Multiple modes of hippocampal-prefrontal interactions in memory-guided behavior.

paper Cited Public

Authors: Shin, Justin D; Jadhav, Shantanu P
Year: 2016
Journal: Current opinion in neurobiology
PMID: 27543753
DOI: 10.1016/j.conb.2016.07.015
PMCID: PMC5056827

Figure 1

Distinct network states in the hippocampal-prefrontal network during behavior(a) Spike and local field potential (LFP) activity in CA1 region of the hippocampus (green) and PFC (black) as an animal approaches a reward well in a spatial task. From top to bottom, the plot shows respectively: broadband LFP (1–400 Hz) in CA1, ripple band filtered LFP (150–250 Hz) in CA1, raster plot with spikes from 18 CA1 place cells, broadband LFP in PFC, raster plot with spikes from 7 PFC neurons, and animal speed. As the animal runs on the track (speed scale bar: 10 cm/sec), CA1 place cells fire in a sequential order. (b) When the animal stops at the reward well, SWRs and replay activity are prominent in the hippocampus. Vertical gray rectangle backgrounds in a denote SWRs detected in CA1 LFP. (c) Theta oscillations are seen in hippocampus during running. Shaded area over CA1 LFP from a on an expanded time scale. Theta filtered LFP (6–12 Hz) is shown overlaid with the broadband LFP. Adapted from [31**] with permission from authors.

Figure 2

Theta and SWR interactions in the hippocampal-prefrontal network during behavior(a) Example of CA1 and PFC cells with overlapping spatial patterns of firing in a W-track spatial alternation task. Color scale indicates spiking intensity on the track. Both cells are preferentially active during outbound trajectories to right (arrows). (b) Schematic illustrating theta coupling between CA1 and PFC observed during exploratory behavior. Schematic on left illustrates phase-locking of spiking to theta oscillations; the one on right illustrates coherence, i.e. phase alignment of theta oscillations in CA1 and PFC. (c) CA1 and PFC cells are phase-locked to hippocampal theta at different characteristic phases. (d) Increase in CA1-PFC theta coherence specifically in the theta band (6–12 Hz) as animals approach the choice point in a maze. (e) Schematic illustrating replay of CA1 place cells during SWRs. Decoded CA1 activity represents spatial trajectories in the maze. SWRs are observed primarily at reward locations (cyan circles) on the W-maze. (f) Activity of CA1 and PFC cells aligned to hippocampal SWRs. PFC cells show both SWR-triggered activation and suppression of activity. (g) Reactivation of spatial information in the hippocampal-prefrontal network. CA1-PFC cell pairs with high spatial overlap are reactivated together during SWRs, while those with dissimilar patterns are suppressed. Adapted from [31**] with permission from authors.

Figure 3

Different network patterns can represent different modes of communication between brain regions. (a) Schematic illustrating that multiple network activity patterns mediate hippocampal-prefrontal interactions during memory-guided behavior. Theta interactions, associated with place cell activity in the hippocampus, are prominent as animals traverse locations in spatial mazes. Awake SWRs are associated with coordinated reactivation of ongoing experience in hippocampal-prefrontal ensembles. During SWRs, PFC cells with representations related to concurrently reactivated hippocampal cells are preferentially excited, while PFC cells with unrelated representations are inhibited. Gamma synchrony also mediates hippocampal-prefrontal interactions, and may play a role in organizing theta and SWR interactions. (b) A closed-loop feedback strategy that couples real-time detection to optogenetic perturbation can be used to selectively perturb communication during specific activity patterns (illustrated for SWRs).

#	Section	Preview
20	Figure 1	Distinct network states in the hippocampal-prefrontal network during behavior(a) Spike and local…
21	Figure 2	Theta and SWR interactions in the hippocampal-prefrontal network during behavior(a) Example of CA1…
22	Figure 3	Different network patterns can represent different modes of communication between brain regions. (a)…

Name	Type
4 Hz rhythms local	phenotype
animals	cohort
anterior cingulate cortex	anatomy
anxiety-like behavior	phenotype
awake SWRs local	phenotype
Awake SWRs local	phenotype
Behavioral history local	phenotype
Behavioral learning local	phenotype
beta oscillations	phenotype
Beta oscillations local	drug
CA1	anatomy
CA3	anatomy
cognition	phenotype
contextual memory retrieval local	phenotype
Correct trials	phenotype
cortex	anatomy
Cue-guided retrieval local	phenotype
Dorsal CA1 local	anatomy
Encoding local	phenotype
entorhinal cortex	anatomy
Fast gamma	phenotype
Flexibility local	phenotype
gamma oscillations	phenotype
Gamma oscillations local	drug
Gamma synchronization local	phenotype
gamma synchrony local	phenotype
Gamma synchrony local	phenotype
Hippocampal-PFC network local	anatomy
Hippocampal-prefrontal ensembles local	phenotype
hippocampal-prefrontal interaction local	phenotype
Hippocampal-prefrontal network	anatomy
Hippocampal SWR replay local	phenotype
hippocampus	anatomy
Imagination local	phenotype
Incorrect trials local	phenotype
infralimbic cortex	anatomy
Intermediate CA1 local	anatomy
learning	phenotype
long-term memory	phenotype
medial prefrontal cortex	anatomy
memory	phenotype
memory-guided behavior local	phenotype
Memory-guided behavior local	phenotype
Memory-guided decision making local	phenotype
memory-guided decisions local	phenotype
Network pattern local	phenotype
neurological disorders	phenotype
novelty detection	phenotype
Nucleus reuniens local	anatomy
optogenetic perturbation local	drug
Oscillatory coherence local	phenotype
perirhinal cortex	anatomy
Place cell activity local	phenotype
Place cell sequences local	phenotype
planning	phenotype
Postrhinal cortex local	anatomy
prefrontal cortex	anatomy
prelimbic cortex	anatomy
Prospective decision making local	phenotype
Reactivation local	phenotype
reinforcement learning	phenotype
retrieval	phenotype
reward	phenotype
sharp-wave ripples local	drug
Sharp-wave ripples local	drug
Sharp-wave ripples local	phenotype
Sharp wave-ripples (SWRs) local	phenotype
slow gamma	phenotype
slow-wave sleep	phenotype
Spatial cognitive maps local	phenotype
spatial learning	phenotype
spatial memory	phenotype
Spatial navigation	phenotype
Spiking correlations local	phenotype
subiculum	anatomy
SWR events local	phenotype
SWR replay local	phenotype
Task representations local	phenotype
temporal lobe	anatomy
theta band	phenotype
Theta coherence	phenotype
theta interactions local	phenotype
theta oscillations	phenotype
Theta synchrony local	phenotype
Ventral CA1 local	anatomy
ventral hippocampus	anatomy
Wakefulness	phenotype
working memory	phenotype

Citation	PMID	DOI	Status
Battaglia, FP et al., Trends Cogn Sci, 2011, The hippocampus: hub of brain network communication for memory	21696996	10.1016/j.tics.2011.05.008	Cited
Benchenane, K et al., Curr Opin Neurobiol, 2011, Oscillations in the prefrontal cortex: a gateway to memory and attention	21429736	10.1016/j.conb.2011.01.004	Cited
Benchenane, K et al., Neuron, 2010, Coherent theta oscillations and reorganization of spike timing in the hippocampal- prefrontal network upon learning	20620877	10.1016/j.neuron.2010.05.013	Cited
Brincat, SL et al., Nat Neurosci, 2015, Frequency-specific hippocampal-prefrontal interactions during associative learning	25706471	10.1038/nn.3954	Cited
Buckner, RL et al., Ann N Y Acad Sci, 2008, The brain’s default network: anatomy, function, and relevance to disease	18400922	10.1196/annals.1440.011	Cited
Buschman, TJ et al., Neuron, 2012, Synchronous oscillatory neural ensembles for rules in the prefrontal cortex	23177967	10.1016/j.neuron.2012.09.029	Cited
Buzsaki, G et al., Curr Opin Neurobiol, 2015, Editorial overview: brain rhythms and dynamic coordination	25700995	10.1016/j.conb.2015.01.016	Cited
Buzsaki, G, Cereb Cortex, 1996, The hippocampo-neocortical dialogue	8670641	10.1093/cercor/6.2.81	Cited
Buzsaki, G, Hippocampus, 2015, Hippocampal sharp wave-ripple: A cognitive biomarker for episodic memory and planning	26135716	10.1002/hipo.22488	Cited
Buzsaki, G, Neuron, 2002, Theta oscillations in the hippocampus	11832222	10.1016/s0896-6273(02)00586-x	Cited
Carr, MF et al., Nat Neurosci, 2011, Hippocampal replay in the awake state: a potential substrate for memory consolidation and retrieval	21270783	10.1038/nn.2732	Cited
Carr, MF et al., Neuron, 2012, Transient slow gamma synchrony underlies hippocampal memory replay	22920260	10.1016/j.neuron.2012.06.014	Cited
Cenquizca, LA et al., Brain Res Rev, 2007, Spatial organization of direct hippocampal field CA1 axonal projections to the rest of the cerebral cortex	17559940	10.1016/j.brainresrev.2007.05.002	Cited
Cheng, S et al., Neuron, 2008, New experiences enhance coordinated neural activity in the hippocampus	18215626	10.1016/j.neuron.2007.11.035	Cited
Cho, KK et al., Neuron, 2015, Gamma rhythms link prefrontal interneuron dysfunction with cognitive inflexibility in Dlx5/6(+/−) mice	25754826	10.1016/j.neuron.2015.02.019	Cited
Churchwell, JC et al., Neurobiol Learn Mem, 2010, Prefrontal and hippocampal contributions to encoding and retrieval of spatial memory	20074655	10.1016/j.nlm.2009.12.008	Cited
Colgin, LL et al., Nature, 2009, Frequency of gamma oscillations routes flow of information in the hippocampus	19924214	10.1038/nature08573	Cited
Colgin, LL, Nat Rev Neurosci, 2016, Rhythms of the hippocampal network	26961163	10.1038/nrn.2016.21	Cited
Delatour, B et al., Eur J Neurosci, 2002, Projections from the parahippocampal region to the prefrontal cortex in the rat: evidence of multiple pathways	11994135	10.1046/j.1460-9568.2002.01973.x	Cited
Diba, K et al., Nat Neurosci, 2007, Forward and reverse hippocampal place-cell sequences during ripples	17828259	10.1038/nn1961	Cited
Eichenbaum, H et al., From Conditioning to Conscious Recollection, 2001	—	—	—
Floresco, SB et al., J Neurosci, 1997, Selective roles for hippocampal, prefrontal cortical, and ventral striatal circuits in radial-arm maze tasks with or without a delay	9030646	10.1523/JNEUROSCI.17-05-01880.1997	Cited
Foster, DJ et al., Hippocampus, 2007, Hippocampal theta sequences	17663452	10.1002/hipo.20345	Cited
Foster, DJ et al., Nature, 2006, Reverse replay of behavioural sequences in hippocampal place cells during the awake state	16474382	10.1038/nature04587	Cited
Fries, P, Neuron, 2015, Rhythms for Cognition: Communication through Coherence	26447583	10.1016/j.neuron.2015.09.034	Cited
Fujisawa, S et al., Neuron, 2011, A 4 Hz oscillation adaptively synchronizes prefrontal, VTA, and hippocampal activities	21982376	10.1016/j.neuron.2011.08.018	Cited
Gordon, JA, Curr Opin Neurobiol, 2011, Oscillations and hippocampal-prefrontal synchrony	21470846	10.1016/j.conb.2011.02.012	Cited
Gregoriou, GG et al., Science, 2009, High-frequency, long-range coupling between prefrontal and visual cortex during attention	19478185	10.1126/science.1171402	Cited
Gupta, AS et al., Nat Neurosci, 2012, Segmentation of spatial experience by hippocampal theta sequences	22706269	10.1038/nn.3138	Cited
Gupta, AS et al., Neuron, 2010, Hippocampal replay is not a simple function of experience	20223204	10.1016/j.neuron.2010.01.034	Cited
Harris, AZ et al., Annu Rev Neurosci, 2015, Long-range neural synchrony in behavior	25897876	10.1146/annurev-neuro-071714-034111	Cited
Hyman, JM et al., Hippocampus, 2005, Medial prefrontal cortex cells show dynamic modulation with the hippocampal theta rhythm dependent on behavior	16015622	10.1002/hipo.20106	Cited
Ishizuka, N et al., J Comp Neurol, 1990, Organization of intrahippocampal projections originating from CA3 pyramidal cells in the rat	2358523	10.1002/cne.902950407	Cited
Ito, HT et al., Nature, 2015, A prefrontal-thalamo-hippocampal circuit for goal-directed spatial navigation	26017312	10.1038/nature14396	Cited
Jadhav, SP et al., Neuron, 2016, Coordinated Excitation and Inhibition of Prefrontal Ensembles during Awake Hippocampal Sharp-Wave Ripple Events	26971950	10.1016/j.neuron.2016.02.010	Cited
Jadhav, SP et al., Science, 2012, Awake hippocampal sharp-wave ripples support spatial memory	22555434	10.1126/science.1217230	Cited
Ji, D et al., Nat Neurosci, 2007, Coordinated memory replay in the visual cortex and hippocampus during sleep	17173043	10.1038/nn1825	Cited
Jones, MW et al., PLoS Biol, 2005, Theta rhythms coordinate hippocampal-prefrontal interactions in a spatial memory task	16279838	10.1371/journal.pbio.0030402	Cited
Karlsson, MP et al., Nat Neurosci, 2009, Awake replay of remote experiences in the hippocampus	19525943	10.1038/nn.2344	Cited
Kemere, C et al., PLoS One, 2013, Rapid and continuous modulation of hippocampal network state during exploration of new places	24023818	10.1371/journal.pone.0073114	Cited
Logothetis, NK et al., Nature, 2012, Hippocampal-cortical interaction during periods of subcortical silence	23172213	10.1038/nature11618	Cited
Lundqvist, M et al., Neuron, 2016, Gamma and Beta Bursts Underlie Working Memory	26996084	10.1016/j.neuron.2016.02.028	Cited
Miller, EK et al., Annu Rev Neurosci, 2001, An integrative theory of prefrontal cortex function	11283309	10.1146/annurev.neuro.24.1.167	Cited
Miller, EK et al., Curr Opin Neurobiol, 2013, Cortical circuits for the control of attention	23265963	10.1016/j.conb.2012.11.011	Cited
O’Neill, J et al., Trends Neurosci, 2010, Play it again: reactivation of waking experience and memory	20207025	10.1016/j.tins.2010.01.006	Cited
Padilla-Coreano, N et al., Neuron, 2016, Direct Ventral Hippocampal-Prefrontal Input Is Required for Anxiety-Related Neural Activity and Behavior	26853301	10.1016/j.neuron.2016.01.011	Cited
Pfeiffer, BE et al., Nature, 2013, Hippocampal place-cell sequences depict future paths to remembered goals	23594744	10.1038/nature12112	Cited
Pfeiffer, BE et al., Science, 2015, PLACE CELLS. Autoassociative dynamics in the generation of sequences of hippocampal place cells	26160946	10.1126/science.aaa9633	Cited
Place, R et al., Nat Neurosci, 2016, Bidirectional prefrontal-hippocampal interactions support context-guided memory	27322417	10.1038/nn.4327	Cited
Rangel, LM et al., Elife, 2016, Rhythmic coordination of hippocampal neurons during associative memory processing	26751780	10.7554/eLife.09849	Cited
Redish, AD, Nat Rev Neurosci, 2016, Vicarious trial and error	26891625	10.1038/nrn.2015.30	Cited
Remondes, M et al., Cell Rep, 2015, Slow-gamma Rhythms Coordinate Cingulate Cortical Responses to Hippocampal Sharp-Wave Ripples during Wakefulness	26549454	10.1016/j.celrep.2015.10.005	Cited
Remondes, M et al., Neuron, 2013, Cingulate-hippocampus coherence and trajectory coding in a sequential choice task	24239123	10.1016/j.neuron.2013.08.037	Cited
Roumis, DK et al., Curr Opin Neurobiol, 2015, Hippocampal sharp-wave ripples in waking and sleeping states	26011627	10.1016/j.conb.2015.05.001	Cited
Siapas, AG et al., Neuron, 1998, Coordinated interactions between hippocampal ripples and cortical spindles during slow-wave sleep	9856467	10.1016/s0896-6273(00)80629-7	Cited
Siapas, AG et al., Neuron, 2005, Prefrontal phase locking to hippocampal theta oscillations	15820700	10.1016/j.neuron.2005.02.028	Cited
Siegle, JH et al., Elife, 2014, Enhancement of encoding and retrieval functions through theta phase-specific manipulation of hippocampus	25073927	10.7554/eLife.03061	Cited
Singer, AC et al., Neuron, 2009, Rewarded outcomes enhance reactivation of experience in the hippocampus	20064396	10.1016/j.neuron.2009.11.016	Cited
Singer, AC et al., Neuron, 2013, Hippocampal SWR activity predicts correct decisions during the initial learning of an alternation task	23522050	10.1016/j.neuron.2013.01.027	Cited
Sirota, A et al., Neuron, 2008, Entrainment of neocortical neurons and gamma oscillations by the hippocampal theta rhythm	19038224	10.1016/j.neuron.2008.09.014	Cited
Sirota, A et al., Proc Natl Acad Sci U S A, 2003, Communication between neocortex and hippocampus during sleep in rodents	12576550	10.1073/pnas.0437938100	Cited
Spellman, T et al., Nature, 2015, Hippocampal-prefrontal input supports spatial encoding in working memory	26053122	10.1038/nature14445	Cited
Vertes, RP et al., Brain Res Bull, 2007, Nucleus reuniens of the midline thalamus: link between the medial prefrontal cortex and the hippocampus	17292803	10.1016/j.brainresbull.2006.12.002	Cited
Vertes, RP, Synapse, 2004, Differential projections of the infralimbic and prelimbic cortex in the rat	14579424	10.1002/syn.10279	Cited
Wang, GW et al., Neurobiol Learn Mem, 2008, Reversible disconnection of the hippocampal-prelimbic cortical circuit impairs spatial learning but not passive avoidance learning in rats	18614383	10.1016/j.nlm.2008.05.009	Cited
Wierzynski, CM et al., Neuron, 2009, State-dependent spike-timing relationships between hippocampal and prefrontal circuits during sleep	19249278	10.1016/j.neuron.2009.01.011	Cited
Wikenheiser, AM et al., Nat Neurosci, 2015, Hippocampal theta sequences reflect current goals	25559082	10.1038/nn.3909	Cited
Wiltgen, BJ et al., Neuron, 2004, New circuits for old memories: the role of the neocortex in consolidation	15450163	10.1016/j.neuron.2004.09.015	Cited
Womelsdorf, T et al., Science, 2007, Modulation of neuronal interactions through neuronal synchronization	17569862	10.1126/science.1139597	Cited
Yu, JY et al., Neurobiol Learn Mem, 2015, Hippocampal-cortical interaction in decision making	24530374	10.1016/j.nlm.2014.02.002	Cited
Zheng, C et al., Neuron, 2016, Spatial Sequence Coding Differs during Slow and Fast Gamma Rhythms in the Hippocampus	26774162	10.1016/j.neuron.2015.12.005	Cited

In this knowledge base

Title	Year	PMID
Predicting Alcohol-Related Memory Problems in Older Adults: A Machine Learning Study with Multi-Domain Features.	2023	37232664

External

Title	Authors	Journal	Year	Link
Cerebellar iTBS ameliorates post-stroke cognitive impairment via the dentate nucleus-ventromedial thalamus pathway.	Pan Y et al.	—	2026	→
Elevated calneuron-1, an accessory subunit of muscarinic receptors, induces frontotemporal dysconnectivity and schizophrenia-like deficits.	Oelschlegel AM et al.	—	2026	→
Disruption of hippocampal-prefrontal neural dynamics and risky decision-making in a mouse model of Alzheimer's disease.	Kim EJ et al.	—	2025	→
Hippocampal-Prefrontal Communication Subspaces Align with Behavioral and Network Patterns in a Spatial Memory Task.	Young RA et al.	—	2025	→
The neural basis of cognitive processing: A review and a speculative architecture.	Verwey WB	—	2025	→
The role of prefrontal-hippocampal functional connectivity in schizophrenia-related cognitive dysfunction and the thalamic ventral midline involvement: <i>in vivo</i> and <i>silico</i> evidence.	Černousova A et al.	—	2025	→
Theta-encoded information flow from dorsal CA1 to prelimbic cortex drives memory reconsolidation.	Radiske A et al.	—	2025	→
Theta-gamma phase-amplitude coupling as a promising neurophysiological biomarker for evaluating the efficacy of low-intensity focused ultrasound stimulation on vascular dementia treatment.	Wang F et al.	—	2025	→
A hierarchical active inference model of spatial alternation tasks and the hippocampal-prefrontal circuit.	Van de Maele T et al.	—	2024	→
Dynamic prediction of goal location by coordinated representation of prefrontal-hippocampal theta sequences.	Wang Y et al.	—	2024	→
Enhanced Hippocampus-Nidopallium Caudolaterale Interaction in Visual-Spatial Associative Learning of Pigeons.	Zhu JY et al.	—	2024	→
Prefrontal cortical ripples mediate top-down suppression of hippocampal reactivation during sleep memory consolidation.	Shin JD et al.	—	2024	→
Cannabidiol attenuates fear memory expression in female rats via hippocampal 5-HT<sub>1A</sub> but not CB1 or CB2 receptors.	Franzen JM et al.	—	2023	→
Geometric transformation of cognitive maps for generalization across hippocampal-prefrontal circuits.	Tang W et al.	—	2023	→
Neurofunctional underpinnings of individual differences in visual episodic memory performance.	Geissmann L et al.	—	2023	→
Performance Baseline of Phase Transfer Entropy Methods for Detecting Animal Brain Area Interactions.	Zhu JY et al.	—	2023	→
Predicting Alcohol-Related Memory Problems in Older Adults: A Machine Learning Study with Multi-Domain Features.	Kamarajan C et al.	—	2023	→
Closed-loop Modulation of the Self-regulating Brain: A Review on Approaches, Emerging Paradigms, and Experimental Designs.	Farkhondeh Tale Navi F et al.	—	2022	→
Dissociable oscillatory theta signatures of memory formation in the developing brain.	Johnson EL et al.	—	2022	→
Rhythmic coordination and ensemble dynamics in the hippocampal-prefrontal network during odor-place associative memory and decision making.	Symanski CA et al.	—	2022	→
Top-down control of hippocampal signal-to-noise by prefrontal long-range inhibition.	Malik R et al.	—	2022	→
Altered hippocampal-prefrontal functional network integrity in adult macaque monkeys with neonatal hippocampal lesions.	Li CX et al.	—	2021	→
Developing of Focal Ischemia in the Hippocampus or the Amygdala Reveals a Regional Compensation Rule for Fear Memory Acquisition.	Yu CL et al.	—	2021	→
Differential Impact of Acute and Chronic Stress on CA1 Spatial Coding and Gamma Oscillations.	Tomar A et al.	—	2021	→
Disrupting the medial prefrontal cortex with designer receptors exclusively activated by designer drug alters hippocampal sharp-wave ripples and their associated cognitive processes.	Schmidt B et al.	—	2021	→
Inhibition of 14-3-3 Proteins Alters Neural Oscillations in Mice.	Jones ZB et al.	—	2021	→
Learning differentially shapes prefrontal and hippocampal activity during classical conditioning.	Klee JL et al.	—	2021	→
Maternal pregnancy diet, postnatal home environment and executive function and behavior in 3- to 4-y-olds.	Mortaji N et al.	—	2021	→
Organization of parietoprefrontal and temporoprefrontal networks in the macaque.	Giarrocco F et al.	—	2021	→
The secret life of predictive brains: what's spontaneous activity for?	Pezzulo G et al.	—	2021	→
Cognitive Decline of Rats with Chronic Fluorosis Is Associated with Alterations in Hippocampal Calpain Signaling.	Nadei OV et al.	—	2020	→
Dorsomedial prefrontal cortex and hippocampus represent strategic context even while simultaneously changing representation throughout a task session.	Hasz BM et al.	—	2020	→
Human hippocampal CA3 damage disrupts both recent and remote episodic memories.	Miller TD et al.	—	2020	→
Oxytocin protects against 3-NP induced learning and memory impairment in rats: Sex differences in behavioral and molecular responses to the context of prenatal stress.	Moslemi M et al.	—	2020	→
Preparation for upcoming attentional states in the hippocampus and medial prefrontal cortex.	Günseli E et al.	—	2020	→
Spatial encoding in dorsomedial prefrontal cortex and hippocampus is related during deliberation.	Hasz BM et al.	—	2020	→
The role of replay and theta sequences in mediating hippocampal-prefrontal interactions for memory and cognition.	Zielinski MC et al.	—	2020	→
Coherent coding of spatial position mediated by theta oscillations in hippocampus and prefrontal cortex	Zielinski MC et al.	—	2019	—
Coherent Coding of Spatial Position Mediated by Theta Oscillations in the Hippocampus and Prefrontal Cortex.	Zielinski MC et al.	—	2019	→
Distinct Neural Circuits Underlie Prospective and Concurrent Memory-Guided Behavior.	Hamm AG et al.	—	2019	→
Dynamics of Awake Hippocampal-Prefrontal Replay for Spatial Learning and Memory-Guided Decision Making.	Shin JD et al.	—	2019	→
Interactions between the hippocampus, prefrontal cortex, and amygdala support complex learning and memory.	Yavas E et al.	—	2019	→
Reservoir computing model of prefrontal cortex creates novel combinations of previous navigation sequences from hippocampal place-cell replay with spatial reward propagation.	Cazin N et al.	—	2019	→
Sharp-wave ripples as a signature of hippocampal-prefrontal reactivation for memory during sleep and waking states.	Tang W et al.	—	2019	→
Activation of 5-HT7 receptor by administration of its selective agonist, LP-211, modifies explorative-curiosity behavior in rats in two paradigms which differ in visuospatial parameters.	Carbone C et al.	—	2018	→
Disruption of dorsal hippocampal - prefrontal interactions using chemogenetic inactivation impairs spatial learning.	Maharjan DM et al.	—	2018	→
Identification of Protein Kinase C Isoforms Involved in Type 1 Diabetic Encephalopathy in Mice.	Zheng J et al.	—	2018	→
Immunolocalization of muscarinic M1 receptor in the rat medial prefrontal cortex.	Oda S et al.	—	2018	→
Inactivation of nucleus reuniens impairs spatial working memory and behavioral flexibility in the rat.	Viena TD et al.	—	2018	→
Hippocampal Administration of Levothyroxine Impairs Contextual Fear Memory Consolidation in Rats.	Yu D et al.	—	2017	→
Hippocampal-Prefrontal Reactivation during Learning Is Stronger in Awake Compared with Sleep States.	Tang W et al.	—	2017	→
Internally generated hippocampal sequences as a vantage point to probe future-oriented cognition.	Pezzulo G et al.	—	2017	→
Multivariate cross-frequency coupling via generalized eigendecomposition.	Cohen MX	—	2017	→
The Interplay of Hippocampus and Ventromedial Prefrontal Cortex in Memory-Based Decision Making.	Weilbächer RA et al.	—	2016	→