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Cited by 158Memory and Neural MechanismsMemory Processes and InfluencesNeuroscience and Neuropharmacology Research

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

Open access
Chao, Owen Y., de Souza Silva, Maria A., Yang, Yi-Mei, Huston, Joseph P.·2020·Neuroscience & Biobehavioral Reviews
DOI 10.1016/j.neubiorev.2020.04.007PMC PMC7302494
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Abstract

Rats and mice have been demonstrated to show episodic-like memory, a prototype of episodic memory, as defined by an integrated memory of the experience of an object or event, in a particular place and time. Such memory can be assessed via the use of spontaneous object exploration paradigms, variably designed to measure memory for object, place, temporal order and object-location inter-relationships. We review the methodological properties of these tests, the neurobiology about time and discuss the evidence for the involvement of the medial prefrontal cortex (mPFC), entorhinal cortex (EC) and hippocampus, with respect to their anatomy, neurotransmitter systems and functional circuits. The systematic analysis suggests that a specific circuit between the mPFC, lateral EC and hippocampus encodes the information for event, place and time of occurrence into the complex episodic-like memory, as a top-down regulation from the mPFC onto the hippocampus. This circuit can be distinguished from the neuronal component memory systems for processing the individual information of object, time and place.

AI snapshot

Written from the paper’s full text.

TL;DR

This review synthesizes evidence that rodents show episodic-like memory—integrated memory for what, where, and when—measured by training-free spontaneous object exploration paradigms. It proposes that a specific mPFC–lateral entorhinal cortex–hippocampus circuit, especially direct mPFC–CA1/CA3 pathways, integrates object, place, and time information, distinct from the component memory systems.

Key findings

  • Episodic-like memory tests combine novel object preference (what), object place preference (where), and temporal-order memory (when). In the ELM2–2 test, adult rats show exploration preferences RD > RS, OS > RS, and OS > OD; ELM2–2 memory is preserved for at least 1 hour, over 2 hours, but not after 4–6 hours, while ELM2–1 memory can last up to 24 hours.
  • Disconnecting the mPFC–CA3 circuit impaired ELM2–2 episodic-like memory while leaving individual NOP, OPP, and TOM memories intact, indicating that episodic-like memory is a meta-system integrating what, where, and when rather than a simple sum of the components. Disconnecting mPFC–CA1 impaired integration and OPP but spared NOP and TOM; disconnecting mPFC–LEC also impaired ELM2–2.
  • The proposed circuit includes direct and indirect mPFC–hippocampus pathways: posterior-dorsal CA1-to-PFC projections support the “when” component, intermediate CA1-to-PFC projections support the “where” component, and CA1/CA3 are cardinal for integration.
  • Neurotransmitter systems in mPFC and hippocampus (glutamate, dopamine, serotonin, acetylcholine, histamine, norepinephrine, cannabinoids) differentially modulate NOP, OPP, TOM, and episodic-like memory; for example, mPFC AMPA/kainate but not NMDA receptors are involved in episodic-like memory.

Methods

  • Design: narrative review of behavioral, anatomical, and neurochemical evidence on episodic-like memory in rodents, focusing on training-free spontaneous object exploration paradigms (NOP, OPP, TOM, SNOP, OiP, and ELM variants).
  • Data/sample: published rodent studies, primarily articles published after 2007; the review excludes context-manipulated object exploration tests such as What-Where-Which and excludes systemic, intracerebroventricular, or global gene-manipulation studies.
  • Analysis: qualitative synthesis comparing lesion, inactivation, disconnection, electrophysiological, pharmacological, imaging, and molecular findings, with summary tables and circuit diagrams.

Limitations

  • Stated: NOP alone is not an appropriate measure of episodic-like memory; methodological factors such as habituation, object exploration duration, object properties, retention interval, circadian phase, and light intensity can confound object exploration tests.
  • Stated: many lesion studies used retention intervals under 10 minutes, and the direction of information flow in disconnection studies is hard to ascertain because connections are ablated; precise circuit control such as optogenetics is needed.
  • Evident from the text: as a narrative review, it does not describe a systematic search or meta-analysis, and its conclusions depend on heterogeneous paradigms, species/strains, and separate studies rather than uniform within-study comparisons.

Model-written summary. Check it against the paper before relying on it.

Integrity signals

Registry

Crossref · 10.1016/j.neubiorev.2020.04.007

Cites

447 of 447 references verified0 citation errors · 0 not checkable

Statistics

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Claims the paper makes

0 of 526 cited sources checked · 0 supported · 0 flagged

  • Findingcitation

    PFC-CA1 disconnected animals showed intact spatial recognition in the ELM2-2 test (positive where index).

    “The disruption of episodic-like memory could not have resulted from the impairment of object location memory since the PFC-CA1 disconnected animals showed intact spatial recognition in the ELM2–2 test (positive where index).”
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    • cites Chao et al., 2017 source

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    • The authors state this as an assumption: If two brain areas interact for a specific function, disrupting one of the areas in one hemisphere combined with a simultaneous disruption of the other area in the opposite hemisphere should lead to a functional deficit.
  • Findingcitation

    When the PFC-CA1 circuit was interrupted, the ability to integrate distinct components into an episodic-like memory was impaired.

    “When the PFC-CA1 circuit was interrupted, the ability to integrate distinct components into an episodic-like memory was impaired.”
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    • cites Chao et al., 2017 source

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    • The authors state this as an assumption: If two brain areas interact for a specific function, disrupting one of the areas in one hemisphere combined with a simultaneous disruption of the other area in the opposite hemisphere should lead to a functional deficit.
  • Findingcitation

    Memory tested by the ELM2-2 test was deficient after disconnecting the PFC-LEC circuit.

    “As expected, memory tested by the ELM2–2 test was deficient, suggesting the PFC-LEC circuit is indispensable for episodic-like memory.”
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    • cites Chao et al., 2016a

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    • The authors state this as an assumption: If two brain areas interact for a specific function, disrupting one of the areas in one hemisphere combined with a simultaneous disruption of the other area in the opposite hemisphere should lead to a functional deficit.
  • Findingcitation

    Disconnection of the PFC-CA1 pathway, while preserving the indirect CA3-LEC-PFC circuit, impaired the interaction index.

    “Disconnection of the PFC-CA1 pathway, while preserving the indirect CA3-LEC-PFC circuit, impaired the interaction index.”
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    • cites Chao et al., 2017 source

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    • The authors state this as an assumption: If two brain areas interact for a specific function, disrupting one of the areas in one hemisphere combined with a simultaneous disruption of the other area in the opposite hemisphere should lead to a functional deficit.
  • Premisecitation

    With the help of sleep for the facilitation of NOP consolidation, object memory can be preserved for up to 3 weeks.

    “With the help of sleep for the facilitation of NOP consolidation, the memory can be preserved for up to 3 weeks (Sawangjit et al., 2018).”
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    • cites Sawangjit et al., 2018 source

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    Findingcitation

    After PFC-CA1 disconnection, performance in the OPP test (where) was disrupted, whereas memories for NOP (what) and TOM (when) were intact.

    “Furthermore, performance in the OPP test (where) was disrupted, whereas memories for NOP (what) and TOM (when), were intact.”
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    • cites Chao et al., 2017 source

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    • The authors state this as an assumption: If two brain areas interact for a specific function, disrupting one of the areas in one hemisphere combined with a simultaneous disruption of the other area in the opposite hemisphere should lead to a functional deficit.

  • May combine two claims.

    Findingcitation

    Disconnecting the PFC-CA3 circuit impaired performance in the ELM2-2 test, but did not interfere with performance in the individual NOP, OPP and TOM tests.

    “By contrast, disconnecting the PFC-CA3 circuit also impaired performance in the ELM2–2 test, but did not interfere with performance in the individual NOP, OPP and TOM tests.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites de Souza Silva et al., 2016 source

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    • The authors state this as an assumption: If two brain areas interact for a specific function, disrupting one of the areas in one hemisphere combined with a simultaneous disruption of the other area in the opposite hemisphere should lead to a functional deficit.

  • May combine two claims.

    Findingcitation

    When the PFC-CA3 pathway was disconnected, the interaction, as well as the where and when indexes were disrupted.

    “When the PFC-CA3 pathway was disconnected, the interaction, as well as the where and when indexes were disrupted.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites de Souza Silva et al., 2016 source

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    • The authors state this as an assumption: If two brain areas interact for a specific function, disrupting one of the areas in one hemisphere combined with a simultaneous disruption of the other area in the opposite hemisphere should lead to a functional deficit.

  • May combine two claims.

    Findingcitation

    After disconnecting the PFC-LEC pathway, the where component was still functional, although weakened, sparing the direct CA3-CA1-PFC circuit.

    “Using the ELM2–2 test, it was found that the where component was still functional, although weakened after disconnecting the PFC-LEC pathway, which spared the direct CA3-CA1-PFC circuit.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Chao et al., 2016a

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    • The authors state this as an assumption: If two brain areas interact for a specific function, disrupting one of the areas in one hemisphere combined with a simultaneous disruption of the other area in the opposite hemisphere should lead to a functional deficit.

  • Classified as probably not a substantial claim.

    Premisecitation

    Episodic-like memory is not simply a combination of what, where and when memories, but a meta-system which integrates these three components into a complex and distinct compound system.

    “Based on the experimental model, episodic-like memory has been found to be not simply a combination of “what”, “where” and “when” memories, but a meta-system which integrates these three components into a complex and distinct compound system (de Souza Silva et al., 2016).”
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    Premisecitation

    Habituation to the testing environment reduces novelty-induced arousal or anxiety and directly contributes to memory for objects.

    “Habituation to the testing environment, which reduces novelty-induced arousal or anxiety, directly contributes to memory for objects.”
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    • cites Maroun and Akirav, 2008

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    Premisecitation

    Rodents have memory for objects for up to 24 hours, and even up to 48 hours.

    “Early studies have indicated that rodents have memory for objects for up to 24 hours (Ennaceur and Delacour, 1988), and even up to 48 hours (Liu et al., 2016).”
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    • cites Ennaceur and Delacour, 1988

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    • cites Liu et al., 2016 source

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    Interpretationreasoning

    In training-based models, the neurobiological system of episodic memory is likely to converge with the amygdala and/or nucleus accumbens for coping with anxiety/fear and/or incentive motivation.

    “Therefore, in such training-based models the neurobiological system of episodic memory is likely to converge with the amygdala and/or nucleus accumbens for coping with anxiety/fear and/or incentive motivation, respectively.”
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    Premisecitation

    Animals can show a memory akin to human episodic memory, with arguments based on evolution, neuroanatomy and neurobiology.

    “The past two decades studies have revealed new insight on this question with evidence that animals can show a memory akin to human episodic memory, with arguments based on evolution, neuroanatomy and neurobiology (Allen and Fortin, 2013; Fortin et al., 2004; Manns and Eichenbaum, 2006; Templer and Hampton, 2013).”
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    • cites Fortin et al., 2004 source

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    • cites Manns and Eichenbaum, 2006

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    Premisenone given

    Spontaneous object exploration in rodent studies of recognition memory is a well-established training-free animal model.

    “Alternatively, spontaneous object exploration in rodent studies of recognition memory is a well-established training-free animal model.”
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    Premisecitation

    Animals can behaviorally respond at certain intervals (seconds to minutes) according to a programmed stimulus.

    “Studies in training animals with classical and operant conditioning have shown that animals can behaviorally respond at certain intervals (seconds to minutes) according to the programmed stimulus (Kirsch et al., 2004; Kyd et al., 2008)”
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    Premisereasoning

    Similar neuroanatomical and neurobiological substrates of memory systems are shared by different species with humans, including a prototype of episodic memory which can be studied in animal models to decipher its neurobiological mechanisms.

    “These perspectives propose that similar neuroanatomical and neurobiological substrates of memory systems are shared by different species with humans, including a prototype of “episodic memory” which can be studied in animal models to decipher its neurobiological mechanisms.”
    Quote in the paperSubstantial claim

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    Premisecitation

    Spontaneous object exploration can be used to assess memory for what (NOP), for where (OPP), and for when (TOM).

    “Spontaneous object exploration can be used to assess memory for “what” (novel object preference; NOP) (Ennaceur and Delacour, 1988), for “where” (object place preference; OPP) (Ennaceur et al., 1997), and for “when” (memory for temporal order or recency; TOM) (Mitchell and Laiacona, 1998).”
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    • cites Ennaceur and Delacour, 1988

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    • cites Ennaceur et al., 1997 source

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    • cites Mitchell and Laiacona, 1998

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    Premisecitation

    Half of the tested mice were able to retain OPP information for up to 6 months, but not after 1 year.

    “In addition, it has been found that the half of the tested mice was able to retain OPP information for up to 6 months, but not after 1 year (Atucha et al., 2019).”
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    • cites Atucha et al., 2019

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    Premisecitation

    Long intervals of days can be timed with internal biological systems of circadian rhythms in animals.

    “Long intervals of days can be timed with internal biological systems of circadian rhythms in animals (Buhusi and Meck, 2005).”
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    • cites Buhusi and Meck, 2005

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    Premisecitation

    Rats are able to anticipate food with 24-hour intervals but not 18-hour intervals.

    “Rats are able to anticipate food with 24-, but not 18-hour intervals (Petersen et al., 2014)”
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    • cites Petersen et al., 2014 source

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    Study design and conductnone given

    Confounding interpretations such as absence of preference for a given object, fear of novelty, hyper- or hypo-locomotor activity, sensorimotor malfunctions and others can affect spontaneous object exploration tests.

    “Caution must be exercised to rule out confounding interpretations, such as the absence of preference for a given object, fear of novelty, hyper- or hypo-locomotor activity, sensorimotor malfunctions and others.”
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    Interpretationnone given

    The methodological factors which impact NOP also influence the OPP test.

    “The methodological factors which impact NOP also influence the OPP test.”
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    Premisecitation

    The placing of animals into the testing arena from the same or different starting locations can potentially impact an OPP-like test, as hippocampus-lesioned rats showed a memory impairment when starting to explore from different, but not the same, locations.

    “The placing of animals into the testing arena from the same or different starting locations can potentially impact an OPP-like test, as it was shown that hippocampus-leisoned rats showed a memory impairment when starting to explore from different, but not the same, locations (see 3.3.2; (Langston and Wood, 2010).”
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    Premisecitation

    Rats are sensitive to the temporal cue of 'how long ago' but not to the cue of 'when' in an episodic-like memory test.

    “They found that rats are sensitive to the cue of “how long ago”, but not to the cue of “when”, and questioned the similarity between episodic-like memory in animals and human episodic memory (Roberts et al., 2008).”
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    • cites Roberts et al., 2008 source

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    Interpretationcitation

    Compared to identical objects, the application of distinct objects in the NOP sample trial is likely to involve not only novel object identity, but also inter-object relationship, and presumably activates brain regions for object-object and/or object-context association more than for object identity.

    “Compared to the application of identical objects, that of distinct objects is likely to involve not only novel object identity, but also inter-object relationship (Arain et al., 2012), which presumably activates brain regions for the processing of object-object and/or object-context association more than that for object identity.”
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    Premisecitation

    A direct way to measure episodic-like memory is to combine the three what, where and when object exploration tests into one integrated paradigm.

    “A direct way to measure episodic-like memory is to combine the three “what”, “where” and “when” object exploration tests into one integrated paradigm (this test was first developed for rats (Kart-Teke et al., 2006) and then adapted for mice (Dere et al., 2005b).”
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    • cites Dere et al., 2005b

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    Premisecitation

    Rats recognize object information in the TOM test with an interval of 3 hours but not after 24 hours.

    “It was also reported that object information in the TOM test with interval of 3 (Barker et al., 2007), but not after 24 (Mitchell and Laiacona, 1998), hours could be “recognized” by rats.”
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    • cites Mitchell and Laiacona, 1998

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    Premisecitation

    The rodent PFC participates in functions such as attention, decision making and memory.

    “Like in primates, the PFC in rodents is considered to participate in functions such as attention, decision making and memory (Chudasama, 2011; Dalley et al., 2004; Preston and Eichenbaum, 2013).”
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    • cites Preston and Eichenbaum, 2013

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    Interpretationreasoning

    The exploration preference patterns RD > RS and OS > OD indicate an interaction between object-location and temporal-order, demonstrating that animals have episodic-like memory.

    “The exploration preference patterns, RD > RS (novel location over old one in recent familiar objects) and OS > OD (old location over novel one in older familiar objects), indicates an interaction between object-location and temporal-order, which demonstrates that the animals have episodic-like memory.”
    Quote in the paperSubstantial claim

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    Interpretationnone given

    The combined 'what-where-when' memory is not merely a summation of the three mnemonic components; it can be impaired when individual memory for 'what', 'where' and 'when' is intact.

    “The combined “what-where-when” memory, however, is not merely a summation of the three mnemonic components, given that “what-where-when” memory could be impaired under the circumstance of intact individual memory for “what”, “where” and “when” (details see section 4.2).”
    Quote in the paperSubstantial claim

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    Premisecitation

    The rodent mPFC is anatomically divided into ACC, PLC and ILC, located along the dorsal-ventral axis, and these subareas are reciprocally interconnected.

    “The rodent mPFC can be anatomically divided into three subareas, namely the anterior cingulate cortex (ACC), prelimbic cortex (PLC) and infralimbic cortex (ILC), which are located along the dorsal – ventral axis (Dalley et al., 2004; Gabbott et al., 2005), and are reciprocally interconnected (Heidbreder and Groenewegen, 2003).”
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    Interpretationreasoning

    Associations between distinct objects (e.g., relative inter-object locations) are processed by the mPFC, while such associative learning is not required when identical objects are applied.

    “A possible explanation is that associations between distinct objects (e.g. relative inter-object locations) are processed by the mPFC, while such associative learning is not required when identical objects are applied.”
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    Interpretationreasoning

    The OiP test presents four distinct objects, instead of two identical objects, and presumably requires higher memory capacity to learn than the NOP/OPP tests.

    “Compared to the NOP and OPP tests, the OiP test presents four distinct objects, instead of two identical objects, as the information to be learned. This test is similar to the SNOP test that applies multiple distinct objects in the sample trial and presumably requires higher memory capacity to learn than the NOP/OPP tests.”
    Quote in the paperNot a substantial claim

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    Interpretationreasoning

    The mPFC is either not required for object recognition memory, or other circuits compensate for this function when the mPFC is inactivated.

    “This implies that the mPFC is either not required for object recognition memory, or that other circuits compensate for this function when the mPFC is inactivated.”
    Quote in the paperSubstantial claim

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    Premisecitation

    Optogenetic stimulation of mPFC glutamatergic neurons does not affect memory for NOP and OPP, but facilitates OiP memory.

    “Optogenetic stimulation of the mPFC glutamatergic neurons did not affect memory for NOP and OPP, but facilitated OiP memory, which is involved in object association information by switching inter-object locations (Benn et al., 2016).”
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    Interpretationreasoning

    A neurobiological system that integrates and organizes different sources of information to form episodic-like memory should exist.

    “Therefore, a neurobiological system which integrates and organizes different sources of information to form such a memory should exist (as discussed below).”
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  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Interpretationreasoning

    The episodic-like memory paradigms are dependent upon the spontaneous object exploration tests of NOP, OPP and TOM and are theoretically influenced by all the methodological factors involved in these tests.

    “The episodic-like memory paradigms (Fig.2) are dependent upon the spontaneous object exploration tests of NOP, OPP and TOM, and thus, theoretically are influenced by all the methodological factors involved in these tests.”
    Quote in the paperNot a substantial claim

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    Premisecitation

    In the ELM2-2 test, adult rats exhibit exploration preferences RD > RS, OS > RS, and OS > OD.

    “In this test, adult rats exhibit a pattern of exploration preferences, where RD > RS (where), OS > RS (when) and OS > OD.”
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    • cites Kart-Teke et al., 2006 source

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    Premisecitation

    Rats retain episodic-like memory for over 2 hours but not after 4-6 hours.

    “Studies manipulating the time interval between trials have shown that rats retain the episodic-like memory for over 2 hours (Belblidia et al., 2015), but not after 4–6 hours (Belblidia et al., 2015; Chao et al., 2014).”
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    Premisecitation

    Pre-sample microinjections into the mPFC of the DA D1/5-R agonist SKF81297 facilitate, and its antagonist SCH23390 disrupt, NOP memory tested 24 hours later.

    “When administrated prior to the sample trial, microinjections into the mPFC of the DA D1/5-R agonist SKF81297 facilitated, and its antagonist SCH23390 disrupted, NOP memory tested 24 hours later (De Bundel et al., 2013; Nagai et al., 2007).”
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    Premisecitation

    Pre-test microinfusions of muscimol into the rat ACC impair NOP memory tested after 24 hours, but not after 20 minutes, implying the ACC is involved in retrieval of NOP in a time-dependent manner.

    “In addition, pre-test microinfusions of muscimol into the rat ACC impaired the NOP memory tested after 24 hours, but not 20 min, implying the ACC is involved in the retrieval of NOP in a time-dependent manner (Pezze et al., 2017).”
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    Premisecitation

    Catecholamine depletion in the mPFC induced by 6-OHDA disrupts TOM, but neither NOP nor OPP.

    “The catecholaminergic systems in the PFC are involved in the processing of TOM, given that catecholamine depletion in the mPFC induced by 6-hydroxydopamine (6-OHDA) disrupted this memory, but neither memory for NOP nor that for OPP (Nelson et al., 2011).”
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    Interpretationcitation

    The midbrain DA interplays with the mPFC in the expression of NOP memory, and communication between a non-lesioned side of the mPFC and midbrain DA systems is necessary for object memory.

    “This implies that the midbrain DA interplays with the mPFC in the expression of NOP memory and that the communication between a non-lesioned side of the mPFC and midbrain DA systems is necessary for object memory.”
    Quote in the paperSubstantial claim

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    Premisecitation

    Transcranial direct current stimulation onto the PFC increases DA levels in the hippocampus and striatum, and improves NOP memory in spontaneous hypertensive rats.

    “Transcranial direct current stimulation onto the PFC also increased DA levels in the hippocampus and striatum, and NOP memory was thereby improved in spontaneous hypertensive rats (Leffa et al., 2016).”
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    Interpretationown data

    Both PFC AMPA/kainate- and NMDA-R are indispensable for encoding of specific object-location relationships, while NMDA-R engages in learning and consolidation, but not recall, of OiP memory.

    “Both the PFC AMPA/kainate- and NMDA-R are indispensable for the encoding of specific object-location relationships, while NMDA-R engages in the learning and consolidation, but not recall, of OiP memory.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Premisecitation

    Pre-sample PFC infusions of AP5 impair OiP memory tested 1 hour later, but not when given pre-test.

    “The same pre-sample PFC infusions of AP5 also impaired OiP memory tested 1 hour later, but not when given pre-test (Barker and Warburton, 2008).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Barker and Warburton, 2008

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  • May combine two claims.

    Interpretationreasoning

    Encoding/consolidation of TOM is dependent upon medial prefrontal cortical AMPA/kainate- and NMDA-R, while AMPA/kainate-R, but not NMDA-R, are required for retrieval of TOM.

    “The encoding/consolidation of TOM is dependent upon the medial prefrontal cortical AMPA/kainate- and NMDA-R, while AMPA/kainate-R, but not NMDA-R, are required for the retrieval of TOM.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Interpretationreasoning

    Expression of NOP memory is dependent on the mGlu5-R, but not the AMPA/kainate-R, of the mPFC.

    “These findings indicate that the expression of NOP memory is dependent on the mGlu5-R, but not the AMPA/kainate-R, of the mPFC.”
    Quote in the paperSubstantial claim

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    Premisecitation

    Long-term (24 hours), but not short-term (5 min), OPP memory is deficient when CREB-binding protein is reduced in the mouse PFC.

    “Long-term (24 hours), but not short-term (5 min), OPP memory was deficient when a cAMP response element binding protein (CREB)-binding protein, histone acetyltransferase, was reduced in the mouse PFC (Vieira and Korzus, 2015).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Vieira and Korzus, 2015

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  • May combine two claims.

    Premisecitation

    A unilateral PFC lesion combined with midbrain DAergic deficiency in the unilateral hemisphere impairs NOP (90 min interval) if lesions are in different hemispheres, but not when in the same hemisphere.

    “A unilateral PFC lesion combined with a midbrain DAergic systems deficiency in the unilateral hemisphere, impaired NOP (90 min interval) if the lesions were in different hemispheres, but not when they were in the same hemisphere.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Chao et al., 2013 source

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  • May combine two claims.

    Premisecitation

    Medial prefrontal cortical DNA methylation, but not histone deacetylation, is involved in OiP memory.

    “In addition, medial prefrontal cortical DNA methylation, but not histone deacetylation, is involved in OiP memory (Scott et al., 2017).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Scott et al., 2017 source

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  • May combine two claims.

    Premisecitation

    Mice with PFC stroke show impaired OPP, but not NOP, memory, along with reduced structural volume in the dorsal medial nucleus of the thalamus.

    “Conversely, mice with PFC stroke showed impaired OPP, but not NOP, memory, along with reduced structural volume in the dorsal medial nucleus of the thalamus (Zhou et al., 2016).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Zhou et al., 2016 source

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  • May combine two claims.

    Premisecitation

    EC-lesioned animals showed deficient spatial navigation in the Morris water maze, but not when spatial cues were provided by proximal objects located in the pool.

    “EC-lesioned animals showed deficient spatial navigation in the Morris water maze (Nyakas et al., 2009; Parron et al., 2004), but not when spatial cues were provided by proximal objects located in the pool (Parron et al., 2004).”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites Nyakas et al., 2009 source

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    • cites Parron et al., 2004

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  • May combine two claims.

    Premisecitation

    Infusions into the mPFC of methyllycaconitine citrate, before learning, or dihydro-β-erythroidine hydrobromide, before the test trial, did not influence OPP (24 hours) memory.

    “In addition, infusions into the mPFC of methyllycaconitine citrate, before learning, or dihydro-β-erythroidine hydrobromide, before the test trial, did not influence OPP (24 hours) memory (Sabec et al., 2018).”
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    • cites Sabec et al., 2018 source

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  • May combine two claims.

    Premisecitation

    Pre-test microinjections of MDL 11,939, a 5-HT2A-R antagonist, into the rat mPFC impaired TOM, but not NOP and OPP, all with 3 hours intervals.

    “Pre-test microinjections of MDL 11,939, a 5-HT2A-R antagonist, into the rat mPFC impaired TOM, but not NOP and OPP, all with 3 hours intervals (Bekinschtein et al., 2013).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Bekinschtein et al., 2013 source

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  • May combine two claims.

    Interpretationreasoning

    Prefrontal cortical D1-R underlie the learning and/or consolidation, but not retrieval, of object-location relevant information.

    “Together, the prefrontal cortical D1-R underlie the learning and/or consolidation, but not retrieval, of object-location relevant information.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Interpretationreasoning

    Neither α7- nor α4β2-nicotinic ACh-R seem to be significantly involved in OPP memory.

    “Neither α7- nor α4β2-nicotinic ACh-R seem to be significantly involved in OPP memory.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Interpretationcitation

    5HT2A-R in the mPFC are critical for memory retrieval in short-term TOM, but not for NOP and OPP.

    “These findings suggest that 5HT2A-R in the mPFC are critical for memory retrieval in short-term TOM, but not for NOP and OPP.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Premisecitation

    The LEC preferentially receives projections from the perirhinal cortex, insular cortex, PLC and ILC, while the MEC mainly connects with the postrhinal, occipital and parietal cortical regions in rats.

    “The LEC preferentially receives projections from the perirhinal cortex, insular cortex, PLC and ILC, while the medial entorhinal cortex (MEC) mainly connects with the postrhinal, occipital and parietal cortical regions in rats (Burwell and Amaral, 1998a, b; Witter et al., 2000).”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites Burwell and Amaral, 1998a, b

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    • cites Witter et al., 2000 source

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  • May combine two claims.

    Premisecitation

    In the SNOP test, impaired spatial recognition and less object exploration were found in EC-lesioned animals.

    “In the SNOP test, impaired spatial recognition and less object exploration were found in EC-lesioned animals (Parron and Save, 2004).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Parron and Save, 2004

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  • May combine two claims.

    Premisecitation

    Projections from the perirhinal cortex to LEC and those from the postrhinal cortex to MEC are functionally different, with the former primarily sending inhibitory signals and the latter primarily sending excitatory ones.

    “Projections from the perirhinal cortex to LEC and those from the postrhinal cortex to MEC are functionally different, with the former primarily sending inhibitory signals (Apergis-Schoute et al., 2007; Pinto et al., 2006; Willems et al., 2018) and the latter primarily sending excitatory ones (Koganezawa et al., 2015).”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites Apergis-Schoute et al., 2007 source

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    • cites Pinto et al., 2006 source

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    • cites Willems et al., 2018 source

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  • May combine two claims.

    Interpretationcitation

    Pharmacological blockage of DA D1- and D2-R and activation of D3-R disrupt short-term object consolidation, but pharmacological activation of DA D1- and D2-R and blockage of D3-R facilitate long-term object consolidation.

    “Pharmacological blockage of DA D1- and D2-R and activation of D3-R disrupt short-term object consolidation, but pharmacological activation of DA D1- and D2-R and blockage of D3-R facilitate long-term object consolidation.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Interpretationreasoning

    The muscarinic ACh-R of the PLC/ILC are essential for the encoding/consolidation, but not retrieval, of TOM and OiP.

    “The muscarinic ACh-R of the PLC/ILC are essential for the encoding/consolidation, but not retrieval, of TOM and OiP.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Interpretationnone given

    Lesion and inactivation studies have provided substantial evidence that TOM, OiP and episodic-like, but not NOP and OPP, memories are dependent on the mPFC.

    “Lesion and inactivation studies have provided substantial evidence that TOM, OiP and episodic-like, but not NOP and OPP, memories are dependent on the mPFC.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Interpretationreasoning

    Pharmacological blockage of prefrontal cortical DA D2- and D3-R leads to NOP deficiency and facilitation, respectively.

    “Thus, pharmacological blockage of the prefrontal cortical DA D2- and D3-R leads to NOP deficiency and facilitation, respectively.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Interpretationreasoning

    It may not be that the mPFC is irrelevant to NOP processing, but rather other neural systems take over when the mPFC is dysfunctional.

    “The results suggest that it may not be the mPFC is irrelevant to NOP processing, but rather other neural systems take over when the mPFC is dysfunctional.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Interpretationreasoning

    The medial prefrontal cortical α7 nicotinic ACh-R underly the learning, but not consolidation and recall, of associative object-location memory, while the α4β2 nicotinic ACh-R are responsible for the retrieval, but not learning and consolidation, of this memory.

    “The medial prefrontal cortical α7 nicotinic ACh-R underly the learning, but not consolidation and recall, of associative object-location memory, while the α4β2 nicotinic ACh-R are responsible for the retrieval, but not learning and consolidation, of this memory.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Premisecitation

    Recent behavioral and electrophysiological evidence indicates that both LEC and MEC process spatial information, with local and global spatial frameworks being represented within LEC and MEC, respectively.

    “Yet, recent behavioral and electrophysiological evidence indicates that both LEC and MEC process spatial information, with local and global spatial frameworks being represented within LEC and MEC, respectively (Knierim et al., 2014; Neunuebel et al., 2013).”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites Knierim et al., 2014 source

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    • cites Neunuebel et al., 2013 source

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  • May combine two claims.

    Interpretationcitation

    The whole EC is likely to engage in long-term object memory, given that EC-lesioned or inactivated animals exhibited deficits in the NOP test when tested 24 hours later.

    “The whole EC is likely to engage in long-term object memory, given that EC-lesioned or inactivated animals exhibited deficits in the NOP test when tested 24 hours later (Lima et al., 2009; Nyakas et al., 2009).”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites Lima et al., 2009 source

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    • cites Nyakas et al., 2009 source

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  • May combine two claims.

    Premisecitation

    Lesions of the MEC did not disrupt memory in the OPP test, but impaired spatial memory tested by the water maze escape task, and combined lesions of the MEC and hippocampus led to a stronger impairment.

    “However, another study showed that lesions of the MEC did not disrupt memory in the OPP test, but impaired spatial memory tested by the water maze escape task and that combined lesions of the MEC and hippocampus led to a stronger impairment (Hales et al., 2014).”
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    • cites Hales et al., 2014 source

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    Premisecitation

    MEC neurons fire for location in the environment and across different contexts, forming "grid-like" activities.

    “In contrast, the MEC neurons fire for location in the environment and across different contexts, forming “grid-like” activities (Fyhn et al., 2004; Hafting et al., 2005).”
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    • cites Fyhn et al., 2004 source

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    • cites Hafting et al., 2005 source

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  • May combine two claims.

    Premisecitation

    Lesions of the LEC did not affect OPP memory, but impaired object-location recognition in a test in which two distinct objects were replaced by two identical ones, chosen from either of the explored type.

    “Lesions of the LEC, on the other hand, did not affect OPP memory (Van Cauter et al., 2013; Wilson et al., 2013c), but impaired object-location recognition in a test in which two distinct objects were replaced by two identical ones, chosen from either of the explored type (Wilson et al., 2013c).”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites Van Cauter et al., 2013 source

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    • cites Wilson et al., 2013c

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  • May combine two claims.

    Premisecitation

    Pre-test microinjections of scopolamine into the MEC had no effect in the NOP test, but decreased the amount of object exploration.

    “Pre-test microinjections of scopolamine into the MEC also had no effect in the NOP test, but decreased the amount of object exploration (Rashid and Ahmed, 2019).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Rashid and Ahmed, 2019

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  • May combine two claims.

    Interpretationcitation

    The LEC preferentially processes object-associated information, e.g., the past and current locations of objects, and the context of the objects.

    “Behavioral, imaging and electrophysiological recording data suggest that LEC preferentially processes object-associated information, e.g., the past and current locations of objects (Beer et al., 2013; Deshmukh and Knierim, 2011; Tsao et al., 2013; Van Cauter et al., 2013), and the context of the objects (Wilson et al., 2013b; Wilson et al., 2013c).”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites Beer et al., 2013 source

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    • cites Deshmukh and Knierim, 2011

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    • cites Tsao et al., 2013 source

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  • May combine two claims.

    Premisecitation

    MEC neurons respond at fixed distances and directions from objects, irrespective of location, shape and size of objects, and have been called object-vector cells.

    “Strikingly, the MEC neurons respond at fixed distances and directions from objects, irrespective of location, shape and size of objects, and have been called object-vector cells (Hoydal et al., 2019).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Hoydal et al., 2019 source

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  • May combine two claims.

    Premisecitation

    Lesions of the LEC of rats spared memory in the classic NOP test, but impaired object memory when 3 or 4 distinct objects were used during the learning.

    “In non-spatial (what) object exploration tests, lesions of the LEC of rats spared memory in the classic NOP test (Kuruvilla and Ainge, 2017; Van Cauter et al., 2013; Wilson et al., 2013b; Wilson et al., 2013c), but impaired object memory when 3 or 4 distinct objects were used during the learning (Hunsaker et al., 2013; Kuruvilla and Ainge, 2017).”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites Kuruvilla and Ainge, 2017

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    • cites Van Cauter et al., 2013 source

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    • cites Wilson et al., 2013b

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  • May combine two claims.

    Premisecitation

    Post-sample infusions of anisomycin into the hippocampal CA1 area impaired long-term (24 hours), but not short-term (3 hours), NOP memory when it was infused within 3, but not 6, hours after the sample trial.

    “Post-sample infusions of anisomycin into the hippocampal CA1 area impaired long-term (24 hours), but not short-term (3 hours), NOP memory when it was infused within 3, but not 6, hours after the sample trial (Rossato et al., 2007), whereas no effect was reported (Balderas et al., 2008).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Rossato et al., 2007 source

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  • May combine two claims.

    Premisecitation

    Rats with hippocampus lesions exhibited intact NOP tested in the same environment, but not in a different one.

    “Rats with hippocampus lesions exhibited intact NOP tested in the same environment, but not in different one.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Piterkin et al., 2008 source

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  • May combine two claims.

    Premisecitation

    The ventral hippocampus is involved in NOP memory, as muscimol infusions led to NOP deficits.

    “The ventral hippocampus is also involved in NOP memory, as muscimol infusions led to NOP deficits (Neugebauer et al., 2018), albeit this was not supported by a lesion study (Broadbent et al., 2004).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Neugebauer et al., 2018 source

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  • May combine two claims.

    Interpretationreasoning

    The hippocampus is undoubtedly important for NOP memory when the retention is over 10 minutes, while its involvement likely depends on contextual novelty, features of context, and probably allocentric signals.

    “Thus, the hippocampus is undoubtedly important for NOP memory when the retention is over 10 minutes (Cohen and Stackman, 2015), while its involvement likely depends on contextual novelty (Kim et al., 2014; Oliveira et al., 2010; Yi et al., 2016), features of context (Piterkin et al., 2008), and probably allocentric signals (Langston and Wood, 2010) (see below).”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites Cohen and Stackman, 2015

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    • cites Kim et al., 2014 source

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    • cites Oliveira et al., 2010 source

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  • May combine two claims.

    Premisecitation

    Post-sample infusions of muscimol and the GABAa-R antagonist bicuculline into the dorsal hippocampus respectively facilitated and disrupted long-term NOP memory in a less-habituated environment, but not after sufficient habituation.

    “Interestingly, post-sample infusions of muscimol and the GABAa-R antagonist bicuculline into the dorsal hippocampus respectively facilitated and disrupted long-term NOP memory in a less-habituated environment, but not after sufficient habituation (Kim et al., 2014; Oliveira et al., 2010).”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites Kim et al., 2014 source

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    • cites Oliveira et al., 2010 source

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  • May combine two claims.

    Interpretationcitation

    The hippocampus is likely involved in NOP consolidation and/or retrieval.

    “On the other hand, the hippocampus is likely involved in NOP consolidation and/or retrieval.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Premisecitation

    Hippocampal CA1 firing rates were enhanced during NOP testing and NOP consolidation is related to an increase of hippocampal CA3-CA1 synaptic efficacy.

    “Hippocampal CA1 firing rates were enhanced during NOP testing (Cohen et al., 2013) and NOP consolidation is related to an increase of the hippocampal CA3-CA1 synaptic efficacy (Clarke et al., 2010).”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites Cohen et al., 2013 source

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    • cites Clarke et al., 2010 source

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  • May combine two claims.

    Premisecitation

    Pre-test muscimol microinjections into the dorsal hippocampus impaired or did not affect NOP memory in mice.

    “Pre-test muscimol microinjections into the dorsal hippocampus was reported to impair (Cohen et al., 2013; Stackman et al., 2016) or not affect (Haettig et al., 2011) NOP memory in mice.”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites Cohen et al., 2013 source

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    • cites Stackman et al., 2016 source

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    • cites Haettig et al., 2011 source

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  • May combine two claims.

    Premisecitation

    Lesions in the dorsal dentate gyrus did not induce NOP/OPP deficits in rats, and DREADD activation of GABAergic parvalbumin neurons in the dentate gyrus showed no effect in the NOP test.

    “However, lesions in the dorsal dentate gyrus did not induce NOP/OPP deficits in rats (Beselia et al., 2010), and DREADD activation of GABAergic parvalbumin neurons in the dentate gyrus also showed no effect in the NOP test, but influenced anxiety-like behaviors, social novelty and contextual fear extinction in mice (Zou et al., 2016).”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites Beselia et al., 2010

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    • cites Zou et al., 2016 source

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  • May combine two claims.

    Premisecitation

    In a setting of exploring three small "positionally" distinct objects, the distal CA1 and proximal CA3 were recruited during the recognition of a novel object, whereas the proximal CA3 and lower blade of dentate gyrus, but not CA1, were involved in novel object recognition during exploring three large "directionally" distinct objects.

    “For instance, in a setting of exploring three small “positionally” distinct objects, the distal CA1 and proximal CA3, which preferentially receive “what” information (Mishkin et al., 1983), were recruited during the recognition of a novel object (increased mRNA of the immediate early genes Arc and Homer1a), whereas the proximal CA3 and lower blade of dentate gyrus, but not CA1, were involved in”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Hoang et al., 2018 source

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  • May combine two claims.

    Interpretationcitation

    Information about object, but not location, can be functionally compensated when the hippocampus is damaged.

    “This result implies that information about object, but not location, can be functionally compensated when the hippocampus is damaged.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Premisecitation

    When the location of two objects was rotated, the CA1 firing pattern remapped, suggesting that the CA1 coordinated the altered spatial information.

    “Electrophysiological recordings of the hippocampal CA1 cells have shown that when the location of two objects was rotated, the CA1 firing pattern remapped, suggesting that the CA1 coordinated the altered spatial information (Lenck-Santini et al., 2005).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Lenck-Santini et al., 2005 source

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  • May combine two claims.

    Premisecitation

    Pre-sample infusions of the protein synthesis inhibitor emetine and the mRNA synthesis inhibitor 5,6-dichlorobenzimidazole 1-β-D-ribofuranoside into the dorsal hippocampus impaired long-term OPP memory, while these infusions did not influence short-term (5 min) OPP memory.

    “Similar effects were found with pre-sample infusions of the protein synthesis inhibitor emetine and the mRNA synthesis inhibitor 5,6-dichlorobenzimidazole 1-β-D-ribofuranoside into the dorsal hippocampus, while these infusions did not influence short-term (5 min) OPP memory (Ozawa et al., 2017).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Ozawa et al., 2017 source

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  • May combine two claims.

    Premisecitation

    Pre-test intra-hippocampus infusions of muscimol disrupted OPP memory tested 24 hours later in rats, supporting a critical role of the hippocampus in the retrieval of long-term OPP memory.

    “Pre-test intra-hippocampus infusions of muscimol also disrupted OPP memory tested 24 hours later in rats (Gaskin et al., 2011), supporting a critical role of the hippocampus in the retrieval of long-term OPP memory.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Gaskin et al., 2011 source

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  • May combine two claims.

    Premisecitation

    The dorsal, but not ventral, hippocampus is critically involved in OPP memory, leading to disrupted OPP memory tested 2 hours, but not 5 min, later.

    “The dorsal, but not ventral, hippocampus has been shown to be critically involved in OPP memory (Gaskin et al., 2009a), leading to disrupted OPP memory tested 2 hours, but not 5 min, later (Tam et al., 2014).”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites Gaskin et al., 2009a

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    • cites Tam et al., 2014 source

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  • May combine two claims.

    Premisecitation

    Application of DREADDs by transferring excitatory- (M3Dq)- or inhibitory- (M4Di)-R into the dorsal hippocampus led to improved long-term memory for OPP, but not NOP, in the M3Dq-activated mice, while the M4Di-activated animals showed the opposite.

    “In line with these findings, application of DREADDs by transferring excitatory- (M3Dq)- or inhibitory- (M4Di)-R into the dorsal hippocampus, led to improved long-term memory for OPP, but not NOP, in the M3Dq-activated mice, while the M4Di-activated animals showed the opposite (Lopez et al., 2016).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Lopez et al., 2016

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  • May combine two claims.

    Interpretationcitation

    The hippocampus plays an important role in OPP memory, which can be mediated by the hippocampal excitatory and inhibitory neurons.

    “Overall, it is clear that the hippocampus plays an important role in OPP memory, which can be mediated by the hippocampal excitatory and inhibitory neurons.”
    Quote in the paperSubstantial claim

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    Premisecitation

    CA1 area was required in both object and location conditions, while CA3 was more recruited for OPP than NOP.

    “CA1 area was required in both object and location conditions, while CA3 was more recruited for OPP than NOP (Beer et al., 2013).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Beer et al., 2013 source

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    Premisecitation

    Post-sample activation of M3Dq selectively in the CA1 interneurons impaired long-term OPP, but not NOP, memory in mice.

    “Post-sample activation of M3Dq selectively in the CA1 interneurons also impaired long-term OPP, but not NOP, memory in mice (Yu et al., 2018).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Yu et al., 2018

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  • May combine two claims.

    Premisecitation

    Mice with specific inactivation of the hippocampal excitatory or inhibitory neurons exhibited long-term OPP deficits, suggesting that both excitatory and inhibitory neurons are cardinal for this memory.

    “Mice with specific inactivation of the hippocampal excitatory or inhibitory neurons exhibited long-term OPP deficits, suggesting that both excitatory and inhibitory neurons are cardinal for this memory (Haettig et al., 2013).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Haettig et al., 2013 source

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  • May combine two claims.

    Premisecitation

    Higher c-fos expression induced by the OPP, but not NOP, test was found in the hippocampal CA1 and CA3 subregions, while Arc mRNA imaging data showed higher involvement of CA3 in OPP than NOP.

    “Higher c-fos expression induced by the OPP, but not NOP, test was found in the hippocampal CA1 and CA3 subregions (Mendez et al., 2015), while Arc mRNA imaging data showed higher involvement of CA3 in OPP than NOP (Beer et al., 2013).”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites Mendez et al., 2015 source

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    • cites Beer et al., 2013 source

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  • May combine two claims.

    Premisecitation

    During "positional" object exploration, LTD was enhanced in the CA1 region, but not dentate gyrus, while the opposite results were found during "directional" object exploration.

    “During “positional” object exploration, LTD was enhanced in the CA1 region, but not dentate gyrus, while the opposite results were found during “directional” object exploration (Kemp and Manahan-Vaughan, 2008).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Kemp and Manahan-Vaughan, 2008

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  • May combine two claims.

    Premisecitation

    Post-sample infusions of the DNMT inhibitor RG108 or 5-aza-2'-deoxycytidine into the hippocampus impaired memory in the OiP, but not NOP, test, suggesting that hippocampal DNA methylation engages in the processing of object-place information.

    “Post-sample infusions of the DNMT inhibitor RG108 or 5-aza-2’-deoxycytidine into the hippocampus impaired memory in the OiP, but not NOP, test, suggesting that hippocampal DNA methylation engages in the processing of object-place information (Scott et al., 2017).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Scott et al., 2017 source

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  • May combine two claims.

    Premisecitation

    Memories for NOP and OPP explicitly altered CA1 and CA3 proteomes, in which the changes of protein expression were largely consistent in CA1 across the two forms of memory, but distinct in CA3.

    “In addition, memories for NOP and OPP explicitly altered CA1 and CA3 proteomes, in which the changes of protein expression were largely consistent in CA1 across the two forms of memory, but distinct in CA3.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites von Ziegler et al., 2018 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    In an episodic-like memory paradigm using social stimuli, mice displayed intact specific memory for "what-where-when" along with increased Arc/Arg3.1 mRNA expression in the hippocampus.

    “mice displayed intact specific memory for “what-where-when” along with increased Arc/Arg3.1 mRNA expression in the hippocampus”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Fellini and Morellini, 2013

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Rats with a CA1 lesion showed deficits in a non-spatial temporal-order task when the inter-trial interval was 10 seconds, but not 3 seconds.

    “rats with the CA1 lesion showed deficits in a non-spatial temporal-order task if the inter-trial interval was 10, but not 3, seconds”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Farovik et al., 2010 source

      Not checked in the free run.

  • May combine two claims.

    Interpretationreasoning

    The CA1 processes temporal information, irrespective of whether spatial or non-spatial stimuli are involved, while the CA3 only participates in this processing if a spatial component is present.

    “These data suggest that the CA1 processes temporal information, irrespective of whether spatial or non-spatial stimuli are involved, while the CA3 only participates in this processing if a spatial component is present.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Premisecitation

    In the "directional" object exploration setting, the mossy fibers-CA3 LTD was facilitated, but not the commissural-CA3 LTD.

    “In the “directional” object exploration setting, the mossy fibers-CA3 LTD was facilitated, but not the commissural-CA3 LTD (Hagena and Manahan-Vaughan, 2011).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Hagena and Manahan-Vaughan, 2011

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    LTD was facilitated at the commissural-associational fibers in CA3 during the "positional" object exploration test, but not at the mossy fibers from the dentate gyrus projecting to the CA3.

    “Interestingly, LTD was facilitated at the commissural-associational fibers in CA3 during the “positional” object exploration test, but not at the mossy fibers from the dentate gyrus projecting to the CA3.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Hagena and Manahan-Vaughan, 2011

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Imaging data show the CA1 to be activated during both spatial and nonspatial processing, while CA3 activation codes primarily information about place.

    “Imaging data also show the CA1 to be activated during both spatial and nonspatial processing, while CA3 activation codes primarily information about place (Beer et al., 2013; Beer et al., 2014).”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites Beer et al., 2013 source

      Not checked in the free run.

    • cites Beer et al., 2014 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Chronic restraint stress disrupted neurogenesis and the when component.

    “restraint disrupted neurogenesis and the when component”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Castilla-Ortega et al., 2014 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    CA3-lesioned rats exhibited intact NOP, TOM and spatial recognition memories but were not capable of episodic-like memory in the ELM2-2 test.

    “CA3 lesioned rats exhibited intact NOP, TOM and spatial recognition memories, but were not capable of episodic-like memory in the ELM2–2 test”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Li and Chao, 2008

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Rats with temporal lobe epilepsy induced by kainate treatment exhibited impaired episodic-like memory in the ELM2-2 test along with disrupted theta coherence across CA1 and dentate gyrus.

    “Rats with temporal lobe epilepsy induced by kainate treatment exhibited impaired episodic-like memory, assessed by the ELM2–2 test, along with disrupted theta coherence across the CA1 and dentate gyrus”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Inostroza et al., 2013b

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Pre-sample infusion of CNQX or AP5 into the rat postsubiculum impaired long-term OPP but not NOP performance.

    “Pre-sample infusion of CNQX or AP5 into the rat postsubiculum also impaired long-term OPP, but not NOP, performance”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Bett et al., 2013 source

      Not checked in the free run.

  • May combine two claims.

    Interpretationcitation

    Hippocampal AMPA- and NMDA-R are important for OPP memory, while whether they account for NOP performance depends on the extent of memory load.

    “The above results suggest that the hippocampal AMPA- and NMDA-R are important for OPP memory, while whether they account for NOP performance depends on the extent of memory load.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Interpretationcitation

    The effects of vasopressin 1b are likely independent of NMDAR, as transgenic mice with selective NMDAR knockout in vasopressin 1b neurons showed intact social and object memories.

    “its effects are likely independent of NMDAR as transgenic mice with selective NMDAR knockout in vasopressin 1b neurons showed intact social and object memories”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Williams Avram et al., 2019 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Voluntary exercise improved neurogenesis and the where index of the ELM2-1 test.

    “exercise improved it and the where index of the ELM2–1 test”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Castilla-Ortega et al., 2014 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    NMDA-R GluN1 and GluN2A levels were elevated in the hippocampus but not in the PFC after habituation to an open field and exploration in the NOP sample trial, while they did not change after the NOP test.

    “NMDA-R GluN1 and GluN2A levels were elevated in the hippocampus, but not in the PFC, after habituation to an open field and exploration in the NOP sample trial, while they did not change after the NOP test”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Cercato et al., 2017 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Post-sample AP5 infusion into the hippocampus impaired OPP, while pre-test AP5 infusion had no influence.

    “Post-sample AP5 infusion into the hippocampus impaired OPP, while pre-test AP5 infusion had no influence”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Yamada et al., 2017 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Inactivation of the CA3/dentate gyrus spared the when component but not the where component.

    “inactivation of the CA3/dentate gyrus spared the when component, but not the where component”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Barbosa et al., 2012 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Transgenic mice with vasopressin 1b knockout exhibited deficient sociability and social novelty in the three-chambered social test and impaired when memory in the ELM2-1 test.

    “Transgenic mice with vasopressin 1b knockout exhibited deficient sociability and social novelty assessed by the three-chambered social test, and impaired when memory in the ELM2–1 test.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites DeVito et al., 2009 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    NOP memory and hippocampal LTP were both impaired even several weeks later by a single systemic administration of MK-801, an NMDA-R blocker, in rats.

    “NOP memory and hippocampal LTP were both impaired even several weeks later by a single systemic administration of MK-801, a NMDA-R blocker, in rats”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Wiescholleck and Manahan-Vaughan, 2013

      Not checked in the free run.

  • The quote only partly states this claim.

    Premisecitation

    Pre-sample AP5 microinjections into the hippocampus did not impair NOP.

    “but not NOP”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites Barker and Warburton, 2015

      Not checked in the free run.

    • cites Yamada et al., 2017 source

      Not checked in the free run.

  • May combine two claims.

    Interpretationcitation

    Glutamate plays an important role in hippocampal plasticity and object memory.

    “Glutamate plays an important role in hippocampal plasticity and object memory.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Interpretationcitation

    The treatment influenced consolidation of information but not retrieval processes.

    “suggesting that the treatment influenced consolidation of information, but not retrieval processes”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Yamada et al., 2017 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Post-sample hippocampal infusions of GluA23Y or G2CT that interfered with GluA2/AMPA-R removal reinstated forgotten OPP long-term memory and did not influence new OPP learning.

    “post-sample hippocampal infusions of GluA23Y or G2CT that interfered with the GluA2/AMPA-R removal, reinstated the forgotten OPP long-term memory and did not influence new OPP learning”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Migues et al., 2016 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Memory consolidation induced by contextual novelty was modulated by DA release from the locus coeruleus rather than the ventral tegmental area, dependent on hippocampal DA D1/5-R but not adrenergic-R.

    “Memory consolidation induced by contextual novelty was modulated by the DA release from the locus coeruleus, rather than ventral tegmental area, which is dependent on the hippocampal DA D1/5-R, but not adrenergic-R”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Takeuchi et al., 2016 source

      Not checked in the free run.

  • May combine two claims.

    Interpretationcitation

    Hippocampal DA D1/2-R are key for performance of location novelty but not object novelty.

    “Thus, the hippocampal DA D1/2-R are key for the performance of location novelty, but not object novelty.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Interpretationreasoning

    Hippocampal DA D1-, D2- and D3-R are involved in NOP consolidation in a bidirectional manner, while D1-R showed variable effects.

    “Thus, the hippocampal DA D1-, D2- and D3-R are involved in NOP consolidation in a bidirectional manner, while D1-R showed variable effects.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Premisecitation

    Systemic post-sample administration of fluoxetine recovered long-term OPP memory, activated Akt/GSK-3β signaling in the hippocampus and increased hippocampal LTP in mice.

    “Systemic post-sample administration of fluoxetine recovered long-term OPP memory, activated Akt/GSK-3β signaling in the hippocampus and increased hippocampal LTP in mice”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Yi et al., 2018

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    TCB-2 also enhanced hippocampal glutamate levels and the mean firing rate of CA1 neurons.

    “TCB-2 also enhanced the hippocampal glutamate levels and the mean firing rate of CA1 neurons”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Zhang et al., 2016 source

      Not checked in the free run.

  • May combine two claims.

    Interpretationcitation

    Hippocampal DA D1/5-R mediate long-term NOP memory, while their roles in OPP memory depend on the extent of memory strength.

    “The hippocampal DA D1/5-R mediate long-term NOP memory, while their roles in OPP memory are dependent on the extent of memory strength.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Premisecitation

    This facilitation effect was blocked by pre-sample trial infusions of SCH23390 but not the β-adrenergic-R antagonist propranolol into the dorsal hippocampus.

    “This facilitation effect was blocked by pre-sample trial infusions of SCH23390, but not of the β-adrenergic-R antagonist propranolol, into the dorsal hippocampus”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Kempadoo et al., 2016 source

      Not checked in the free run.

  • May combine two claims.

    Interpretationcitation

    CA1 NMDA signaling is essential for processing spatial but not temporal information in an episodic-like context.

    “This suggests that the CA1 NMDA signaling is essential for the processing of spatial, but not temporal, information in an episodic-like context.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Place et al., 2012 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Application of JWH-018, a synthetic cannabinoid 1/2-R agonist, decreased potassium-evoked glutamate and GABA release and LTP in hippocampus slices.

    “Application of JWH-018, a synthetic cannabinoid 1/2-R agonist, decreased potassium-evoked glutamate and GABA release and LTP in hippocampus slices”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites Barbieri et al., 2016 source

      Not checked in the free run.

    • cites Basavarajappa and Subbanna, 2014

      Not checked in the free run.

  • May combine two claims.

    Interpretationreasoning

    Hippocampal ACh-R play key roles in memory consolidation, with nicotinic and muscarinic ACh-R related to facilitation and disruption of mnemonic storage, respectively.

    “The hippocampal ACh-R play key roles in memory consolidation, with nicotinic and muscarinic ACh-R being related to facilitation and disruption of mnemonic storage, respectively.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Premisecitation

    In cultured hippocampal neurons, co-application of choline and NMDA/glycine caused larger currents than NMDA/glycine alone, and choline enhanced NMDA-R-mediated LTP of miniature excitatory postsynaptic currents.

    “co-application of choline and NMDA/glycine caused larger currents than the application of NMDA/glycine alone; choline enhanced NMDA-R-mediated LTP of miniature excitatory postsynaptic currents (EPSC)”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Li et al., 2013

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Long-term NOP memory was not influenced when the injection was made 160 min after the sample trial or 90 min before the test trial.

    “long-term NOP memory was also not influenced when the injection was made 160 min after the sample trial or 90 min before the test trial”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Balderas et al., 2012 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Intervention with the interaction between the nicotinic α7 ACh-R and NMDA-R blocked these effects in vitro and disrupted NOP memory in mice.

    “Intervention with the interaction between the nicotinic α7 ACh-R and NMDA-R blocked these effects in vitro, and disrupted NOP memory in mice”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Li et al., 2013

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Post-sample microinjections of scopolamine into the hippocampus disrupted NOP memory after 90 min but not 24 hours.

    “Post-sample microinjections of scopolamine into the hippocampus disrupted NOP memory after 90 min, but not 24 hours”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Balderas et al., 2012 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    CA1 infusion of the cannabinoid 1-R agonist ACEA, but not the cannabinoid 2-R agonist JWH-015 or palmitoylethanolamide, had similar effects, suggesting a role of hippocampal cannabinoid 1-R in NOP consolidation.

    “Similar effects were found by the CA1 infusion of the cannabinoid 1-R agonist ACEA, but not the cannabinoid 2-R agonist JWH-015 or palmitoylethanolamide, an endogenous fatty acid amide with affinity to cannabinoid-R GPR55 and GPR119, suggesting a role of hippocampal cannabinoid 1-R in NOP consolidation”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Clarke et al., 2008 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Application of the nicotinic α7 ACh-R agonist FRM-17874 facilitated NOP in rats and dose-dependently enhanced theta oscillation induced by electrical stimulation in the rodent hippocampus.

    “Application of the nicotinic α7 ACh-R agonist FRM-17874 facilitated NOP in rats and dose-dependently enhanced the theta oscillation induced by electrical stimulation in the rodent hippocampus”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Stoiljkovic et al., 2015 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Mice with selective knockout of cannabinoid 1-R in GABAergic neurons exhibited disruption of NOP (30 min) memory and facilitation of spontaneous IPSC in CA1 pyramidal neurons in vitro.

    “Mice with selective knockout of cannabinoid 1-R in the GABAergic neurons, exhibited disruption of NOP (30 min) memory, and facilitation of spontaneous IPSC in the CA1 pyramidal neurons in vitro”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Albayram et al., 2016 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Knockdown of cannabinoid 1-R-interacting protein 1 in the mouse hippocampus increased cell proliferation and neuroblast differentiation in the dentate gyrus and improved NOP memory.

    “knockdown of the cannabinoid 1-R-interacting protein 1 in the mouse hippocampus increased cell proliferation and neuroblast differentiation in the dentate gyrus and improved NOP memory”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Jung et al., 2017 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Infusions of scopolamine and physostigmine, an acetylcholinesterase inhibitor, into the hippocampal CA3 area impaired and enhanced spatial and object recognition, respectively.

    “infusions of scopolamine and physostigmine, an acetylcholinesterase inhibitor, into the hippocampal CA3 area impaired and enhanced spatial and object recognition, respectively”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Hunsaker et al., 2007b

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    NE modulates multiple functions, including arousal, attention, stress, and learning and memory.

    “NE modulates multiple functions, including arousal, attention, stress, and learning and memory”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites Benarroch, 2009 source

      Not checked in the free run.

    • cites Schwarz and Luo, 2015 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Pre-test infusions of scopolamine into the dorsal CA1 area did not affect NOP memory but reduced overall object exploration time.

    “Pre-test infusions of scopolamine into the dorsal CA1 area did not affect NOP memory, but reduced the overall object exploration time”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Rashid and Ahmed, 2019

      Not checked in the free run.

  • May combine two claims.

    Interpretationcitation

    Different subtypes of hippocampal 5-HT-R play distinct roles in object recognition, with 5-HT1A-, 5-HT1B- and 5-HT2A-R involved in facilitation of consolidation, while 5-HT4-R seems to impair object consolidation and/or retrieval.

    “Different subtypes of hippocampal 5-HT-R play distinct roles in object recognition, whereby 5-HT1A-, 5-HT1B- and 5-HT2A-R are involved in facilitation of consolidation, while 5-HT4-R seems to impair the processing of object consolidation and/or retrieval.”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    The locus coeruleus located in the brainstem is a cluster of adrenergic neurons that release NE across the central nervous system.

    “The locus coeruleus located in the brainstem is a cluster of adrenergic neurons that release NE across the central nervous system.”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites Benarroch, 2009 source

      Not checked in the free run.

    • cites Schwarz and Luo, 2015 source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    The G-protein-coupled cannabinoid 1-R is enriched in axonal terminals in the brain, while cannabinoid 2-R is mainly, but not exclusively, expressed in the periphery system.

    “The G-protein-coupled cannabinoid 1-R is enriched in axonal terminals in the brain, while cannabinoid 2-R is mainly, but not exclusively, expressed in the periphery system”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites Lu and Mackie, 2016

      Not checked in the free run.

    • cites Lutz et al., 2015 source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    The endocannabinoid system critically mediates development, synaptic plasticity, cognition and neuropsychiatric disorders.

    “The endocannabinoid system critically mediates development, synaptic plasticity, cognition and neuropsychiatric disorders”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites Lu and Mackie, 2016

      Not checked in the free run.

    • cites Lutz et al., 2015 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Inactivating the atypical protein kinase C isoform M zeta (PKMζ) in the dorsal hippocampus abolished memory for OPP but not NOP.

    “Inactivating the atypical protein kinase C isoform M zeta (PKMζ) in the dorsal hippocampus abolished memory for OPP, but not NOP”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Hardt et al., 2010 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    The RGS14 gene knockout mouse exhibited improved NOP memory and facilitation of LTP in the CA2 but not CA1 area.

    “The RGS14 gene knockout mouse exhibited improved NOP memory and facilitation of LTP in the CA2, but not CA1, area.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Lee et al., 2010 source

      Not checked in the free run.

  • May combine two claims.

    Interpretationcitation

    Cannabinoid 1-R in the hippocampus play distinct roles in the modulation of NOP and OPP memory, as evidenced by memory being impaired and improved through pharmacological activation and blockage of the receptor, respectively.

    “The cannabinoid 1-R in the hippocampus play distinct roles in the modulation of NOP and OPP memory, as evidenced by memory being impaired and improved through pharmacological activation and blockage of the R, respectively.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Premisecitation

    Object exploration increased expression of the immediate-early genes Nr4a1 and Nr4a2, while intra-hippocampal knockdown of either one impaired long-term OPP (24 hours) memory.

    “Object exploration also increased the expression of the immediate-early genes Nr4a1 and Nr4a2, while intra-hippocampal knockdown of either one impaired long-term OPP (24 hours) memory”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites McNulty et al., 2012 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Increased expression of BDNF in the hippocampal CA1 with transduction of AAV9-BDNF elevated phosphorylation levels of CaMKII, CREB, TrkB and p38 MAPK, and facilitated long-term OPP but not NOP memory.

    “Increased expression of BDNF in the hippocampal CA1 with the transduction of AAV9-BDNF, elevated the phosphorylation level of CaMKII, CREB, tropomyosin receptor kinase (TrkB) and p38 MAPK, and facilitated long-term OPP, but not NOP, memory”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Wang et al., 2017b

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    This effect is dependent upon the ERK/MAPK pathways, given that facilitated LTP in the CA2 was blocked by U0126, a MEK inhibitor.

    “This effect is dependent upon the ERK/MAPK pathways, given that facilitated LTP in the CA2 was blocked by U0126, a MEK inhibitor”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Lee et al., 2010 source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing), S4 (based).

    Interpretationnone given

    The functions of hippocampal neurotransmitter systems are governed by different subtypes of receptors.

    “The functions of hippocampal neurotransmitter systems are governed by different subtypes of receptors.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Interpretationnone given

    Hippocampal DA, ACh and NE bi-directionally modulate NOP and OPP memories, while glutamate, 5-HT, histamine and cannabinoids are also engaged.

    “The hippocampal DA, ACh and NE bi-directionally modulate NOP and OPP memories, while glutamate, 5-HT, histamine and cannabinoids are also engaged.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Premisecitation

    Inhibition of d-amino acid oxidase through d-serine modulation augmented NMDA-R-mediated LTP in the hippocampus ex vivo and improved long-term NOP memory in vivo.

    “inhibition of d-amino acid oxidase through d-serine modulation, augmented NMDA-R-mediated long-term potentiation (LTP) in the hippocampus ex vivo and improved long-term NOP memory in vivo”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Hopkins et al., 2013 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Post-sample hippocampal infusions of histone acetylase inhibitors decreased histone acetylation and impaired NOP memory.

    “Post-sample hippocampal infusions of histone acetylase inhibitors decreased histone acetylation and impaired NOP memory”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites Federman et al., 2013 source

      Not checked in the free run.

    • cites Zhao et al., 2012 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    A direct hippocampus-PFC pathway originates from the ventral hippocampal CA1 area and subiculum onto the mPFC, while sparse projections from the intermediate third of the hippocampus also exist.

    “A direct hippocampus-PFC pathway originates from the ventral hippocampal CA1 area and subiculum onto the mPFC, while sparse projections from the intermediate third of the hippocampus also exist”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites Cenquizca and Swanson, 2007

      Not checked in the free run.

    • cites Jay and Witter, 1991

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Expression of NF-kB and the immediate-early gene zif268 were increased after object exploration, and post-trial intra-hippocampal inhibition of NF-kB or zif268 impaired NOP memory.

    “Expression of the nuclear factor kappa B (NF-kB) and the immediate-early gene zif268 were increased after object exploration, and post-trial intra-hippocampal inhibition of NF-kB or zif268 impaired NOP memory”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Zalcman et al., 2015 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Disrupted long-term OPP but not NOP memory, along with impaired hippocampal LTP and reduced histone H2B, H3 and H4 acetylation, were found in CREB-binding protein-flox mice microinjected with AAV-Cre into the dorsal hippocampus to produce hippocampal CREB-binding protein depletion.

    “Disrupted long-term OPP, but not NOP, memory, along with impaired hippocampal LTP and reduced histone H2B, H3 and H4 acetylation, were found in the CREB-binding protein-flox mice microinjected with AAV-Cre into the dorsal hippocampus to produce hippocampal CREB-binding protein depletion”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Barrett et al., 2011 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Strong multi-synaptic (indirect pathway) connections between the mPFC and hippocampus exist, but monosynaptic projections (direct pathway) also exist.

    “There are strong multi-synaptic (indirect pathway) connections between the mPFC and hippocampus, but monosynaptic projections (direct pathway) also exist”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Rajasethupathy et al., 2015 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Longer learning of the sample trial of the NOP test increased hippocampal histone H3 acetylation and persistence of NOP memory, which could be prevented by NF-kB inhibition.

    “Longer learning of the sample trial of the NOP test increased hippocampal histone H3 acetylation and persistence of NOP memory, which could be prevented by NF-kB inhibition”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Federman et al., 2013 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Post-sample intra-hippocampus BDNF infusions compensated OPP deficits induced by anisomycin, and hippocampal BDNF infusions facilitated long-term OPP memory.

    “Post-sample intra-hippocampus BDNF infusions were found to compensate OPP deficits induced by anisomycin, and hippocampal BDNF infusions facilitated long-term OPP memory”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Ozawa et al., 2014 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    The opposite information flow was found after correct answers together with stronger alpha/beta oscillations.

    “By contrast, the opposite information flow was found after correct answers together and with stronger alpha/beta oscillations”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Brincat and Miller, 2015

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Levels of NMDA GluN1-, GluN2-, mGlu1-, mGlu2/3- and DA D1-R were higher, but GABAA-R was lower, in the ventral than dorsal hippocampus, while mGlu5-, GABAB- and DA D2-R were unchanged across the hippocampus.

    “The levels of NMDA GluN1-, GluN2-, mGlu1-, mGlu2/3- and DA D1-R were higher, but GABAA-R was lower, in the ventral than dorsal hippocampus, while mGlu5-, GABAB- and DA D2-R were unchanged across the hippocampus”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Dubovyk and Manahan-Vaughan, 2018

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    PFC-hippocampus theta oscillations were enhanced after an error made in a paired associative learning task and were primarily directed by PFC-to-hippocampus information flow.

    “the PFC-hippocampus theta oscillations were enhanced after an error made in a paired associative learning task, and were primarily directed by the PFC to hippocampus information flow”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Brincat and Miller, 2015

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    The nucleus reuniens (NR) in the medial thalamus, the perirhinal cortex and LEC are mutually connected with the PFC and hippocampus.

    “The nucleus reuniens (NR) in the medial thalamus, the perirhinal cortex and LEC are mutually connected with the PFC and hippocampus”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites Apergis-Schoute et al., 2006 source

      Not checked in the free run.

    • cites Burwell and Amaral, 1998a

      Not checked in the free run.

    • cites Hoover and Vertes, 2007 source

      Not checked in the free run.

  • May combine two claims.

    Interpretationnone given

    The intermediate and ventral hippocampus send projections to the mPFC, which presumably transfers hippocampus-relevant information to the PFC.

    “The intermediate and ventral hippocampus send projections to the mPFC, which presumably transfers hippocampus-relevant information to the PFC.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Premisecitation

    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”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Place et al., 2016 source

      Not checked in the free run.

  • May combine two claims.

    Interpretationcitation

    PFC-hippocampal projections generate oscillatory synchronization and support the concept of a directional pathway from hippocampus towards PFC as focal for information processing.

    “This illustrates that the PFC-hippocampal projections generate an oscillatory synchronization and supports the concept of a directional pathway of hippocampus towards the PFC as focal for information processing”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Siapas et al., 2005 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Ventral CA1 cells required stronger afferent stimulation to elicit action potentials, showed lower neuronal excitability and attenuated LTP induced by theta burst stimulation than dorsal CA1 cells.

    “the ventral CA1 cells required stronger afferent stimulation to elicit action potentials, showed lower neuronal excitability and attenuated LTP induced by theta burst stimulation than the dorsal CA1 cells”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Dubovyk and Manahan-Vaughan, 2018

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    The LEC-CA1 pathway is recruited for processing of exploration of familiar objects and object-recency, while the LEC-dentate gyrus-CA3 pathway is activated for processing of recognition of novel objects and object-recency.

    “the LEC-CA1 pathway is recruited for the processing of exploration of familiar objects and of object-recency, while the pathway of LEC-dentate gyrus-CA3 is activated for the processing of recognition of novel objects and for object-recency”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites Aggleton et al., 2012 source

      Not checked in the free run.

    • cites Kinnavane et al., 2014 source

      Not checked in the free run.

    • cites Olarte-Sanchez et al., 2014 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    The interplay between the mPFC and medial thalamus is critical for TOM and OiP but not NOP tests.

    “The interplay between the mPFC and medial thalamus is also critical for TOM and OiP, but not NOP, tests”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Cross et al., 2012 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    A subpopulation of single NR and LEC neurons sends axonal collaterals to both mPFC and hippocampus, implicating that the NR and LEC can directly and simultaneously modulate the activities of mPFC and hippocampus.

    “a subpopulation of single NR and LEC neurons sends axonal collaterals to both mPFC and hippocampus, implicating that the NR and LEC can directly and simultaneously modulate the activities of mPFC and hippocampus”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites Hoover and Vertes, 2012

      Not checked in the free run.

    • cites Varela et al., 2014 source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    The posterior-dorsal CA1 to PFC pathway was crucial for memory for temporal-order, but not for NOP, OPP and OiP.

    “Furthermore, the posterior-dorsal CA1 to PFC pathway was crucial for the memory for temporal-order, but not for NOP, OPP and OiP.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Barker et al., 2017 source

      Not checked in the free run.

    • The authors state this as an assumption: If two brain areas interact for a specific function, disrupting one of the areas in one hemisphere combined with a simultaneous disruption of the other area in the opposite hemisphere should lead to a functional deficit.

  • May combine two claims.

    Premisecitation

    The PFC-LEC pathway is engaged in the processing of object-associated identity, location and context information, but not in NOP, OPP and TOM.

    “This pathway is also engaged in the processing of object-associated identity, location and context information, but not in NOP, OPP and TOM (Chao et al., 2016a).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Chao et al., 2016a

      Not checked in the free run.

  • May combine two claims.

    Interpretationreasoning

    Disconnecting the PFC-CA1 and PFC-CA3 pathways revealed differential effects on episodic-like memory, indicating distinct functional roles of the PFC-CA1 versus -CA3 pathways.

    “Disconnecting the PFC-CA1 and PFC-CA3 pathways revealed differential effects on episodic-like memory, indicating distinct functional roles of the PFC-CA1 versus -CA3 pathways.”
    Quote in the paperSubstantial claim
    • The authors state this as an assumption: If two brain areas interact for a specific function, disrupting one of the areas in one hemisphere combined with a simultaneous disruption of the other area in the opposite hemisphere should lead to a functional deficit.

  • May combine two claims.

    Premisecitation

    Retrieval of OiP memory was dependent on the PFC-hippocampus AMPA-R, but not NMDA-R.

    “Retrieval of OiP memory was dependent on the PFC-hippocampus AMPA-R, but not NMDA-R (Barker and Warburton, 2015).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Barker and Warburton, 2015

      Not checked in the free run.

    • The authors state this as an assumption: If two brain areas interact for a specific function, disrupting one of the areas in one hemisphere combined with a simultaneous disruption of the other area in the opposite hemisphere should lead to a functional deficit.

  • May combine two claims.

    Premisecitation

    NR-lesioned rats exhibited intact NOP, OPP and short-term OiP memories, but long-term OiP memory was impaired.

    “The NR-lesioned rats exhibited intact NOP, OPP and short-term OiP memories, but long-term OiP memory was impaired.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Barker and Warburton, 2018

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    In the ELM4-2 test, inactivation of the posterior-dorsal CA1 to PFC pathway impaired the when, but not where, component of episodic-like memory, while inactivation of the intermediate CA1-PFC pathway disrupted the where, but not when, component.

    “In the ELM4–2 test, inactivation of the posterior-dorsal CA1 to PFC pathway impaired the when, but not where, component of episodic-like memory, while inactivation of the intermediate CA1-PFC pathway disrupted the where, but not when, component.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Barker et al., 2017 source

      Not checked in the free run.

    • The authors state this as an assumption: If two brain areas interact for a specific function, disrupting one of the areas in one hemisphere combined with a simultaneous disruption of the other area in the opposite hemisphere should lead to a functional deficit.

  • May combine two claims.

    Premisecitation

    The intermediate CA1 to PFC pathway was important for OiP memory, but not for NOP, OPP and temporal-order.

    “In contrast, the intermediate CA1 to PFC pathway was important for OiP memory, but not for NOP, OPP and temporal-order.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Barker et al., 2017 source

      Not checked in the free run.

    • The authors state this as an assumption: If two brain areas interact for a specific function, disrupting one of the areas in one hemisphere combined with a simultaneous disruption of the other area in the opposite hemisphere should lead to a functional deficit.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Recent human imaging studies show distinct but complementary characteristics of CA1 and CA3 in episodic memory.

    “Recent human imaging studies shed light on the distinct but complementary characteristics of CA1 and CA3 in episodic memory (Copara et al., 2014; Dimsdale-Zucker et al., 2018).”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites Copara et al., 2014 source

      Not checked in the free run.

    • cites Dimsdale-Zucker et al., 2018 source

      Not checked in the free run.

  • May combine two claims.

    Interpretationreasoning

    Although the CA1-PFC pathway was preserved, episodic-like and associated spatial memories were still impaired, highlighting the role of the interplay between the PFC and CA3 in the processing of episodic information.

    “These results reveal that, although the CA1-PFC pathway was preserved, episodic-like and associated spatial memories were still impaired, which highlights the role of the interplay between the PFC and CA3 in the processing of episodic information.”
    Quote in the paperSubstantial claim
    • The authors state this as an assumption: If two brain areas interact for a specific function, disrupting one of the areas in one hemisphere combined with a simultaneous disruption of the other area in the opposite hemisphere should lead to a functional deficit.
179 of 179

  • The paper relies on this without support.

    All behaviors are motivated and guided by positive and negative outcomes (reinforcers).

    “However, all behaviors are “motivated” and guided by positive and negative outcomes (reinforcers).”

  • The authors state this as an assumption.

    The methodological factors in the NOP test apply to the TOM test.

    “The methodological factors in the NOP test are suggested to apply to the TOM test as well.”

  • The paper relies on this without support.

    The TOM test is designed for animals to remember both sets of objects while forming differential memory decay for each one.

    “The TOM test is designed for animals to remember both sets of objects, while forming differential memory decay for each one.”

  • The paper relies on this without support.

    The rodent behavioral tasks used in the cited studies (NOP, OPP, ELM2-1, ELM2-2, etc.) validly measure the cognitive constructs they are said to measure, including episodic-like memory.

    “episodic-like memory”

  • The authors state this as an assumption.

    If two brain areas interact for a specific function, disrupting one of the areas in one hemisphere combined with a simultaneous disruption of the other area in the opposite hemisphere should lead to a functional deficit.

    “The basic proposition of the disconnection approach is that, if two brain areas interact for a specific function, disrupting one of the areas in one hemisphere combined with a simultaneous disruption of the other area in the opposite hemisphere (i.e. disconnecting the circuit at two different levels) should lead to a functional deficit.”

  • The authors state this as an assumption.

    An impairment of one of the components (what, where, when) should cause a failure of episodic memory.

    “given that, by logic, an impairment of one of the components should cause a failure of episodic memory.”
6 of 6

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • The mPFC has an integrative role in object, place and time information.

    “The mPFC has an integrative role in object, place and time information [114, 115] as well as reward-regulated mechanisms of spatial learning [116, 117].”

    From The extracellular matrix and perineuronal nets in memory (2022) · cites this paper as [114]

  • Damage to the hippocampus is associated with defects in episodic-related memory functions in monkeys and rodents.

    “research in these studies shows that damage to the hippocampus is associated with defects in episodic-related memory functions in monkeys [112] and rodents [66,113,114].”

    From Is episodic-like memory <i>like</i> episodic memory? (2024) · cites this paper as [66]

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

Each contradiction between two passages listed here was confirmed by an independent check.

  • Rat retention claim cites a mouse study

    Minor

    The claim attributes retention for over two hours in rats to Belblidia et al. (2015), but the cited reference describes a study in mice.

  • Conflicting claims about prefrontal NMDA receptors in object-place learning

    Minor

    One passage says prefrontal NMDA receptors are indispensable for encoding object-location relationships and for learning OiP memory. A later passage says they are not essential for learning object-place associations.

2 of 2

Cites

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Related

Authors
Chao, O. Y., de Souza Silva, M. A., Yang, Y.-M., & Huston, J. P.
Affiliations
  • University of Minnesota (US)
  • Heinrich Heine University Düsseldorf (DE)
Corresponding author
  • Yang, Yi-Mei
  • Huston, Joseph P.
ORCID
Venue
Neuroscience & Biobehavioral Reviews
Publisher
Elsevier BV
Published
2020-06
Volume
113
Pages
373-407
ISSN
0149-7634 (ISSN-L)
DOI
10.1016/j.neubiorev.2020.04.007
PMC
PMC7302494
OpenAlex
W3015373542
Semantic Scholar
572bae24f9319a147be915b0ff86782fa9bdc65f
Cited by
158
References
447
Citations by year
2026: 23 · 2025: 23 · 2024: 29 · 2023: 22 · 2022: 33 · 2021: 22 · 2020: 6
FWCI
2.80
Type
journal article
Language
en
Open access
Licence
Locations
  • Neuroscience & Biobehavioral Reviews (publishedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
Funders
Heinrich-Heine-Universität Düsseldorf
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Keywords
medial prefrontal cortex, hippocampus, entorhinal cortex, episodic-like memory, object memory, spatial memory, temporal memory, memory circuits, top-down control, neurotransmitter systems, rodents
MeSH terms
Animals, Exploratory Behavior, Hippocampus, Neural Pathways, Rodentia, Prefrontal Cortex, Recognition, Psychology, Mice, Rats, Memory, Episodic

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Claims read by deepseek-v4.1-flash under definition version 3 (extract-v3) on 2026-10-09.

Classified by jev-1.13-20260917 (gold-guideline-v0.2) on 2026-10-09.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

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