High-frequency oscillations are prominent in the extended amygdala

Abstract

Previously, it was reported that various cortical and subcortical structures display high-frequency local field potential (LFP) oscillations in the 110- to 160-Hz range (HFOs), distinct from sharp-wave ripples. In the present study, we characterize HFOs in the extended amygdala. Rats were implanted with tetrode bundles in the bed nucleus of the stria terminalis (BNST), central amygdala (CeA), as well as adjacent regions (pallidum, caudate-putamen, and lateral septum). At all recorded sites, HFO power showed a systematic dependence on behavioral state: highest during quiet wakefulness, intermediate during paradoxical sleep, and lowest during active waking or slow-wave sleep. CO2 asphyxiation as well as anesthesia with isoflurane or urethane abolished HFOs. HFOs stood out relative to all other fast-frequency LFP components because they were highly coherent between distant sites of the extended amygdala, ipsi- and contralaterally. HFOs affected neuronal firing in two ways: firing rate could vary as a function of HFO power (rate modulation) or HFOs could entrain firing on a cycle-to-cycle basis (phase modulation). The incidence of phase-modulated neurons was about twice higher in BNST and CeA (20–40%) than in adjacent regions (≤8%). Among BNST and CeA neurons, many more were phase-modulated than rate-modulated, although about half of the latter were also phase-modulated. Overall, these results indicate that HFOs entrain the activity of a high proportion of neurons in the extended amygdala. A major challenge for future studies will be to identify the mechanisms supporting the high coherence of HFOs within and across hemispheres.