Coupling of Sharp Wave Events between Zebrafish Hippocampal and Amygdala Homologues

Abstract

The mammalian hippocampus exhibits spontaneous sharp wave events (1-30 Hz) with an often-present superimposed fast ripple oscillation (120-220 Hz) to form a sharp wave ripple (SWR) complex. During slow-wave sleep or quiet restfulness, SWRs result from the sequential spiking of hippocampal cell assemblies initially activated during learned or imagined experiences. Additional cortical/subcortical areas exhibit SWR events that are coupled to hippocampal SWRs, and studies in mammals suggest that coupling may be critical for the consolidation and recall of specific memories. In the present study, we have examined juvenile male and female zebrafish, and show that SWR events are intrinsically generated and maintained within the telencephalon and that their hippocampal homologue, the anterodorsolateral lobe (ADL), exhibits SW events with approximately 9% containing an embedded ripple (SWR). Single-cell calcium imaging coupled to local field potential (LFP) recordings, revealed that approximately 10% of active cells in the dorsal telencephalon participate in any given SW event. Furthermore, fluctuations in cholinergic tone modulate SW events consistent with mammalian studies. Moreover, the basolateral amygdala (BLA) homologue exhibits SW events with approximately 5% containing an embedded ripple. Computing the SW peak coincidence difference between the ADL and BLA showed bidirectional communication. Simultaneous coupling occurred more frequently within the same hemisphere, and in coupled events across hemispheres, the ADL more commonly preceded BLA. Together, these data suggest conserved mechanisms across species by which SW and SWR events are modulated, and memories may be transferred and consolidated through regional coupling.Significance StatementWe provide a comprehensive analysis of spontaneous activity within the telencephalon of juvenile zebrafish, demonstrating that SWR events are intrinsically generated and maintained within this structure. SWs are modulated by the cholinergic system and possibly other cortical/subcortical areas. We also show that SW events are associated with neuronal ensemble activity. Additionally, we provide evidence that the BLA exhibits SWR events. Spontaneous activity between the ADL and BLA shows bidirectional communication, which suggests conserved mechanisms by which learned experiences are transferred and consolidated in this vertebrate. These findings showcase conserved memory-related mechanisms between mammals and zebrafish, and further support the use of zebrafish to better understand molecular mechanisms that interfere with processes critical to learning and memory consolidation.