Sprouting interneurons in mushroom bodies of adult cricket brains

Abstract

In crickets, neurogenesis persists throughout adulthood for certain local brain interneurons, the Kenyon cells in the mushroom bodies, which represent a prominent compartment for sensory integration, learning, and memory. Several classes of these neurons originate from a perikaryal layer, which includes a cluster of neuroblasts, surrounded by somata that provide the mushroom body's columnar neuropil. We describe the form, distribution, and cytology of Kenyon cell groups in the process of generation and growth in comparison to developed parts of the mushroom bodies in adult crickets of the species Gryllus bimaculatus. A subset of growing Kenyon cells with sprouting processes has been distinguished from adjacent Kenyon cells by its prominent f-actin labelling. Growth cone-like elements are detected in the perikaryal layer and in their associated sprouting fiber bundles. Sprouting fibers distant from the perikarya contain ribosomes and rough endoplasmic reticulum not found in the dendritic processes of the calyx. A core of sprouting Kenyon cell processes is devoid of synapses and is not invaded by extrinsic neuronal elements. Measurements of fiber cross-sections and counts of synapses and organelles suggest a continuous gradient of growth and maturation leading from the core of added new processes out to the periphery of mature Kenyon cell fiber groups. Our results are discussed in the context of Kenyon cell classification, growth dynamics, axonal fiber maturation, and function.

Cytoarchitecture and ultrastructure of neural stem cell niches and neurogenic complexes maintaining adult neurogenesis in the olfactory midbrain of spiny lobsters, Panulirus argus

“…Their cell membranes are not separated by interspersed processes of cell body glia. A similar lack of glial ensheathment was reported for neuronal progenitor cells located centrally in the cluster of mature Kenyon cell somata in the mushroom bodies of adult crickets (Mashaly et al, 2008). Type C cells in the periphery of the proliferation zone are at least partially and in many cases completely surrounded by a thin layer of electron-dense tissue consisting of processes of cell body glia (Fig.…”

“…In mammalian brains, adult neurogenesis predominantly produces new local interneurons of the olfactory bulb (periglomerular cells and granule cells) and the hippocampal dentate gyrus (granule cells; Kriegstein and Alvarez-Buylla, 2009). In brains of some insect species, adult neurogenesis generates new local interneurons (Kenyon cells) of the mushroom bodies (Cayre et al, 1994(Cayre et al, , 1996Gu et al, 1999;Dufour and Gadenne, 2006;Mashaly et al, 2008;Zhao et al, 2008;Ghosal et al, 2009). The mushroom bodies are large protocerebral neuropils that in most insects receive projections neurons (PNs) from the antennal lobes and thus represent the second stage of the central olfactory pathway; moreover, they are centers for multisensory integration (Strausfeld et al, 2009).…”

“…Based on the finding that, in Drosophila, glial cells associated with larval NBs secrete glycoproteins regulating NB proliferation (Ebens et al, 1993), it has been suggested that these glial cells form a stem cell niche for late embryonic and larval NBs (Maurange and Gould, 2005). However, glial cells are not associated with the neuronal progenitor cells in the Kenyon cell layer of adult crickets in a pattern suggesting that they form a stem cell niche (Mashaly et al, 2008). We hypothesize that the presence or lack of a stem cell niche associated with the aNBs reflects the generally enormous difference in the duration of adult neurogenesis between decapod crustaceans and insects.…”

“…These NBs produce intermediate progenitor cells that act as self-renewing transit-amplifying cells that give rise to GMCs (Bello et al, 2008;Boone and Doe, 2008;Bowman et al, 2008;Izergina et al, 2009;Boyan et al, 2010). Adult neurogenesis in the mushroom bodies of insects is based on continued mitotic activity of a few NBs surviving after larval development (Cayre et al, 1994(Cayre et al, , 1996(Cayre et al, , 2002Gu et al, 1999;Dufour and Gadenne, 2006;Mashaly et al, 2008;Zhao et al, 2008;Ghosal et al, 2009). These adult NBs appear to generate progeny as the canonical embryonic and larval NBs (Dufour and Gadenne, 2006;Zhao et al, 2008); however, the exact cell lineage that they produce has not yet been established.…”

Agonistic behavior enhances adult neurogenesis in maleAcheta domesticuscrickets

“…However, both studies were performed in female crickets and no quantitative data were provided. In support of our conclusion, Mashaly and colleagues observed some pyknotic Kenyon cells and degenerating cellular components in electron micrographs of the Kenyon cell perikaryial layer and MB calyx regions of adult Gryllus bimaculatus crickets (Mashaly et al, 2008). Our results are similar to findings in mammals, where many new neurons die within a few days of birth (Cameron et al, 1993;Dayer et al, 2003).…”