A role for nitric oxide in sensory-induced neurogenesis in an adult insect brain.
In the adult cricket, neurogenesis occurs in the mushroom bodies, the main integrative structures of the insect brain. Mushroom body neuroblast proliferation is modulated in response to environmental stimuli. However, the mechanisms underlying these effects remain unspecified. In the present study, we demonstrate that electrical stimulation of the antennal nerve mimics the effects of olfactory activation and increases mushroom body neurogenesis. The putative role of nitric oxide (NO) in this activity-regulated neurogenesis was then explored. In vivo and in vitro experiments demonstrate that NO synthase inhibition decreases, and NO donor application stimulates neuroblast proliferation. NADPH-d activity, anti-L-citrulline immunoreactivity, as well as in situ hybridization with a probe specific for Acheta NO synthase were used to localize NO-producing cells. Combining these three approaches we clearly establish that mushroom body interneurons synthesize NO. Furthermore, we demonstrate that experimental interventions known to upregulate neuroblast proliferation modulate NO production: rearing crickets in an enriched sensory environment induces an upregulation of Acheta NO synthase mRNA, and unilateral electrical stimulation of the antennal nerve results in increased L-citrulline immunoreactivity in the corresponding mushroom body. The present study demonstrates that neural activity modulates progenitor cell proliferation and regulates NO production in brain structures where neurogenesis occurs in the adult insect. Our results also demonstrate the stimulatory effect of NO on mushroom body neuroblast proliferation. Altogether, these data strongly suggest a key role for NO in environmentally induced neurogenesis.
Cayre
M
M
Laboratoire NMDA, UMR 6156, parc scientifique de Luminy, case 907, 13288 Marseille Cedex, 9, France. cayre@ibdm.University-mrs.fr
Malaterre
J
J
Scotto-Lomassese
S
S
Holstein
G R
GR
Martinelli
G P
GP
Forni
C
C
Nicolas
S
S
Aouane
A
A
Strambi
C
C
Strambi
A
A
D000344:Afferent Pathways / Q000502:physiology; D000818:Animals; D001921:Brain / Q000378:metabolism; D002454:Cell Differentiation / Q000187:drug effects / Q000502:physiology*; D049109:Cell Proliferation; D002956:Citrulline / Q000378:metabolism; D004780:Environment, Controlled; D004791:Enzyme Inhibitors / Q000494:pharmacology; D005260:Female; D006135:Gryllidae / Q000166:cytology / Q000378:metabolism*; D007395:Interneurons / Q000378:metabolism; D008969:Molecular Sequence Data; D024521:Mushroom Bodies / Q000166:cytology / Q000378:metabolism*; D009252:NADPH Dehydrogenase / Q000378:metabolism; D026602:Nitrergic Neurons / Q000166:cytology / Q000378:metabolism*; D009569:Nitric Oxide / Q000378:metabolism*; D020030:Nitric Oxide Donors / Q000494:pharmacology; D019001:Nitric Oxide Synthase / Q000037:antagonists & inhibitors / Q000235:genetics / Q000378:metabolism; D012333:RNA, Messenger / Q000378:metabolism; D017386:Sequence Homology, Amino Acid; D012903:Smell / Q000502:physiology; D013234:Stem Cells / Q000187:drug effects / Q000378:metabolism; D015854:Up-Regulation / Q000502:physiology
D004791:Enzyme Inhibitors; D020030:Nitric Oxide Donors; D012333:RNA, Messenger; D002956:Citrulline; D009569:Nitric Oxide; D019001:Nitric Oxide Synthase; D009252:NADPH Dehydrogenase