Transitory and activity-dependent expression of neurogranin in olfactory bulb tufted cells during mouse postnatal development

Abstract

Neurogranin (Ng) is a brain-specific postsynaptic calmodulin-binding protein involved in synaptic activity-dependent plasticity. In the adult olfactory bulb (OB), Ng is expressed by a large population of GABAergic interneurons in the granule cell layer. We show here that, during postnatal development, Ng is also expressed by OB neurons in the superficial external plexiform layer (sEPL) and glomerular layer (GL). These Ng-positive neurons display morphological and neurochemical features of superficial and external tufted cells. Ng expression in these cells is transient during OB development: few elements express Ng at postnatal day (P) 5, increasing in number and reaching a peak at P10, then progressively decreasing. At P30, Ng is rarely detectable in these neurons. Ng expression in developing tufted cells is also modulated at the cellular level: at earlier stages, Ng labeling is distributed throughout the cell body and dendritic arborization in the GL, but, at P20, when the glomerular circuits are fully matured, Ng becomes restricted to the soma and proximal portion of tufted cell apical dendrites. We show that olfactory deprivation at early postnatal stages induces a strong increase in Ng-positive tufted cells from P10 to P20, whereas no changes have been observed following olfactory deprivation in adult mice. These findings demonstrate that Ng expression in sEPL-GL is restricted to developmental stages and indicate its activity-dependent regulation in a time window critical for glomerular circuit development, suggesting a role for Ng in maturation and dendritic remodeling of tufted cells.