Diversity of neural signals mediated by multiple, burst-firing mechanisms in rat olfactory tubercle neurons

Olfactory information is processed by a diverse group of interconnected forebrain regions. Most efforts to define the cellular mechanisms involved in processing olfactory information have been focused on understanding the function of the olfactory bulb, the primary second-order olfactory region, and its principal target, the piriform cortex. However, the olfactory bulb also projects to other targets, including the rarely studied olfactory tubercle, a ventral brain region recently implicated in regulating cocaine-related reward behavior. We used whole cell patch-clamp recordings from rat tubercle slices to define the intrinsic properties of neurons in the dense and multiform cell layers. We find three common firing modes of tubercle neurons: regular-spiking, intermittent-discharging, and bursting. Regular-spiking neurons are typically spiny-dense-cell-layer cells with pyramidal-shaped, dendritic arborizations. Intermittently discharging and bursting neurons comprise the majority of the deeper multiform layer and share a common morphology: multipolar, sparsely spiny cells. Rather than generating all-or-none stereotyped discharges, as observed in many brain areas, bursting cells in the tubercle generate depolarizing plateau potentials that trigger graded but time-limited discharges. We find two distinct subclasses of bursting cells that respond similarly to step stimuli but differ in the role transmembrane Ca currents play in their intrinsic behavior. Calcium currents amplify depolarizing inputs and enhance excitability in regenerative bursting cells, whereas the primary action of Ca in nonregenerative bursting tubercle neurons appears to be to decrease excitability by triggering Ca-activated K currents. Nonregenerative bursting cells exhibit a prolonged refractory period after even short discharges suggesting that they may function to detect transient events.