Two species of gamma oscillations in the olfactory bulb: dependence on behavioral state and synaptic interactions

Gamma oscillations (40-100 Hz), originally seen in the olfactory bulb (OB), have long been a defining characteristic of sensory coding in the olfactory system. This study proposes that gamma oscillations are of two types, associated with different behavioral features and synaptic origins within the OB. Local field potentials were recorded from rat and mouse OBs during various behavioral periods (immobility, alert motionlessness, exploration and odor discrimination). High frequency gamma activity (65-100 Hz) is shown to be correlated with the sniff cycle, initiated at the peak of inhalation and is called type 1 gamma. It is prominent during exploratory behavior, but also present during resting and trained odor discrimination. Low frequency gamma activity (35-65 Hz), called type 2 gamma, is not strongly correlated with the sniff cycle, is inhibited by the sniff onset and is prominent during alert immobility. Rest and alert immobility are characterized by alternating type 1 and type 2 gamma rhythms, while exploratory sniffing and odor discrimination show a dramatic decrease in type 2 gamma with a broadband increase in the power of type 1 gamma. Periods of alert immobility prior to odor discrimination in trained animals show dominance of type 2 gamma, with episodes lasting up to 0.5 second. Data from mice with selective deletion of granule cell inhibition in the OB show a selective loss of type 2 gamma with type 1 gamma dramatically enhanced during exploratory behavior, suggesting that mutual inhibition between granule cells or centrifugal inhibitory input drives type 2 gamma, and that the excitatory-inhibitory connections between mitral and granule cells likely drive type 1 gamma. Gamma activity is not a single type of oscillation, and the largest amplitude gamma bursts are often those associated with an attentive cognitive state rather than odor sniffing.