Animal’s behavior relies on the processing of environmental cues and signals about bodily state, yet physiology of their coordination remains poorly understood. Hippocampal and cortical information is relayed to hypothalamus and midbrain in rodents and other mammals mainly via the lateral septal nucleus (LS). We used high-density single and dual-site electrophysiological registration of local field potentials and of neuronal discharge in behaving mice to study network synchronization in LS and its coordination with inputs from the medial prefrontal cortex (mPFC) and hippocampus. Local field potentials (LFP) and neuronal discharge in LS displayed intermittent episodes (40-120 ms duration) of synchronization at frequencies between 40 and 90 Hz. These fast oscillations were behavioral state-dependent, coordinated within LS and, strikingly, were coherent with concurrently recorded gamma oscillations in the mPFC and, less prominently, in the hippocampus during slow- and theta-rhythmic epochs, respectively. Neuronal activity in LS was modulated by locally recorded LFP gamma oscillations: the discharge of the vast majority of recorded cells was significantly modulated by the locally recorded rhythm. As a population, LS units fired near troughs of gamma cycles. LFP and the neuronal discharge recorded simultaneously from LS and mPFC displayed coordinated patterns of activity between the two regions in the gamma frequency band. Furthermore, our recordings of LFP and neuronal activity in LS in novel and familiar environments suggest experience-dependence of network synchrony in LS and its potential relevance for shaping behavioral responses to novelty processed by hippocampus and mPFC.