Prefrontal Theta Oscillations Promote Selective Encoding of Behaviorally Relevant Events

Abstract

The ability to capture the most relevant information from everyday experiences without constantly learning unimportant details is vital to survival and mental health. While decreased activity of the medial prefrontal cortex (mPFC) is associated with failed or inflexible encoding of relevant events in the hippocampus, mechanisms used by the mPFC to discern behavioral relevance of events are not clear. To address this question, we chemogenetically activated excitatory neurons in the mPFC of male rats and examined its impact on local network activity and differential associative learning dependent on the hippocampus. Rats were exposed to two neutral stimuli in two environments whose contingency with an aversive stimulus changed systematically across days. Over 2 weeks of differential and reversal learning, theta band activity began to ramp up toward the expected onset of the aversive stimulus, and this ramping activity tracked the subsequent shift of the set (stimulus modality to environment) predictive of the aversive stimulus. With chemogenetic mPFC activation, the ramping activity emerged within a few sessions of differential learning, which paralleled faster learning and stronger correlations between the ramping activity and conditioned responses. Chemogenetic mPFC activity, however, did not affect the adjustment of ramping activity or behavior during reversal learning or set-shifting, suggesting that the faster learning was not because of a general enhancement of attention, sensory, or motor processing. Thus, the dynamics of the mPFC network activation during events provide a relevance-signaling mechanism through which the mPFC exerts executive control over the encoding of those events in the hippocampus.

Prefrontal–hippocampal interaction during the encoding of new memories

“…In trace eyeblink conditioning, chemogenetic activation of excitatory neurons in the prelimbic region enables rats to associate a neutral stimulus and eyelid shock over an extended temporal interval that is prohibitively long for untreated rats to learn ( Volle et al, 2016 ). Moreover, in a differential learning paradigm, in which the only one of the two neutral stimuli is paired with eyelid shock, the same manipulation facilitates the formation of differential association without erroneously increasing behavioural responses to the other neutral stimulus ( Jarovi et al, 2018 ). In both studies, the chemogenetic manipulation specifically augmented the duration of oscillatory activity evoked by the shock-predictive stimulus, but not the non-predictive stimulus.…”

Increases in theta CSD power and coherence during a calibrated stop-signal task: implications for goal-conflict processing and the Behavioural Inhibition System

“…Specifically, during memory recall, the hippocampus (acting as the core of the BIS) is thought to reduce the effects of interference by eliminating competing memories to enable the individual to recall only the correct memory (Gray & McNaughton, 2000). Furthermore, rodent research has identified increased theta synchrony between the medial prefrontal cortex and the hippocampus during memory retrieval (O'Neill, Gordon, & Sigurdsson, 2013) and during the encoding of behaviourally relevant events (Jarovi, Volle, Yu, Guan, & Takehara-Nishiuchi, 2018). Therefore, it is possible that the MF theta, observed here as part of an MF-MPO region pair during goal conflict, is related to the BIS process of resolving conflicts between competing, behaviourally relevant, memories during recall.…”

Prefrontal neural ensembles develop selective code for stimulus associations within minutes of novel experiences

“…In fact, one hour after training in contextual fear conditioning, the transcription of multiple plasticity-related genes is upregulated in the mPFC, leading to immediate changes in synaptic structure and physiology (Bero et al, 2014). Parallel studies also showed that by enhancing the activity of mPFC neurons during training, it is possible to facilitate the acquisition of hippocampusdependent memories (Benn et al, 2016;Volle et al, 2016;Jarovi et al, 2018;Shibano et al, 2020). These observations, along with earlier findings of impaired hippocampus-dependent memories with disrupted mPFC (Hannesson et al, 2004;Takehara-Nishiuchi et al, 2005;Zhao et al, 2005;Barker and Warburton, 2008;Gilmartin and Helmstetter, 2010;Devito and Eichenbaum, 2011;Gilmartin et al, 2013;Bero et al, 2014), led us to hypothesize that the mPFC may work with, but not follows, the hippocampus to form new memories (Takehara-Nishiuchi, 2020b).…”