Firing of interior colliculus auditory neurons is phase-locked to the hippocampus theta rhythm during paradoxical sleep and waking

The activity of 52 single auditory units in the central nucleus of the inferior colliculus (IC) was recorded along with cortical and hippocampal (CA1) electrograms and neck muscle electromyograms in behaving, head-restrained guinea pigs during paradoxical sleep (PS) and wakefulness. Sixteen (30%) of the IC auditory units showed positive correlation with the hippocampal theta (θ) rhythm: 8 (15%) were θ rhythmic with θ phase-locking (type 1), 8 (15%) showed only θ phase-locking with no rhythmicity (type 2), while 70% did not show any correlation to hippocampal θ rhythm (type 3). During wakefulness IC neurons (4 of 13) showed a higher synchrony with hippocampal θ when sound-stimulated at the unit's characteristic frequency. During PS all IC auditory neurons recorded presented some hippocampal θ correlation: 40% were rhythmic and phase-locked to the θ frequency and 60% were nonrhythmic maintaining the θ phase-locking. Shifts in the angle of phase-locking to the θ rhythm were observed during PS. It is suggested that the hippocampal θ rhythm may play the part of an internal clock, adding a temporal dimension to the processing of auditory sensory information.