An important contribution to neural circuit oscillatory dynamics is the ongoing activation and inactivation of hyperpolarization-activated currents (Ih). Network synchrony dynamics play an important role in the initial processing of odor signals by the main and accessory olfactory bulb (MOB and AOB, respectively). In the mouse olfactory bulb, we show that Ih is present in granule cells (GCs), the most prominent inhibitory neuron in the olfactory bulb, and that Ih underlies subthreshold resonance in GCs. In accord with the properties of Ih, the currents exhibited sensitivity to changes in extracellular K+ concentration and ZD7288, a blocker of Ih. ZD7288 also caused GCs to hyperpolarize and increase their input resistance, suggesting that Ih is active at rest in GCs. Inclusion of cAMP in the intracellular solution shifted the activation of Ih to less negative potentials in the MOB, but not the AOB, suggesting that channels with different subunit composition mediate Ih in these regions. Furthermore, we show that mature GCs exhibit Ih-dependent subthreshold resonance in the theta frequency range (4-12 Hz). Another inhibitory subtype in the MOB, the periglomerular cells, exhibited Ih-dependent subthreshold resonance in the delta range (1-4 Hz), while principal neurons, the mitral cells, do not exhibit Ih-dependent subthreshold resonance. Importantly, Ih size, as well as the strength and frequency of resonance in GCs exhibited a postnatal developmental progression, suggesting that this development of Ih in GCs may differentially contribute to their integration of sensory input and contribution to oscillatory circuit dynamics.
Significance Statement: The hyperpolarization-activated current (Ih) plays an essential role in neuronal function and network oscillatory dynamics throughout the nervous system. Network synchrony dynamics are an important component of the initial processing of odor signals in the olfactory bulb (OB). Here we provide new evidence that granule cells (GCs), the major inhibitory subtype in the OB, exhibit an Ih-dependent subthreshold resonance in the theta frequency range (4-12 Hz). Notably, Ih size and the strength of subthreshold resonance in GCs exhibited a postnatal developmental progression, suggesting that this development of Ih in GCs may differentially contribute to their integration of sensory input and contribution to oscillatory circuit dynamics.
The authors report no conflict of interest.
NIH-NIDCD DCR01-DC-009817 and NIH-NIA AG049937A grants to (R.C.A). NSF-GRFP DGE 1322106 to (R.H).