Bidirectional prefrontal-hippocampal interactions support context-guided memory

“…paper. anuscript A uthor M anuscript A uthor M anuscript A uthor M anuscript with theta during context exploration and during object sampling, confirming that each LFP recording reflects local oscillations of relevant neural activity at each trial phase (Supplementary Table 1; Buzsaki et al.12).”

“, 2014, 2017), we hypothesized that experimental head injury could disrupt neurophysiological function in two critical brain regions subserving these functions, namely, the hippocampus and medial prefrontal cortex (McDonald et al., 2002; Sigurdsson and Duvarci, 2015; Place et al., 2016).”

“Notably, a similar mechanism was observed for PFC–hippocampus interactions in rats [71] and monkeys [55], where the exact frequency determined the directionality of the information flow.”

“…context, hippocampal networks send information about the context to the prefrontal cortex, whereas when the animal subsequently evaluates the object choices, prefrontal networks send information to the hippocampus, presumably to guide retrieval of the appropriate memories (Place et al. 2016).”

“, 2015), plays a critical role in regulating hippocampal encoding of information beyond space and time (Gruber et al., 2017; Navawongse and Eichenbaum, 2013; Place et al., 2016; Young and Shapiro, 2011).”

“These results are also consistent with episodic memory findings that PFC biases encoding and retrieval of mnemonic information in HPC (9, 28, 29) and a recent proposal (30) that memories for individual experiences are updated through HPC-mPFC interactions to create generalized knowledge that supports complex behaviors…”

“Research in rodents, however, does provide some clues as to the necessity and directionality of vmPFC-hippocampal communication during associative learning (Place et al., 2016).”

“Recognizing the appropriate learning context and ultimately selecting the right hippocampal map may require extrahippocampal processing and inputs (Place et al., 2016).”

“2015) and during the retrieval of goal-relevant memories in rodents (Place et al. 2016).”

“…implicated in different goal-directed behaviors in rodents, including contextual and spatial memory (Benchenane et al., 2010; Harvey et al., 2012; Place et al., 2016), multisensory integration (Song et al., 2017; Aronov et al., 2017; Terada et al., 2017), and sensory detection (Pinto and Dan,…”

“…the idea that PFC-hippocampus engage in coordinated activity [143–145], and in fact point to the role of the prefrontal cortex in driving hippocampal activity in certain situations when the goal states (e.g. current target) need to be retrieved in a context appropriate manner [109,147,148].”

“How might this switch be mediated? The prefronal cortex (PFC) might possibly play an important role, given its interaction with the hippocampus is known to be modulated by task demands (Place et al., 2016).”

“The importance of the hippocampus in representing trial blocks or abstract states is consistent with a growing body of work showing a role for the hippocampal-frontal interactions in decision making, both spatial and not (Barron et al., 2013; Boorman et al., 2016; Ginther et al., 2011; Mack et al., 2016; Miller et al.…”

“[161] found that when animals explored objects within a known environment, the mPFC oscillated first and the HC was entrained to the mPFC’s theta rhythm.”

“…conceptual learning: the vmPFC is hypothesized to bias hippocampal retrieval toward relevant memories by highlighting task-relevant features and discounting specific details (Rich and Shapiro, 2009; van Kesteren et al., 2012; Navawongse and Eichenbaum, 2013; Mack et al., 2016; Place et al., 2016).”

“Furthermore, we have shown that the direction of information flow during scene imagination mirrors that observed during memory retrieval (Place et al., 2016), with vmPFC driving hippocampal activity.”

“Additional evidence suggests that hippocampal — mPFC interactions are critical when conceptual knowledge is applied to new situations with the same underlying conceptual structure [9 ,76].”

“10), suggesting that forming new episodic memories involves the flow of neural activity from posterior regions into the frontal lobe 47 .”

“This fits well with previous work showing that activity in the hippocampus precedes that in the mPFC in rats during context-guided retrieval (Place et al., 2016)2 and in humans during autobiographical memory construction (McCormick et al.”

“Furthermore, theta frequency synchronization between dHPC and mPFC has been observed during goal selection in long-term memory tasks (Benchenane et al., 2010; Preston and Eichenbaum, 2013; Place et al., 2016), and may therefore generally reflect the retrieval of task-relevant representations to guide decision-making.”

“This is important to note because our MVGC toolbox has been widely adopted within the community, with > 3;500 downloads and a significant number of high-impact research publications using the method (e.g., Yellin et al., 2015; Bruneau et al., 2015; Place et al., 2016; Schmitt et al., 2017; Wilber et al., 2017).”

“Frequency-specific synchrony is a wide-spread neuronal phenomenon and has been reported in various cognitive tasks (Buschman and Miller, 2007; Phillips et al., 2014; Place et al., 2016) and in different brain networks involving for example sensory cortices (Gregoriou et al.”

“Recent evidence suggests that the prefrontal cortex (PFC) is involved in influencing this type of hippocampal maintenance of relevant memories in a context-dependent manner [100,101].”

“Previous studies have employed these methods to investigate the interactions between/among different brain areas in cognitive function and abnormalities in neurological diseases [21-35].”

“For example, theta oscillations in the HPC have been shown to precede those in the medial prefrontal cortex (mPFC) when subjects first enter a unique context, while mPFC theta activity precedes that in the HPC later in the trial when decisions are made within this context [41].”

“…recording studies have shown that encoding of object–place associative information requires the flow of information from the HPC to the mPFC (Place et al., 2016), whereas retrieval requires mPFC to HPC information trnasfer (Place et al., 2016) via the NRe (Hallock et al., 2016;).”

“…information traveling in corticohippocampus circuits, we speculate that these circuits exhibit preferential wiring for keeping a global record of spatialtemporal relationships in the service of guiding future memorybased decisions (Wood et al., 1999; Buzsáki and Moser, 2013; Place et al., 2016).”

“Collectively, this provides support for the idea that bidirectional HPC → mPFC and mPFC → RE → HPC interactions act to guide context-appropriate recall of episodic memories 9,66,67 , and that these interactions may be facilitated by neural synchrony in different frequency bands 41,68 – 70 .”

“On the authority of the theta-amplitude cross-correlation in the hippocampal/prefrontal pathway, the correlation invigorates following an accurate performance under a context learning task (Place et al., 2016).”

“For instance, mPFC neural activity precedes hippocampal and ventral temporal lobe activity during memory retrieval 214–217 .”

“Moreover, the neural activity becomes transiently coupled between the mPFC and hippocampus during the retrieval of the mapping (Place et al., 2016) as well as decisionmaking guided by the retrieved mapping (Hyman et al.”

“Our findings are consistentwith recent findings in rodents (Place et al., 2016) that have shown that hippocampal–PFC”

“…considerable data revealing bidirectional projections of the midline thalamic RE with both the mPFC and HPC (Vertes, 2006; Padilla-Coreano et al., 2012; Anderson et al., 2016; Place et al., 2016; Eichenbaum, 2017; Ramanathan et al., 2018a; Dolleman-van der Weel et al., 2019; Vertes et al., 2022).”

“pal memories can be used to anticipate attentional states (Place et al., 2016).”

“…hippocampus and PFC are functionally coupled at various stages of SWM, and the direction of this coupling may transition from a predominantly hippocampus-to-PFC information flow during encoding and maintenance to a ‘top-down’ flow during retrieval (see also Eichenbaum, 2017; Place et al., 2016).”

“Depending on the phase of memory processing, the prefrontal-hippocampal coupling via oscillatory synchrony has been found to be either unidirectional from the HP to PFC or bidirectional (Siapas et al., 2005; Hallock et al., 2016; Place et al., 2016).”

“Neuroscience of temporal sequences Neurons that are selectively activated for particular serial positions in a sequences are present in many areas of the frontal cortex of monkeys [31] and in rat hippocampus [28].”

“studies (Andino-Pavlovsky et al., 2017; Guise & Shapiro, 2017; Place et al., 2016) correspond to respiration-coupled oscillations, which were recently shown to be prominent in the mPFC (Biskamp et al.”

“campus (Benchenane et al. 2010; Fujisawa and Buzsaki 2011; Place et al. 2016) or the primary somatosensory cortex and the hippocampus (Grion et al.”

“Cognitive State: Context Memory Significant evidence supports the generally-accepted view that the HPC is critically important for context memories (e.g., Burgess et al., 2002; Howard and Eichenbaum, 2013; Smith et al., 2013; Eichenbaum, 2014; Place et al., 2016; Maurer and Nadel, 2021).”

“, 2010), and the type of information being processed (Place et al., 2016).”

“Finally, bidirectional prefrontalhippocampal interactions may support context-guided memory, wherein the hippocampus sends contextual information to the prefrontal cortex, which guides the successful retrieval of memories in the hippocampus [76].”

“Furthermore, it has been shown that coordination of theta oscillations between the HPC and the mPFC increases during free exploration (20), anxiety-related behaviors (21, 22), decision making (23), and mnemonic processes that are spatial/contextually guided and rewarded (24, 25).”

“Such a context-dependent shift has been suggested in previous analyses of decision-making.(67,85,86) We further explored this shift by examining when individual assemblies”

“Second, we measured these cytokines in the hippocampus and prefrontal cortex, two key brain regions related to the memory network (Place et al., 2016).”

“The mPFC receives input from the hippocampus, which is thought to provide information about the current context [39,40].”

“Rodent electrophysiological studies have also revealed synchronized activity between hippocampus and PFC in these frequency bands during spatial memory tasks (Simons and Spiers, 2003; Jones and Wilson, 2005; Benchenane et al., 2010; Place et al., 2016; Spiers, 2021).”

“, 2018), and electrophysiology experiments find interactions between HPC and dmPFC local field potentials, spike times, or both (Siapas et al., 2005; Jones and Wilson, 2005; Hyman et al., 2005; Sirota et al., 2008; Hyman et al., 2010; Benchenane et al., 2010; Hyman et al., 2011; Colgin, 2011; Gordon, 2011; O’Neill et…”

“In contrast, the medial prefrontal cortex leads over the hippocampus when rats sample the objects [10, 11].”

“Previous studies have identified unidirectional information transfer in the direct ventral hippocampus–mPFC pathway 43,44 and the mPFC–hippocampus bidirectional indirect pathway via the thalamic nucleus reuniens 45 , whereas the role of the LEC–mPFC pathway remained enigmatic as a ‘missing piece’…”

“This boundary effect has been recently replicated in the rodent hippocampus during two paradigms where space served to contextualize experience (Bulkin et al., 2018; Place et al., 2016).”

“For example, the correlation (including Granger correlations) of LFPs showed that hippocampal theta oscillations precede mPFC theta oscillations during spatial contextual tasks, while this trend reverses in an object-guided task.(45) In other cases, the influence may be bidirectional, lasting over several theta cycles.”

“Mechanistically, integration occurs when previously stored memories are reactivated as new, related information is being encoded via hippocampal-medial prefrontal [61] theta oscillations [71], with MPFC guiding reinstatement of relevant memories [72] and driving mismatch computations [73].”

“Rodent electrophysiological studies have also revealed synchronized activity between the hippocampus and PFC in these frequency bands during spatial memory tasks (Simons and Spiers 2003; Jones and Wilson 2005; Benchenane et al. 2010; Place et al. 2016; Spiers 2020).”

“It conveys updated value information to hippocampus 33 – 35 and amygdala 36,37 for the formation and retrieval of value-associated memories, and also shares intense reciprocal connections with other cortical areas where sensory and motor information is analyzed and extracted 8,38 – 40 .”

“Moreover, rodents that were trained in the one-trial inhibitory avoidance task, considerable evidence have indicated that memory consolidation and retrieval were associated with the CaMKIICREB signaling pathways in the HPC and the PFC (Place et al. 2016; Ghasemzadeh and Rezayof 2016).”

“Moreover, several results support the idea that these connections bidirectionally exchange theta information (Siapas et al. 2005; Place et al. 2016) as in the present model.”

“Electrophysiological studies in rodents (Buzsáki and Draguhn, 2004; Place et al., 2016; Tort et al., 2009) and magnetoencephalography data in humans (Backus et al.”

“Interestingly, the communication latency between PFC and HP is hypothesized to be approximately 26 to 28 ms or approximately 1⁄4 of a theta cycle [43].”