Olfactory nerve axons terminate in olfactory bulb glomeruli forming excitatory synapses onto the dendrites of mitral/tufted (M/T) and juxtaglomerular cells, including external tufted (ET) and periglomerular (PG) cells. PG cells are heterogeneous in neurochemical expression and synaptic organization. We used a line of mice expressing green fluorescent protein under the control of the glutamic acid decarboxylase 65kDa gene (GAD65+) promoter to characterize a neurochemically identified subpopulation of PG cells by whole cell recording and subsequent morphological reconstruction. GAD65+ GABAergic PG cells form two functionally distinct populations: 33% are driven by monosynaptic olfactory nerve (ON) input (ON-driven PG cells), the remaining 67% receive their strongest drive from an ONETPG circuit with no or weak monosynaptic ON input (ET-driven PG cells). In response to ON stimulation ON-driven PG cells exhibit paired-pulse depression (PPD), which is partially reversed by GABA_B receptor antagonists. The ONETPG circuit exhibits phasic GABA_B-R-independent PPD. ON input to both circuits is under tonic GABA_B-R-dependent inhibition. We hypothesize that this tonic GABA_BR-dependent presynaptic inhibition of olfactory nerve terminals is due to autonomous bursting of ET cells in the ONETPG circuit, which drives tonic spontaneous GABA release from ET-driven PG cells. Both circuits likely produce tonic and phasic postsynaptic inhibition of other intraglomerular targets. Thus olfactory bulb glomeruli contain at least two functionally distinct GABAergic circuits that may play different roles in olfactory coding.