Oscillations in the basolateral amygdala: aversive stimulation is state dependent and resets the oscillatory phase

Slow oscillations (<1 Hz) in neural activity occur during sleep and quiet wakefulness in both animals and humans. Here we show that in urethan-anesthetized animals, neurons in the basolateral amygdala in vivo display a slow oscillation between resting membrane potential (down-state) and depolarized potentials (up-states) occurring at a frequency of approximately 0.3 Hz. This oscillation is insensitive to the holding potential and continues unabated under voltage clamp, indicating that up-states are synaptically driven. Somatosensory stimulation (footshock) delivered during the down-state evoked an all-or-none transition into an up-state. When delivered during down-states, footshocks triggered up-states and reset the phase of the neural oscillation, effectively synchronizing activity in the basolateral amygdala. This phase reset was reproduced by posterior thalamus stimulation, confirming that it was mediated by aversive sensory input. In contrast, a footshock delivered during the up-state was ineffective in stimulating BLA neurons. We conclude that oscillatory activity in the basolateral amygdala is driven by ensembles of cortical neurons. These ensembles gate the response of amygdala neurons to aversive stimulation in a state-dependent manner. Aversive stimulation is effective when the network is in the down-state but ineffective when the network is in an up-state.