Interplay between Hippocampal Sharp-Wave-Ripple Events and Vicarious Trial and Error Behaviors in Decision Making

Abstract

Summary Current theories posit that memories encoded during experiences are subsequently consolidated into longer-term storage. Hippocampal sharp-wave ripple (SWR) events have been linked to this consolidation process during sleep, but SWRs also occur during awake immobility, where their role remains unclear. We report that awake SWR rates at the reward site are inversely related to the prevalence of vicarious trial and error (VTE) behaviors, thought to be involved in deliberation processes. SWR rates were diminished immediately after VTE behaviors and an increase in the rate of SWR events at the reward site predicted a decrease in subsequent VTE behaviors at the choice point. Furthermore, SWR disruptions increased VTE behaviors. These results suggest an inverse relationship between SWRs and VTE behaviors, and suggest that awake SWRs and associated planning and memory consolidation mechanisms are engaged specifically in the context of higher levels of behavioral certainty.

Episodic memory retrieval success is associated with rapid replay of episode content

“…Under similar conditions in rodents replay is known to occur preferentially during brief high-frequency sharp-wave ripple (SWR) events in the hippocampus (19)(20)(21). In contrast, slower theta-related sequence events are observed during active navigation and decision making in rodents (19,20,22,23). Thus, during memory retrieval, we expected that performance in the current experiment would be supported by replay events with a relatively longer lag between states.…”

“…Previous research demonstrating replay, which did not link replay to behavior, identified an approximately 40-50 ms lag between states (elements of a sequence) either during tasks involving lengthy planning periods or during rest periods (17,18). Under similar conditions in rodents replay is known to occur preferentially during brief high-frequency sharp-wave ripple (SWR) events in the hippocampus (19)(20)(21). In contrast, slower theta-related sequence events are observed during active navigation and decision making in rodents (19,20,22,23).…”

A Closer Look at the Hippocampus and Memory

“…Interestingly, iterative viewing could serve to increase processing and binding of interrelationships among stimuli. Rodents exhibit similar iterative viewing behaviors, which are strongly linked to memory formation [41], are disrupted by hippocampal lesions [56, 57], and are associated with hippocampal theta activity and sharp-wave ripples [58, 59]. Other self-generated exploratory behaviors that enhance learning in the rodent (i.e., rearing) have been independently associated with increased hippocampal activity [60].…”

Three brain states in the hippocampus and cortex

“…In a range of behavioral paradigms requiring the hippocampus, substantial time is spent outside locomotion. For example, in navigational paradigms, animals routinely pause or reduce locomotion, whether over the course of spontaneous exploratory excursions, upon attainment of the goal location, or as a consequence of imposed delays that render tasks hippocampus‐dependent (Ainge et al, ; Eilam & Golani, ; Papale, Zielinski, Frank, Jadhav, & Redish, ; Redish, ; Tolman, ; Wallace & Whishaw, ). In our own experiments using a simple navigational maze, we find that unambiguous still state periods comprise ∼25% of all time in the task (Kay et al, ).…”