Crittenden et al., 1998; Aso et al., 2009), are not stereotyped (Figure 1A) (Murthy et al., 2008; Caron et al., 2013); that is, individual flies show distinct…”
The neuronal architecture of the mushroom body provides a logic for associative learning (2014, background): “their parallel axons form the three MB lobes (Figure 1) (Crittenden et al., 1998).”
Two independent mushroom body output circuits retrieve the six discrete components of Drosophila aversive memory. (2015, background): “Based on their axonal morphology, KCs are classed into three different subtypes: axons from a/b and a0/b0 KCs branch at the anterior extremity of the peduncle to form the vertical (a and a0) and medial (b and b0) lobes, whereas axons from g neurons form a single medial g lobe (Crittenden et al., 199”
Three Dopamine Pathways Induce Aversive Odor Memories with Different Stability (2012, background): “represented by a small subset of Kenyon cells [10,11,12], which are major intrinsic neurons of the MB and categorized into the a/ b, a’/b’ and c neurons (Figure 1A) [13].”
Origins of Cell-Type-Specific Olfactory Processing in the Drosophila Mushroom Body Circuit. (2017, unknown): “Olfactory information conveyed to the MB is represented by the activity of 2,000 Kenyon cells (KCs), which can be classified into a/b, a0/b0, and g types from morphological and developmental characteristics (Aso et al., 2009; Crittenden et al., 1998; Lee et al., 1999).”
Transposition Driven Genomic Heterogeneity in the Drosophila Brain: A Dissertation (2012, unknown): “Depending on the morphology of their axonal projections, these 5000 neurons can be further subdivided into three subgroups: αβ, α’β’ and γ (Crittenden et al., 1998).”
Sequential use of mushroom body neuron subsets during drosophila odor memory processing. (2007, unknown): “The 2500 intrinsic neurons in each MB can be subdivided into at least three morphological subsets -αβ, α′β′ and γ- based on the bundling of their axonal projections in the region of the MBs called the lobes (Crittenden et al., 1998).”
Cell Type-Specific Transcriptome Analysis in the Drosophila Mushroom Body Reveals Memory-Related Changes in Gene Expression (2016, unknown): “The MB lobes can be subdivided broadly into 3 separate groups ( / , / , and ), based on where KCs target their axons (Crittenden et al., 1998; Lin et al., 2007).”
Forgetting is regulated through Rac activity in Drosophila. (2010, unknown): “The MB intrinsic neurons can be further classified into three major subtypes with axonal projections in different lobes: following their birth order, the g, a0b0, and ab neurons (Crittenden et al., 1998; Lee et al., 1999).”
Dopamine and Octopamine Differentiate between Aversive and Appetitive Olfactory Memories in Drosophila (2003, background): “The former alternative is supported by the observation that the MB lobes are equipped with DA and OA receptors that can couple to AC of the rut type via Gs protein (Han et al., 1996; Han et al., 1998, Crittenden et al., 1998; Kim et al., 2003).”
Synaptic organization of the mushroom body calyx in Drosophila melanogaster (2002, result): “It is also consistent with evidence from genetic and molecular biological studies demonstrating the existence of non-isomorphic subsets of grouped Kenyon cells in the mushroom bodies of flies (Yang et al., 1995; Ito et al., 1997; Crittenden et al., 1998).”
A pair of inhibitory neurons are required to sustain labile memory in the Drosophila mushroom body (2011, unknown): “Olfactory memories are believed to be stored in the output synapses of third-order olfactory system neurons in the mushroom body (MB) [5, 14–16], a symmetrical structure comprised of roughly 2500 neurons on each side of the brain that can be structurally and functionally dissected into ab, a0b0, and”
Different Kenyon Cell Populations Drive Learned Approach and Avoidance in Drosophila (2013, unknown): “Therefore, NP7175, NP6024, and c708a females were crossed to uas shits1 males.”