GABAergic phenotype of periglomerular cells in the rodent olfactory bulb

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Abstract
Periglomerular (PG) cells in the rodent olfactory bulb are heterogeneous anatomically and neurochemically. Here we investigated whether major classes of PG cells use γ‐aminobutyric acid (GABA) as a neurotransmitter. In addition to three known subtypes of PG cells expressing tyrosine hydroxylase (TH), calbindin D‐28k (CB), and calretinin (CR), we identified a novel PG cell population containing the GABAA receptor α5 subunit. Consistent with previous studies in the rat, we found that TH‐positive cells were also labeled with antibodies against GABA, whereas PG cells expressing CB or the α5 subunit were GABA‐negative. Using GAD67‐GFP knockin mice, we found that all PG cell subtypes expressed GAD67‐GFP. Calretinin labeled the major fraction (44%) of green fluorescent protein (GFP)‐positive cells, followed by TH (16%), CB (14%), and the α5 subunit (13%). There was no overlap between these neuronal populations, which accounted for ≈85% of GAD67‐GFP‐positive cells. We then demonstrated that PG cells labeled for TH, CB, or CR established dendrodendritic synapses expressing glutamic acid decarboxylase (GAD) or the vesicular inhibitory amino acid transporter, VGAT, irrespective of their immunoreactivity for GABA. In addition, CB‐, CR‐, and TH‐positive dendrites were apposed to GABAA receptor clusters containing the α1 or α3 subunits, which are found in mitral and tufted cells, and the α2 subunit, which is expressed by PG cells. Together, these findings indicate that all major subtypes of PG cells are GABAergic. In addition, they show that PG cells provide GABAergic input to the dendrites of principal neurons and are interconnected with other GABAergic interneurons, which most likely are other PG cells. J. Comp. Neurol. 502:990–1002, 2007.