Bidirectional prefrontal-hippocampal interactions support context-guided memory
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We compared the dynamics of hippocampal and prefrontal interactions in rats as they used spatial contexts to guide the retrieval of object memories. Functional connectivity analysis indicated a flow of contextual information from the hippocampus to prefrontal cortex upon the rat's entry into the spatial context. Conversely, upon the onset of object sampling, the direction of information flow reversed, consistent with prefrontal control over the retrieval of context-appropriate hippocampal memory representations.
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Theta oscillations in the hippocampus precede those in the PFC during the onset of contextual exploration, while prefrontal cortical theta precedes that in the hippocampus during the onset of object exploration.
“Theta oscillations in the hippocampus precede those in the PFC during the onset of contextual exploration, while the prefrontal cortical theta precedes that in the hippocampus during the onset of object exploration”
From The medial prefrontal cortex - hippocampus circuit that integrates information of object, place and time to construct episodic memory in rodents: Behavioral, anatomical and neurochemical properties (2020) · cites this paper as Place et al., 2016
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The nucleus reuniens orchestrates prefrontal-hippocampal synchrony during spatial working memory
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“…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;).”
From Engrams to Pathologies of the Brain
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“…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).”
BackgroundMemory instability as a gateway to generalization
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Thalamic nucleus reuniens coordinates prefrontal-hippocampal synchrony to suppress extinguished fear
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“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 .”
Theta Oscillations Through Hippocampal/Prefrontal Pathway: Importance in Cognitive Performances
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Theta oscillations promote temporal sequence learning
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“For instance, mPFC neural activity precedes hippocampal and ventral temporal lobe activity during memory retrieval 214–217 .”
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“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.”
MethodGruber, M. J., Hsieh, L., Staresina, B. P., Elger, C. E., Fell, J., Axmacher, N., & Charan Ranganath, A. (2018) · Journal of Cognitive Neuroscience · doi:10.1162/jocn_a_01302 · Cited by 51 · see citing works
“Our findings are consistentwith recent findings in rodents (Place et al., 2016) that have shown that hippocampal–PFC”
InfluentialNeural circuits for the adaptive regulation of fear and extinction memory
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“…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).”
BackgroundPreparation for upcoming attentional states in the hippocampus and medial prefrontal cortex
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“pal memories can be used to anticipate attentional states (Place et al., 2016).”
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“…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).”
A retrieval-specific mechanism of adaptive forgetting in the mammalian brain
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“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).”
BackgroundInfluentialDimensions and mechanisms of memory organization
de Sousa, A. F., Chowdhury, A., & Silva, A. J. (2021) · Neuron · doi:10.1016/j.neuron.2021.06.014 · Cited by 46 · see citing works
Huang, T., Guo, W., Wang, Y., Chang, L., Shang, N., Chen, J., Fan, R., Zhang, L., Gao, X., Niu, Q. L., et al. (2020) · Neurotoxicity Research · doi:10.1007/s12640-020-00283-0 · Cited by 42 · see citing works
Short-term memory for spatial, sequential and duration information
Manohar, S., Pertzov, Y., & Masud Husain, B. (2017) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2017.05.023 · Cited by 41 · see citing works
“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].”
BackgroundHippocampal–prefrontal interactions during spatial d ecision‐making
Tavares, L. C. S., & Tort, A. B. L. (2021) · Hippocampus · doi:10.1002/hipo.23394 · Cited by 41 · see citing works
“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.”
BackgroundFernandez, L. M. J., Comte, J., Merre, P. L., Lin, J., Salin, P. A., & Crochet, S. (2016) · Cerebral Cortex · doi:10.1093/cercor/bhw311 · Cited by 37 · see citing works
“campus (Benchenane et al. 2010; Fujisawa and Buzsaki 2011; Place et al. 2016) or the primary somatosensory cortex and the hippocampus (Grion et al.”
BackgroundResponse Flexibility: The Role of the Lateral Habenula
Hones, V. I., & Mizumori, S. J. Y. (2022) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2022.852235 · Cited by 38 · see citing works
“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).”
BackgroundACC Theta Improves Hippocampal Contextual Processing during Remote Recall
Wirt, R. A., & Hyman, J. M. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.04.080 · Cited by 39 · see citing works
“, 2010), and the type of information being processed (Place et al., 2016).”
BackgroundValence processing in the PFC: Reconciling circuit-level and systems-level views.
Coley, A. A., Padilla-Coreano, N., Patel, R. R., & Tye, K. (2021) · International review of neurobiology · doi:10.1016/bs.irn.2020.12.002 · Cited by 36 · see citing works
What’s in a context? Cautions, limitations, and potential paths forward
Stark, S. M., Reagh, Z. M., Yassa, M. A., & Stark, C. E. L. (2017) · Neuroscience Letters · doi:10.1016/j.neulet.2017.05.022 · Cited by 37 · see citing works
“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].”
BackgroundStress Facilitates the Development of Cognitive Dysfunction After Chronic Ethanol Exposure
Rodberg, E. M., den Hartog, C. R., Anderson, R. I., Becker, H. C., Moorman, D. E., & Vazey, E. M. (2017) · Alcoholism Clinical and Experimental Research · doi:10.1111/acer.13444 · Cited by 37 · see citing works
Morici, J. F., Weisstaub, N., & Zold, C. L. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2203024119 · Cited by 37 · see citing works
“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).”
Physiological Signature of Memory Age in the Prefrontal-Hippocampal Circuit
Makino, Y., Polygalov, D., Bolaños, F., Benucci, A., & McHugh, T. J. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.11.075 · Cited by 36 · see citing works
Modulation of local field potentials and neuronal activity in primate hippocampus during saccades
Doucet, G., Gulli, R. A., Corrigan, B. W., Duong, L., & Martínez-Trujillo, J. (2019) · Hippocampus · doi:10.1002/hipo.23140 · Cited by 36 · see citing works
Chen, D., Kunz, L., Lv, P., Zhang, H., Zhou, W., Liang, S., Axmacher, N., & Wang, L. (2021) · Science Advances · doi:10.1126/sciadv.abj0200 · Cited by 34 · see citing works
Information transmission in HPC-PFC network for spatial working memory in rat
Xia, M., Liu, T., Bai, W., Zheng, X., & Tian, X. (2018) · Behavioural Brain Research · doi:10.1016/j.bbr.2018.08.024 · Cited by 34 · see citing works
Domanski, A. P. F., Kucewicz, M. T., Russo, E., Tricklebank, M. D., Robinson, E. S. J., Durstewitz, D., & Jones, M. W. (2023) · Current Biology · doi:10.1016/j.cub.2023.02.029 · Cited by 34 · see citing works
“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”
BackgroundResultNeuroprotectin D1 Protects Against Postoperative Delirium-Like Behavior in Aged Mice
Zhou, Y., Wang, J., Li, X., Li, K., Chen, L., Zhang, Z., & Peng, M. (2020) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2020.582674 · Cited by 32 · see citing works
“Second, we measured these cytokines in the hippocampus and prefrontal cortex, two key brain regions related to the memory network (Place et al., 2016).”
MethodConcept formation as a computational cognitive process
Morton, N. W., & Preston, A. R. (2021) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2020.12.005 · Cited by 32 · see citing works
“The mPFC receives input from the hippocampus, which is thought to provide information about the current context [39,40].”
BackgroundDas, A., & Menon, V. (2021) · Journal of Neuroscience · doi:10.1523/jneurosci.0802-21.2021 · Cited by 33 · see citing works
“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).”
BackgroundShi, Z., Wen, Y., Huang, Z., Yu, L., & Zhang, D. (2020) · Stroke and Vascular Neurology · doi:10.1136/svn-2019-000309 · Cited by 31 · see citing works
Hasz, B. M., & Redish, A. D. (2020) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2020.107215 · Cited by 31 · see citing works
“, 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…”
BackgroundLi, K., Wang, J., Chen, L., Guo, M., Zhou, Y., Li, X., 张宗泽, & Peng, M. (2022) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2021.751570 · Cited by 31 · see citing works
Theta Oscillations Support Prefrontal-hippocampal Interactions in Sequential Working Memory
Su, M., Hu, K., Liu, W., Wu, Y., Wang, T., Cao, C., Sun, B., Zhan, S., & Ye, Z. (2023) · Neuroscience Bulletin · doi:10.1007/s12264-023-01134-6 · Cited by 30 · see citing works
“In contrast, the medial prefrontal cortex leads over the hippocampus when rats sample the objects [10, 11].”
Developmental differences in temporal schema acquisition impact reasoning decisions
Pudhiyidath, A., Roome, H. E., Coughlin, C. A., Nguyen, K. V., & Preston, A. R. (2019) · Cognitive Neuropsychology · doi:10.1080/02643294.2019.1667316 · Cited by 32 · see citing works
Spaced training enhances memory and prefrontal ensemble stability in mice
Glas, A., Hübener, M., Bonhoeffer, T., & Goltstein, P. M. (2021) · Current Biology · doi:10.1016/j.cub.2021.06.085 · Cited by 30 · see citing works
Beyond hippocampus: Thalamic and prefrontal contributions to an evolving memory
Yadav, N., Toader, A. C., & Rajasethupathy, P. (2024) · Neuron · doi:10.1016/j.neuron.2023.12.021 · Cited by 31 · see citing works
Construction and use of mental models: Organizing principles for the science of brain and mind
Duncan, J. (2024) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2024.109062 · Cited by 30 · see citing works
Peng, X., & Burwell, R. D. (2021) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2021.107520 · Cited by 29 · see citing works
Estradiol and progesterone in female reward-learning, addiction, and therapeutic interventions
Hilz, E. N., & Lee, H. J. (2022) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2022.101043 · Cited by 25 · see citing works
Prefrontal and lateral entorhinal neurons co-dependently learn item–outcome rules
Jun, H., Lee, J. Y., Bleza, N. R., Ichii, A., Donohue, J. D., & Igarashi, K. M. (2024) · Nature · doi:10.1038/s41586-024-07868-1 · Cited by 26 · see citing works
“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’…”
Bladon, J. H., Sheehan, D. J., Freitas, C. S. D., & Howard, M. W. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.1420-18.2019 · Cited by 27 · see citing works
“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).”
BackgroundThe role of the pre-commissural fornix in episodic autobiographical memory and simulation
Williams, A. N., Ridgeway, S., Postans, M., Graham, K. S., Lawrence, A. D., & Hodgetts, C. J. (2020) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2020.107457 · Cited by 25 · see citing works
Theta oscillations as a substrate for medial prefrontal-hippocampal assembly interactions
Nardin, M., Kaefer, K., Stella, F., & Csicsvari, J. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.113015 · Cited by 27 · see citing works
“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.”
MethodMemory allocation and integration in rodents and humans
Schlichting, M. L., & Frankland, P. W. (2017) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2017.07.013 · Cited by 25 · see citing works
“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].”
BackgroundDas, A., & Menon, V. (2022) · Cerebral Cortex · doi:10.1093/cercor/bhac018 · Cited by 24 · see citing works
“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).”
BackgroundCognitive neurophysiology of the prefrontal cortex
Helfrich, R. F., & Knight, R. T. (2019) · Handbook of clinical neurology · doi:10.1016/b978-0-12-804281-6.00003-3 · Cited by 22 · see citing works
Varga, N. L., Morton, N. W., & Preston, A. R. (2024) · Oxford University Press eBooks · doi:10.1093/oxfordhb/9780190917982.013.47 · Cited by 23 · see citing works
Salimi, M., Ghazvineh, S., Nazari, M., Dehdar, K., Garousi, M., Zare, M., Tabasi, F., Jamaati, H., Salimi, A., Barkley, V., et al. (2021) · Brain Research · doi:10.1016/j.brainres.2021.147368 · Cited by 24 · see citing works
Chen, W., Liang, J., Wu, Q., & Han, Y. (2024) · Nature Communications · doi:10.1038/s41467-024-50388-9 · Cited by 30 · see citing works
“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 .”
Amiri, S., Jafari‐Sabet, M., Keyhanfar, F., Falak, R., Shabani, M., & Rezayof, A. (2020) · Psychopharmacology · doi:10.1007/s00213-020-05465-4 · Cited by 21 · see citing works
“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).”
Prefrontal Synaptic Activation During Hippocampal Memory Reactivation
Nishimura, Y., Ikegaya, Y., & Sasaki, T. (2020) · Cell Reports · doi:10.1016/j.celrep.2021.108885 · Cited by 21 · see citing works
Ursino, M., Cesaretti, N., & Pirazzini, G. (2022) · Cognitive Neurodynamics · doi:10.1007/s11571-022-09836-9 · Cited by 20 · see citing works
“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.”
BackgroundResultJafari‐Sabet, M., Mofidi, H., & Attarian-Khosroshahi, M.-S. (2017) · Canadian Journal of Physiology and Pharmacology · doi:10.1139/cjpp-2017-0228 · Cited by 20 · see citing works
Varga, N. L., & Manns, J. R. (2021) · NeuroImage · doi:10.1016/j.neuroimage.2021.118600 · Cited by 22 · see citing works
“Electrophysiological studies in rodents (Buzsáki and Draguhn, 2004; Place et al., 2016; Tort et al., 2009) and magnetoencephalography data in humans (Backus et al.”
Yu, J. Y., & Frank, L. M. (2021) · PLoS Biology · doi:10.1371/journal.pbio.3001393 · Cited by 19 · see citing works
“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].”
- Authors
- Place, R., Farovik, A., Brockmann, M., & Eichenbaum, H.
- Affiliations
- Boston University (US)
- Venue
- Nature Neuroscience
- Published
- 2016-08
- Volume
- 19
- Issue
- 8
- Pages
- 992-994
- ISSN
- 1097-6256 (ISSN-L)
- 1546-1726
- PMC
- PMC4961615
- OpenAlex
- W2470034833
- Semantic Scholar
- 62121b3f1a5d06bcf2dc7e797e92d8322a273694
- Cited by
- 200
- References
- 25
- Citations by year
- 2026: 10 · 2025: 20 · 2024: 16 · 2023: 16 · 2022: 19 · 2021: 23 · 2020: 23 · 2019: 13 · 2018: 24 · 2017: 28 · 2016: 8
- FWCI
- 15.48
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute of Mental Health (R01MH051570, P50MH094263)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Keywords
- bidirectional information flow, spatial context, hippocampus, prefrontal cortex, functional connectivity, rats
- MeSH terms
- Animals, Behavior, Animal, Hippocampus, Male, Memory, Nerve Net, Neurons, Reward, Prefrontal Cortex, Rats, Long-Evans
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